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Lectins are carbohydrate binding (glyco)proteins which are ubiquitous in nature. In plants, they are distributed in various families and hence ingested daily in appreciable amounts by both humans and animals. One of the most nutritionally important features of plant lectins is their ability to survive digestion by the gastrointestinal tract of consumers. This allows the lectins to bind to membrane glycosyl groups of the cells lining the digestive tract. As a result of this interaction a series of harmful local and systemic reactions are triggered placing this class of molecules as antinutritive and/or toxic substances. Locally, they can affect the turnover and loss of gut epithelial cells, damage the luminal membranes of the epithelium, interfere with nutrient digestion and absorption, stimulate shifts in the bacterial flora and modulate the immune state of the digestive tract. Systemically, they can disrupt lipid, carbohydrate and protein metabolism, promote enlargement and/or atrophy of key internal organs and tissues and alter the hormonal and immunological status. At high intakes, lectins can seriously threaten the growth and health of consuming animals. They are also detrimental to numerous insect pests of crop plants although less is presently known about their insecticidal mechanisms of action. This current review surveys the recent knowledge on the antinutritional/toxic effects of plant lectins on higher animals and insects.
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Antinutritional properties of plant lectins
Ilka M. Vasconcelos*, Jose
´Tadeu A. Oliveira
Departamento de Bioquı
´mica e Biologia Molecular, Universidade Federal do Ceara
´, Caixa Postal 6020,
Campus do Pici, CEP 60451-970, Fortaleza, CE, Brazil
Available online 2 June 2004
Lectins are carbohydrate binding (glyco)proteins which are ubiquitous in nature. In plants, they are distributed in various
families and hence ingested daily in appreciable amounts by both humans and animals. One of the most nutritionally important
features of plant lectins is their ability to survive digestion by the gastrointestinal tract of consumers. This allows the lectins to
bind to membrane glycosyl groups of the cells lining the digestive tract. As a result of this interaction a series of harmful local
and systemic reactions are triggered placing this class of molecules as antinutritive and/or toxic substances. Locally, they can
affect the turnover and loss of gut epithelial cells, damage the luminal membranes of the epithelium, interfere with nutrient
digestion and absorption, stimulate shifts in the bacterial flora and modulate the immune state of the digestive tract.
Systemically, they can disrupt lipid, carbohydrate and protein metabolism, promote enlargement and/or atrophy of key internal
organs and tissues and alter the hormonal and immunological status. At high intakes, lectins can seriously threaten the growth
and health of consuming animals. They are also detrimental to numerous insect pests of crop plants although less is presently
known about their insecticidal mechanisms of action. This current review surveys the recent knowledge on the
antinutritional/toxic effects of plant lectins on higher animals and insects.
q2004 Elsevier Ltd. All rights reserved.
Keywords: Plant lectins; Antinutritional effects; Higher animals; Insects
1. Introduction ................................................................... 385
2. Lectins in plant foods ............................................................ 386
3. Oral toxicity of plant lectins to higher animals.......................................... 387
4. Resistance of lectins to proteolysis .................................................. 388
5. Effects of lectins on the digestive tract ............................................... 389
6. Systemic effects of dietary lectins ................................................... 390
7. Insecticidal properties of plant lectins ................................................ 393
8. Conclusions ................................................................... 397
References ....................................................................... 397
1. Introduction
Plant lectins were originally detected by the medical
student Stillmark (1888), in Dorpat/Estonia when he was
working on his dissertation thesis on castor beans (Ricinus
communis L.). At this time he described the presence of a
toxic proteinaceous factor in extracts from castor beans
which also agglutinated red blood cells. To indicate the
source in which it had been found the name ricin was
adopted. Thus, historically, this fact is considered the true
starting point of the research on plant lectins (Ru
1998). The term lectin (legere ¼Latin verb for to select)
was coined by Boyd many years later to emphasise the
ability of some hemagglutinins to discriminate blood cells
within the ABO blood group system (Boyd and Reguera,
1949; Boyd and Shapleigh, 1954). Presently, the term lectin
is prevalent over that of hemagglutinin and is broadly
0041-0101/$ - see front matter q2004 Elsevier Ltd. All rights reserved.
Toxicon 44 (2004) 385–403
*Corresponding author. Fax: þ55-85-288-9789.
E-mail address: (I.M. Vasconcelos).
employed to denote ‘all plant proteins possessing at least
one non-catalytic domain, which binds reversibly to a
specific mono- or oligosaccharide’ (Peumans and Van
Damme, 1995). Alternatively, lectins are also defined as
‘proteins or glycoproteins of non-immune origin with one or
more binding sites per subunit, which can reversibly bind to
specific sugar segments through hydrogen bonds and
Van Der Waals interactions’ (Lis and Sharon, 1998). Both
these definitions are very comprehensive and include non-
agglutinating and some enzyme proteins (Van Damme et al.,
1998) such as the class I plant chitinase, considered as a
lectin because its single carbohydrate-binding domain is
structurally distinct of its catalytic site and does not directly
participate in the chitinolytic activity of this enzyme
(Peumans and Van Damme, 1994). Obviously, chitinases
cannot be called as agglutinins or phytohemagglutinins
since they do not possess agglutination and/or glycoconju-
gate precipitation properties, as they are not multivalent
carbohydrate-binding proteins. Another class of plant
proteins which are also considered as lectins, according to
the above definitions, are the type 2 RIPs (ribosome-
inactivating proteins). Ricin, abrin and modeccin are well
known examples of two-chain RIPs which irreversibly
inactivate ribosomes by removing a specific adenine from a
highly conserved tetranucleotide‘GA
GA’loop present in
28 S RNA of the large ribosomal subunit (Endo and Tsurugi,
1987; Barbieri et al., 1993). The high toxicity of these
proteins to living cells is associated to the A chain which
possesses the enzymatic RNA-N-glycosidase domain but it
is the carbohydrate-binding or lectin domain in the B chain
which interacts with cell surface sugar receptors, mediating
endocytosis of type 2 RIPs, an essential event that precedes
cellular toxicity (Barbieri et al., 1993; Peumans and Van
Damme, 1994; Olsnes et al., 1999).
Considering the overall structure of plant lectins they are
subdivided into four major classes: Merolectins which are
proteins having a single carbohydrate-binding domain;
Hololectins, comprising all lectins having di- or multivalent
carbohydrate-binding sites; Chimerolectins, proteins con-
sisting of one or more carbohydrate-binding domain(s) plus
an additional catalytic or another biological activity
dependent on a distinct domain other than the carbo-
hydrate-binding site; and Superlectins which also possess at
least two carbohydrate-binding domains but differ from the
hololectins because their sites are able to recognise
structurally unrelated sugars (Van Damme et al., 1998).
Although plant lectins are considered a very complex and
heterogeneous group of proteins at the biochemical/
physicochemical viewpoint, sequence, structural infor-
mation and molecular cloning of lectin genes enable
subdivision of plant lectins in seven families of structurally
and evolutionary related proteins: legume lectins; chitin-
binding lectins; type 2 RIP and related lectins; monocot
mannose-binding lectins; jacalin-related lectins; amaranthin
lectin family and cucurbit phloem lectins (reviewed in Van
Damme et al., 1998; Murdock and Shade, 2002).
Plant lectins are also subdivided into five groups, according
to the monosaccharide for which they exhibit the highest
affinity: D-mannose/D-glucose, D-galactose/N-acetyl-D-
galactosamine, N-acetyl-D-glucosamine, L-fucose and N-
acetylneuraminic acid (Goldstein et al., 1997). Thus
depending on the specificity toward a given monosaccharide
the lectin will selectively bind to one of these above sugars
which are typical constituents of eukaryotic cell surfaces
(Lis and Sharon, 1998). In regard to their localisation, plant
lectins are generally most abundant in the seeds but they are
also found in different vegetative tissues such as in roots,
leaves, barks, flowers, bulbs and rhizomes (Broekaert et al.,
1987; Peumans et al., 1997; Ratanapo et al., 1998; Van
Damme et al., 2000).
The wide distribution of lectins in all tissues of plants
and their ubiquitous presence in the plant kingdom suggest
important roles for these proteins. One possible physiologi-
cal function that has emerged is the defensive role of these
carbohydrate-binding proteins against phytopathogenic
microorganisms, phytophagous insects and plant-eating
animals (Chrispeels and Raikhel, 1991; Harper et al.,
1995; Gatehouse et al., 1995). Indeed it has been shown
that plant lectins possess cytotoxic, fungitoxic, anti-insect
and anti-nematode properties either in vitro or in vivo and
are toxic to higher animals (Oliveira et al., 1994; Peumans
and Van Damme, 1995; Oka et al., 1997; Ripoll et al., 2003).
For example, the toxic effects of PHA, the lectin from
Phaseolus vulgaris, on monogastric animals are well
documented (Pusztai, 1991; Pusztai et al., 1995), and the
expression in transgenic plants of genes encoding for the
lectins GNA (from Galanthus nivalis; snowdrop), PSA
(Pisum sativum; pea), WGA (Triticum vulgare; wheatgerm),
ConA (Canavalia ensiformis; jack bean), AIA (Artocarpus
integrifolia; jack fruit), OSA (Oriza sativa; rice) and UDA
(Urtica dioica; stinging nettle) resulted in added protection
against insect pests and/or phytopathogenic nematodes or
fungi (Hilder et al., 1995; Does et al., 1999; Hilder and
Boulter, 1999; Powell, 2001; Ripoll et al., 2003).
One of the most important features of plant lectins,
compatible with the proposed defensive function, is the
remarkably high resistance to proteolysis and stability over
a large range of pH, even when they are out of their natural
2. Lectins in plant foods
Plants offer an enormous variety of macro- and
micronutrients necessary for heterotrophs such as microbes
and plant-eating organisms including nematodes, insects,
various other invertebrates and higher animals. Food for
human consumption is derived either from plant sources or
from animals. Animals themselves are ultimately dependent
upon plants for their survival. As lectins are present in the
most commonly edible plant foods such as tomato, potato,
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403386
beans, peas, carrots, soybeans, cherries, blackberries, wheat
germ, rice, corn, garlic, peanuts, mushrooms, avocado,
beetroot, leek, cabbage, tea, parsley, oregano, spices and
nuts, and also in several non-cultivated plant species
(Nachbar and Oppenheim, 1980; Liener, 1986; Gupta and
Sandhu, 1998; Oliveira et al., 2000; Leontowicz et al.,
2001), the exposure of heterotroph organisms, including
human beings, to functionally active lectins is a common
event. Actually, the presence of nutritionally significant
amounts of active lectins in fresh and processed foods and
the lack of public knowledge concerning the deleterious
effects of dietary lectins on the gut and health have led to a
number of outbreaks of food poisoning. For example, Noah
et al. (1980) reported seven incidents involving 43 persons
in which the poisonings were attributed to toxins present in
uncooked or partially cooked kidney beans (Phaseolus
vulgaris). In 1981, a television programme by BBC cited a
total of 330 outbreaks of kidney bean food poisonings
involving 880 people (Bender and Reaidi, 1982). In 1988, a
hospital launched a ‘healthy eating day’ in its staff canteen
at lunchtime. One dish contained red kidney beans and 31
portions were served. Between 3 and 7 pm, 11 customers
suffered from profuse vomiting and some diarrhoea. No
pathogens were isolated from the food, but the beans
contained abnormally high concentration of PHA (Gilbert,
1988). These examples all relate to kidney bean. However, it
is possible that there have been problems with other lectin-
containing foods that have not been reported.
3. Oral toxicity of plant lectins to higher animals
As already mentioned, the knowledge that some lectins
are toxic to animals dates back to 1888, when Stillmark
published his work on the deleterious effects of a
proteinaceous substance present in castor bean. Soon after
similar toxic substances were discovered in the seeds of
Croton triglium (crotin) and Abrus precatorius (abrin) and
in the bark of Robinia pseudoacacia (robinia) (Van Damme
et al., 1998). With the increasing interest on lectins
heightened particularly from the discovery of blood group
specificity (Renkonnen, 1948; Boyd and Reguera, 1949) and
from the realisation that PHA induced mitosis in mature,
non-dividing human lymphocytes (Nowell, 1960), many
other lectins were identified and isolated. Some of these
were found to be toxic or antinutritional for man and
animals. In general, nausea, bloating, vomiting and
diarrhoea characterize the oral acute toxicity of lectins on
humans exposed to them. In experimental animals fed on
diets containing plant lectins the evident symptoms are loss
of appetite, decreased body weight and eventually death
(Liener et al., 1986; Duranti and Gius, 1997; Lajolo and
Genovese, 2002). The mechanisms by which lectins mediate
toxicity and the characteristic which dictate whether a lectin
will be deleterious or not are not completely understood.
Nevertheless, from a nutritional viewpoint, it is important to
find ways of identifying which lectin is and which is not
As an attempt to predict the oral toxicity of lectins using
small amounts of sample toward minimising costs and
reducing the experimental time, many lectins were tested for
toxicity by intradermal or intraperitoneal administration in
rats and mice (Liener, 1986, 1994; Reynoso-Camacho et al.,
2003). From these studies it emerged that whilst most
parentally toxic lectins were also orally toxic, a few
exhibited no oral toxicity. Contrarily some parenterally
non-toxic lectins were highly toxic when orally adminis-
tered. Therefore, intradermal or intraperitoneal tests
designed to evaluate oral toxicity are not a reliable predictor.
Furthermore, parenteral administration is not the common
route by which animals are exposed to dietary lectins. Data
currently available indicate that multiple exposure and long-
term studies may be also needed to address lectin toxicity
(Grant et al., 2000).
The ability of lectins to selectively bind to different types
of blood cells has also been proposed as a means to predict
oral toxicity of these proteins. It has been suggested that the
hemagglutinating ability could form a basis for in vitro
screening of potentially toxic lectins. Thus, lectins which
strongly agglutinate a wide range of different red blood cells
should generally have high oral toxicity for rats, whereas
those agglutinating only rabbit and/or enzyme-treated rat
erythrocytes should not (Grant et al., 1983, 1995). However a
lack of a significant number of assays to firmly establish such
relationship together with exception to this rule found for
several lectins such as the Cratylia argentea lectin (CAA)
which strongly agglutinates a wide range of erythrocytes
being essentially non-toxic (Rios et al., 1996), mean that this
approach is not a reliable predictor. As with intradermal and
intraperitoneal toxicity studies, this procedure cannot be used
alone to predict which lectin will or will not have deleterious
effects when consumed orally. In fact, the unique reliable
way of predicting the oral toxicity of lectins is by feeding the
target animal on diets containing the purified lectin. More-
over, it is important to carry out these tests on several
different animal species and not just on rats and mice.
Accordingly, kidney beans induced pancreas growth in
chicks but not in pigs (Huisman et al., 1990a,b). Recently,
Douglas et al. (1999) detected that SBA (Glycine max;
soybean agglutinin) accounted for approximately 15% of the
growth depression from raw soybeans in chicks, whereas
Liener (1953) estimated that lectins accounted for approxi-
mately 50% of the growth-inhibiting effect of raw soybean
meal in rats. In addition, it has been considered that the
degree to which some lectins affect metabolism is, in part,
dependent on dietary history of the animal and the exact
composition of the diet (Grant, 1999). However, it is
impractical to test all lectins under all circumstances in
vivo. To establish a screening system, it is thus important to
develop a clear picture of the properties of specific lectins that
lead them to be toxic to man and animals.
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 387
4. Resistance of lectins to proteolysis
Plant proteins are generally regarded as more resistant
to proteolysis than most proteins of animal origin (Fried-
man, 1996; Sgarbieri, 1996; El-Adawy, 2002). Indeed, the
apparent digestibility of proteins in vivo from leguminous
seeds and oilseeds in their raw state varies from 15.6% to
about 80% depending upon the origin (Grant et al., 1995;
Carbonaro et al., 2000; Preet and Punia, 2000; Cuadrado
et al., 2002). In contrast, animal proteins, such as egg
albumin or casein, are 85 94% digestible in vivo (Oliveira
et al., 1994; Vasconcelos et al., 2001). Many plant lectins
in particular have been found to be resistant to degradation
by proteases in vitro (Carbonaro et al., 1997) and in the gut
in vivo (Pusztai, 1991). This may in fact be a common
feature of this class of proteins. PHA (Pusztai et al., 1979;
Hara et al., 1984), ConA (Nakata and Kimura, 1985),
ConBr (Canavalia brasiliensis)(Oliveira et al., 1994),
CAA (Oliveira et al., unpublished data), PTA (Psopho-
carpus tetragonolobus; winged bean) (Higuchi et al.,
1983), LEA (Lycopersicon esculentum; tomato) (Kilpatrick
et al., 1985), GNA, SBA, WGA, PSA, SNA-I, SNA-II
(Sambucus nigra; elderberry), VFL (Vicia faba; broad
bean) and DGL (Dioclea grandiflora; mucuna) (Pusztai,
1991; Bardocz et al., 1995) were all showed to be resistant
to in vivo breakdown by proteolytic enzymes. The extent
of the in vivo lectin resistance to degradation by the gut
enzymes was variable but in some cases it reached very
high values. For instance, in one trial with rats fed on
known amounts of intragastrically administered pure
lectins, the feces were found to contain (by ‘rocket
immunoelectrophoresis’) over 90% of the ingested PHA,
ConA and GNA in a form still fully reactive towards rabbit
anti-lectin antibodies (Pusztai, 1991). Of a particular
interest is the finding that biologically intact WGA was
detected in ileostomy effluent and fecal collections from
human subjects consuming a diet containing wheat germ
(Brady et al., 1978). These observations demonstrated that
PHA, ConA, GNA and WGA transverse the rat and human
small intestine, respectively, intact. Conceivably orally
ingested plant lectins remaining at least partially undi-
gested in the gut may bind to a wide variety of cell
membranes and glycoconjugates of the intestinal and
colonic mucosa leading to various deleterious effects on
the mucosa itself as well as on the intestinal bacterial flora
and other inner organs (Ru
¨diger, 1998).
It is also noteworthy that far less of the lectins survive the
in vitro treatment with proteolytic enzymes (Rios et al.,
1996). This was the case for ConBr, CAA and DGL, all
glucosemannose specific lectins, which were digested to a
far higher extent (52 84%) than in vivo. Thus, it is possible
that in the gut the lectins may even be protected from
proteolytic degradation during gut passage perhaps as a result
of binding to epithelial or lumenal gut components. The slight
protection from proteolytic degradation in vitro conveyed by
adding glucose, Ca
and Mn
to the reaction mixture is
consistent with this possibility. Nevertheless, as a result of
high resistance to proteolytic degradation in vivo nutrition-
ally significant amounts of certain dietary lectins will survive
in an intact and highly reactive form within the gut lumen.
Obviously this is crucial for them to exhibit the full
spectrum of their biological activities on animals (Fig. 1).
Fig. 1. Spectrum of biological activities of plant lectins on higher animals.
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403388
Thus the deleterious effects of lectins depend definitively on
the degree of lectin resistance to proteolytic degradation
(Caygill, 1999).
5. Effects of lectins on the digestive tract
As most lectins are not degraded during their passage
through the digestive tract they are able to bind the epithelial
cells which express carbohydrate moieties recognised by
them. This event is undoubtedly the second one in
importance for determining the toxicity of orally fed lectins.
Indeed, lectins which are not bound by the mucosa usually
induce little or no harmful antinutritive effect for the
consumers (Pusztai and Bardocz, 1996). Once bound to
the digestive tract, the lectin can cause dramatic changes in
the cellular morphology and metabolism of the stomach and/
or small intestine and activate a cascade of signals which
alters the intermediary metabolism. Thus, lectins may induce
changes in some, or all, of the digestive, absorptive,
protective or secretory functions of the whole digestive
system and affect cellular proliferation and turnover. In 1960,
´suggested that the toxic effects of ingested lectins were
due to their ability to combine with specific receptor sites of
the cells lining the small intestine and to cause a non-specific
interference with absorption and nutrient utilisation (Jaffe
1960). Many observations either in vivo or in vitro support
´’s hypothesis (Oliveira et al., 1988; Hajos et al., 1995).
PHA was also able to attach to gastric mucosal and parietal
cells inhibiting the gastric acid secretion in conscious rats
´s et al., 2000, 2001). Additionally, PHA-treated pigs
showed an increase in stomach weights and mucosa thickness
(Radberg et al., 2001). In fact, if appropriate carbohydrate
moieties are expressed on the surface of any structure or
organ, lectins will be able to bind to them (Pusztai, 1991;
Jordinson et al., 1997; Otte et al., 2001; Bryk and Gheri,
2002). Moreover, in rats some lectins appeared to progress-
ively mediate changes in the glycosylation of the gut leading
to an increase in the binding sites to which they could attach
(Pusztai et al., 1995). As the glycosylation state of the gut
among higher animals shows many similarities it is plausible
to suppose that the adverse effects of dietary lectins observed
on experimental animals will be comparable in human
beings. Obviously the severity of these adverse effects will
depend on the gut region to which the lectin will bind
(Baintner et al., 2000).
Many lectins either directly or indirectly cause profound
morphological and physiological modifications in the small
intestine. Such alterations characteristically lead to
increased shedding of brush border membranes, accelerated
cell-loss and shortened, sparse and irregular enterocyte
microvilli (Pusztai, 1991; Bardocz et al., 1995; Herzig et al.,
1997). In fact, binding of lectins to the gut epithelium is
frequently accompanied by disruption of the brush borders
and disorganisation of the main absorptive cells, which
cause reduction in the absorptive surface area and absorp-
tion of nutrients. One result of this is cellular hyperplasia
and increased endogenous secretion leading to large
increases in the small intestinal weight of rats fed lectins
(Otte et al., 2001; Sasaki et al., 2002). Actually some lectins
have been shown to trigger notable trophic effects on the
intestine. PHA and PNA consistently reversed the fall in
gastrointestinal and pancreatic growth associated with total
parenteral nutrition by stimulating the release of specific
hormones, such as gastrin, cholecystokinin (CCK) and
enteroglucagon (Jordinson et al., 1999). Parenteral admin-
istration of ConA significantly elevated epithelial cell
proliferation in the rat intestine (Fitzgerald et al., 2001).
Regardless of the precise nature of the initial response by the
small intestinal cells to the growth signal, it is clear that
there is an obligatory accumulation of polyamines, such as
putrescine, spermidine and spermine, in small crypts
(Pusztai, 1991; Bardocz et al., 1996). This is followed by
secondary responses, which include increased DNA, RNA,
protein and carbohydrate tissue contents (Pusztai et al.,
1988; Bardocz et al., 1995). Increased rat small intestinal
weight has also been related to SBA, ConA, ConBr, WGA
and PNA (peanut agglutinin) (Pusztai, 1991; Grant, 1991,
1999). A dramatic dose-dependent hyperplastic growth of
the small intestine was also observed by oral administration
of ML-1 (Viscum album; mistletoe lectin), probably due to
the avid binding and endocytosis of this lectin by gut
epithelial cells (Pusztai et al., 1998). In contrast, no weight
effect was found for the small intestine in the PHA-treated
pigs. However, morphometric analyses of the small intestine
of these animals showed a decrease in villus heights, an
increase in crypt depths and crypt cell mitotic indices, fewer
vacuolated enterocytes per villus and reduced vacuole size.
Additionally, a decrease in the absorption of different-sized
marker molecules after gavage feeding and a decrease in
intestinal marker permeability were observed (Radberg
et al., 2001). PHA also induces growth of the large intestine
(Bardocz et al., 1995). Nevertheless, in this digestive tract
section the changes were much less marked than those
observed in the small intestine (Grant, 1999).
In addition to the disruptive effects on cell membrane,
lectins have been shown to inhibit various intestinal and
brush border enzymes. A non-competitive inhibition of
enterokinase from rat duodenal brush borders was observed
in vitro in the presence of ConA, PHA or SBA, PHA being
the most potent inhibitor (Rouanet et al., 1983). PHA also
interacted and inhibited brush border dipeptidase in vitro
(Erickson et al., 1985). Sucrose, maltase, alkaline phospha-
tase, leucine aminopeptidase and g-glutamyltransferase, all
suffered a significant decrease in activities by inclusion of
PTA in a basal diet offered to rats (Higuchi et al., 1984).
RCA (R. communis), PHA and UEA interacted with various
human small intestine brush-border hydrolases such as
sucrase, isomaltase, maltase glucoamylase, lactase, neutral
and acid aminopeptidases and dipeptidyl peptidase IV
(Triadou and Audran, 1983). PHA decreased the hydrolysis
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 389
of casein, bovine serum albumin and heat-treated bean
extract by pepsin and pancreatin (Thompson et al., 1986).
The insecticidal GNA given to pathogen-free rats increased
the activities of the brush border enzymes alkaline
phosphatase and aminopeptidase whereas sucrase isomal-
tase activity was nearly halved (Pusztai et al., 1996). ASA,
the lectin from edible garlic (Allium sativum), induced
increased activities of disaccharidases and acid phosphatase
in the rat jejunum whereas the activities of alkaline
phosphatase, lactate dehydrogenase and adenosine tripho-
sphatase were lower (Gupta and Sandhu, 1998). Thus, the
well established lectin-induced disruption of intestinal
microvilli combined with the in vivo inhibitory effects on
gut enzymes suggest that the lectins interfere, either directly
or indirectly, not only with the utilisation of dietary protein
and carbohydrate but also with the initial and final stages of
protein/carbohydrate digestion and transport.
An additional secondary toxic effect of undigested
lectin, particularly PHA, in the small intestine which may
further reduce the efficiency of digestion and absorption
of food is a dramatic overgrowth of coliform bacteria
(Wilson et al., 1980; Pusztai et al., 1993a; Bardocz et al.,
1996). The mechanism by which lectins promote
proliferation of coliforms, mainly Escherichia coli,is
not fully understood. However, it has been established
that in relation to PHA, the bacterial proliferation arises
primarily as a result of its effects on epithelial cell
metabolism (Pusztai, 1991; Pusztai et al., 1995). Indeed
PHA-mediated mucus secretion, epithelial cell loss,
serum protein leakage and reduced digestion of dietary
protein possibly further aid bacterial proliferation by
providing a good source of nutrients (Grant, 1999). In
consequence, the increase in bacterial numbers in the
small intestine may lead to overproduction of bacterial
toxins which also contributes to the worsening of animal
Although almost all the theory about the general
deleterious effects of dietary lectins on animals was built
from various comprehensive studies carried out with PHA,
other lectins showed some similar effects. We showed that
ConBr, a lectin from Canavalia brasiliensis, which shares
90% amino acid sequence similarity with ConA (Grangeiro
et al., 1997), inhibited rat growth probably through
interference in the metabolism as elevated losses of
nitrogen and dry matter in the feces and lower retention
of ingested nitrogen were observed (Oliveira et al., 1994).
Recently, we observed that another ConA related lectin,
CAA (Cratylia argentea agglutinin), interacted with the
epithelium of duodenum, jejunum and ileum of rats fed on
diets containing the C. argentea seed meal or CAA at 2%
protein level. CAA-binding to the cells lining the gut
lumen (Fig. 2) may have significantly impaired nutrient
absorption which led to a reduced body weight gain in such
animals, higher fecal and nitrogen outputs and lower
nutritional parameters.
6. Systemic effects of dietary lectins
High rates of internalisation of dietary lectins by
enterocytes after binding to the small intestine cells appear
to be a common event (Pusztai, 1991; Bardocz et al., 1995).
Lectins, which bind to epithelial cells, may be taken up into
cells by endocytosis, be released by exocytosis into the
intracellular space from where they are subsequently
transported throughout the body. As a result, reactive
forms of the lectins are distributed in the circulation and
internal tissues and may lead to deleterious systemic effects.
For instance, the N-acetylglucosamine-specific agglutinins,
WGA, UDA and DSA (Datura stramonium; thorn apple),
when offered to rats at the level of 7 g/kg diet, bound to and
were endocytosed by the epithelial cells of the small
intestine (Pusztai et al., 1993b). An appreciable portion of
the endocytosed WGA, the most damaging amongst the
three lectins tested, was transported across the gut wall into
the systemic circulation where it was deposited in the walls
of the blood and lymphatic vessels (Pusztai et al., 1993b).
PHA was found to induce a powerful, selective humoral
response of the IgG-type when raw beans were fed to rats
Fig. 2. Light micrograph (600 £) of a duodenum villus of a rat fed
for 10 days on a diet containing 2% Cratylia argentea seed lectin.
Incubation of a duodenum transverse section with rabbit anti-lectin
immunoglobulins and alkaline phosphatase-conjugated goat anti-
rabbit IgG produced a dark staining on the villus surface
representing the immunolabelling lectin bound to a mature
enterocyte. No enterocyte staining was observed in control rats
fed on an egg white based diet.
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403390
(Grant et al., 1985), growing steers (Williams et al., 1984)
and pigs (Begbie and King, 1985), indicating its absorption
through the gut wall. However, development of circulating
antibodies to the lectin was unable to prevent either
bacterial proliferation or the uptake of the dietary lectin
into the systemic circulation (Pusztai, 1989). For instance,
the presence of antibodies from human blood against the
banana lectin (BanLec-1) was detected in a screening for
reactivity to foodstuff components (Koshte et al., 1990,
1992). Circulating antibodies to three structurally related
legume lectins, ECorL (Erythrina corallodendron), PNA
and SBA, and to WGA were purified by lectin-affinity
chromatography from human sera indicating that antibodies
to dietary lectins commonly present in human diets exist in
the sera of healthy humans (Tchernychev and Wilchek,
1996). The authors argued that the significant amounts of
circulating antibodies which reacted with EcorL, as it is not
a dietary protein, is because legume lectins share consider-
able structural similarities (Van Damme et al., 1998).
Recently, the mucosal immunogenicity of a number of plant
lectins, with different sugar specificities, was investigated in
mice (Lavelle et al., 2000). Accordingly both oral and
intranasal delivery of five plant lectins, LEA, ML-1, PHA,
WGA and UEA-1, stimulated the production of specific
serum IgG and IgA antibodies after three intranasal or oral
The ability of most plant lectins to transverse the gut
barrier is not limited to antibody production but can also
trigger histamine release from basophils (Haas et al., 1999).
Accordingly 16 common lectins, particularly ConA, PHA,
PSA, SNA and LCA (Lens culinaris; lentil) were able to
induce human basophils to secrete interleukin-4 (IL-4) and
IL-13, the key promoters of Th2 responses and IgE
synthesis. Since lectins can enter the circulation after oral
uptake, they might play a role in inducing the so-called early
IL-4 required to switch the immune response towards a Th2
response and type I allergy.
In a recent review, Cordain et al. (2000) stated that the
interaction of dietary lectins with enterocytes and lympho-
cytes might facilitate the translocation of both dietary and
gut-derived pathogenic antigens to peripheral tissues
causing a persistent peripheral antigenic stimulation in
genetically susceptible individuals. This might ultimately
result in the expression of overt rheumatoid arthritis (RA).
A striking anatomical change evident in rats fed on
lectins is the severe atrophy of the thymus. This occurs to
disappeared after feeding PHA for 10 days (Oliveira et al.,
1988, 1994). Although the precise significance of this
involution is not clear, it is quite likely that it may affect
cell-mediated immune responses having serious conse-
quences for the animal. Thus, the proliferation of normally
innocuous intestinal bacteria and even the absorption of an
antigenic form of lectin which has been shown to gain entry
to the systemic circulation are possibly related to
the incapacity of these animals to develop an adequate
humoral and cell-mediated immune response.
Usually animals fed on legume diets develop pancreas
hypertrophy. Formerly this phenomenon had been exclu-
sively associated to dietary protease inhibitors. Studies by
Oliveira et al. (1988) and Pusztai et al. (1988) unequivocally
showed that the purified PHA included into diets offered to
rats promoted hypertrophy of the pancreas in a dose
response fashion. This was in fact the first time that
pancreatic hypertrophy was shown to be due to diets which
contained purified lectins free from trypsin inhibitors. Since
then, this effect has consistently been observed in rats fed on
different diets containing purified lectins from other
legumes (Oliveira et al., 1994; Vasconcelos et al., 2001).
Recently Kelsall et al. (2002) demonstrated in long-term
feeding trials that even low doses (40 mg/rat/day) of PNA
given to rats could significantly influence pancreatic growth.
They suggested that this trophic action might have potential
adverse implications for the development of pancreatic
cancer in humans. Accumulation of polyamines has been
shown to precede organ hypertrophy (Pusztai et al., 1988;
Bardocz et al., 1996). Further PHA, SBA, PNA and WGA-
induced pancreatic growth of rats, in vivo, are related to
increasing CCK plasma levels with corresponding increase
in pancreatic protein output suggesting that the ingestion of
lectins might have major CCK-mediated effects on
gastrointestinal function and pancreas growth (Herzig
et al., 1997; Jordinson et al., 1997). CCK is a peptide
hormone released from the I-cells of the upper small
intestine which is a potent stimulator of various physiologi-
cal functions such as pancreas enzyme secretion, reduction
of food intake, inhibition of gastric emptying and stimu-
lation of gall bladder contraction (Sayegh and Ritter, 2003).
Grant et al. (1999) suggested that secretion of pancreatic
digestive enzymes induced in rats by first-time oral exposure
to PHA (E
isolectin) was mediated only in part by CCK.
They suggested that additional mechanisms or hormones,
such as secretin, might play a role in modulating later
exocrine pancreas responses to PHA. PHA was also able to
stimulate pancreatic amylase secretion in rats which was
blocked by devazepide, a CCK-A receptor antagonist
´s et al., 2000). Radberg et al. (2001) observed that
the size of the pancreatic acini was greater in the PHA-
treated pigs, but no increases in enzyme content or
pancreatic weight could be determined. However, the
blood plasma levels of CCK were higher in the PHA-
treated than in the control pigs.
Disturbances of the hormonal homeostasis of animals
were also observed upon feeding lectins. PHA reduced the
circulating levels of insulin initially by interfering with its
secretion from the pancreas but later insulin synthesis was
also impaired. Surprisingly, normal blood glucose concen-
trations were maintained in rats fed with PHA despite the
low circulating insulin levels (Pusztai, 1991; Bardocz et al.,
1996). The exact mechanism by which lectins cause changes
in insulin production remains unclear. However, it is
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 391
possible that through its binding to neuroendocrine cells in
the gut or to other non-pancreatic endocrine organs, PHA
may trigger the release of hormones which impair insulin
synthesis/secretion. Alternatively, it is likely that the
insulin-mimicking properties of lectins in vivo may interfere
with the feedback regulation of pancreatic insulin pro-
duction (Bardocz et al., 1996).
Liver enlargement was shown to be another systemic
effect of dietary lectins (Oliveira et al., 1988; Pusztai, 1991).
The increase in liver weight may be due to a response of this
organ to the disturbance of the general metabolism that
occurs when animals are fed with lectins. In fact some
lectins induce body fat catabolism and glycogen loss,
leading to depletion of the body reserves (Grant et al., 1987,
1995). Dietary PHA, for instance, induces an increase in
body lipid utilization. A direct correlation between dietary
PHA and increased amounts of urinary 3-hydroxybutyrate
output of rats was observed, providing a strong evidence for
the occurrence of a PHA-dependent increased lipolysis
(Oliveira et al., 1988). The lipid depletion occurred
primarily from the adipose tissues whereas little change
was observed in liver lipid levels. In contrast, the glycogen
content of the liver was halved whereas the glycogen
concentration in skeletal muscle was not significantly
affected during the same period (Oliveira et al., 1988;
Pusztai, 1989). According to Pusztai et al. (1998) ML-1
reduced body fat reserves probably through depression of
circulating insulin levels. Dietary PHA also alters the rate of
muscle protein synthesis without significantly affecting the
rate of protein degradation, resulting in loss of muscle
weight (Palmer et al., 1987). It is possible that circulating
lectin may have interacted directly with muscle cells leading
to impairment of protein synthesis (Pusztai et al., 1989).
Alternatively, this effect may have been indirect and
hormonally mediated (Pusztai, 1991). Moreover, increased
concentration of urinary N (mainly urea-N) was observed in
PHA-fed rats suggesting disturbances in the protein
metabolism (Oliveira et al., 1988). Increased activities of
liver glutamic pyruvic transaminase (LGPT) and glutamic
oxaloacetic transaminase (LGOT), indicative of increased
catabolism of amino acids in the liver, were also observed
when increasing amounts of dietary PLA (Phaseolus
lunatus; lima bean) were offered to rats (Aletor and Fetuga,
1985). In summary, dietary lectins seem to interfere with the
overall metabolism of body lipid, protein and carbohydrate
(Pusztai, 1991; Grant, 1999). Such effects may have a
bearing upon hepatomegaly. Although the significance of
the morphological and metabolic changes in the liver of
lectin-fed animals remains to be elucidated, such adverse
effects upon this key organ certainly contribute to the overall
toxicity of dietary lectin.
Lung hypertrophy was also detected in rats fed with
diets containing ML-1 (Pusztai et al., 1998). Peanut
lectin which displays affinity for glycoproteins found
specifically on arterial smooth muscle cells stimulated the
growth of smooth muscle and pulmonary arterial cells,
suggesting that biologically active PNA present in peanut
oil could possibly contribute significantly to its athero-
genic properties (Kritchevsky et al., 1998).
Recently our group purified a toxic and hemagglutinat-
inglectin(IAAL)fromsalsa(Ipomoea asarifolia
R. et Schult., Convolvulaceae) leaves which agglutinates
rabbit, horse and ovine red cells but not cow, sheep, goat,
dog and human erythrocytes. This activity was not abolished
by simple sugars but fetuin, avidin and N-acetyl-D-
neuraminic acid were inhibitory (Santos, 2001). IAAL
injected intraperitoneally into mice and rats induced
dyspnoea, tonicclonic convulsions and flaccid paralysis
prior to death. IAAL was also toxic to orally fed mice. When
IAAL was daily intubated into female mice, for 15 days, it
induced stunted growth, diarrhoea, severe respiratory
distress and muscle tremors. The liver of the female mice
receiving IAAL showed megalocytose and hepatocytes with
vacuolar degeneration and piknotic nuclei. In the kidneys,
tubular liquefactive necrosis, atrophy and destruction of
glomeruli and congestion of blood vessels occurred (data
not shown). Surprisingly, the litter was also affected with
some of these above symptoms (Fig. 3), although in a lesser
Despite the adverse effects of dietary lectins, in recent
years, considerable work has been done on the possible uses
of them, at non-toxic oral doses, to obtain therapeutically
beneficial effects, such as promotion of gut regrowth after
total parenteral nutrition or exposure to elemental diets
(Jordinson et al., 1999; Sasaki et al., 2002), use as drug
delivery agents or oral vaccine adjuvants (Lavelle, 2001;
Lavelle et al., 2001) or use in anti-cancer therapies (Pryme
et al., 1998, 1999).
Fig. 3. Light micrograph (100 £) of kidney section from a suckling
mouse pup whose mother was intubated for 15 days with
Ipomea asarifolia agglutinin (IAAL, 68 mg/day/mouse) showing
blood vessel congestion (BVC), glomerulus atrophy (GA) and
tubular necrosis (TN).
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403392
7. Insecticidal properties of plant lectins
The insecticidal activity (Table 1) of plant lectins against
a large array of insect species belonging to the Coleoptera,
Homoptera, Diptera and Lepidoptera order has been well
documented (Gatehouse et al., 1995; Schuler et al., 1998;
Carlini and Grossi-de-Sa
´, 2002). This feature represents a
potential of using plant lectins as naturally occurring
insecticide agents against the pests which restrain increased
crop production. Generally the in vitro bioassay undertaken
to judge this biological characteristic consists of inclusion of
the studied lectin into artificial diets offered to the target
insect during a given period of time. In general, the lectin
levels incorporated into artificial diets to test oral toxicity
have varied from 1 to 50 mg/g diet or from 5 to 1500 mg/ml
diet to deliver these proteins to chewing and sucking insects,
respectively. Then, the parameters which indicate the
harmful effects of lectins on insects include larval weight,
size, color, mortality, feeding inhibition, antimetabolic
effects, honeydew excretion levels, pupation, delays in
total developmental time, adult emergence and/or fecundity
on the first and/or second generation of the insects which
have been reared on lectin-containing artificial diets.
Although the precise mode of insecticidal action of plant
lectins is not fully understood it appears that resistance to
proteolytic degradation by the insect digestive enzymes and
binding to insect gut structures are two basic prerequisites
for lectins to exert their deleterious effects on insects. As in
higher animal systems (Pusztai, 1991), the harmful effects of
lectins on insects are attributed mainly to binding of them to
the surface of the intestinal epithelial cells which lead to
interference with the digestive, protective, or secretory
functions of the intestine. Nevertheless, it is quite obvious
that for binding to the intestine structures, cells and/or to any
digestive enzyme or either to other insect component, the
orally fed lectins have firstly to be refractory to the action of
proteolytic enzymes and, in addition, to encounter satisfac-
tory environmental conditions of pH and temperature to
exert their effects. Indeed, structure/function analysis by
site-directed mutagenesis indicated that the insecticidal
and binding activities of the GlcNAc-specific lectin GSII
(Griffonia simplicifolia) and its mutant forms were corre-
lated with the resistance to proteolytic degradation by the
midgut extracts and binding to the digestive tract of third or
fourth instar larvae of Callosobruchus maculatus (Coleop-
tera: Bruchidae), the cowpea weevil. This insect when
reared on a GSII-containing artificial diet had a within-seed
prolonged development time and inhibited growth (Zhu-
Salzman et al., 1998). These effects may have resulted from
the binding of this lectin to the chitin of the peritrophic
membrane, a structure existing in the gut of most
phytophagous insects which protects the gut epithelial
cells from abrasive food particles (Peumans and Van
Damme, 1994). It is likely that other GlcNAc-specific
lectins (Table 1) share similar mode of action on insects.
The two chitin-binding lectins, TEL and KpLec, from
Talisia esculenta and Koelreuteria paniculata seeds,
respectively, negatively affected the larval development of
C. maculatus and Anagasta kuehniella (Lepidoptera:
Pyralidae; Mediterranean flour moth) through binding to
glycan receptors on the surface of cells lining the insect gut
(Macedo et al., 2002, 2003). Regression analysis showed
that for every 0.1% increase in TEL dose given via artificial
seeds, there were a 3.9% ðR2¼0:98Þand 4.1% ðR2¼0:99Þ
increase in mortality of C. maculatus and Zabrotes
subfasciatus (Coleoptera: Bruchidae), respectively (Macedo
et al., 2002) whereas for every 0.1% increase in KpLec dose,
there were a 5.9% ðR2¼0:98Þand 5.3% ðR2¼0:96Þ
increase in mortality of C. maculatus and Anagasta
kuehniella, respectively (Macedo et al., 2002). Immuno-
logical studies carried out to elucidate the mechanism of
action of the mannose-specific lectin GNA on the rice brown
planthoppers (Nilaparvata lugens; Homoptera: Delphaci-
dae) showed that no significant proteolytic degradation
occurred either in the gut or honeydew of insects fed on
lectin-containing diet (Powell et al., 1998). The fully active
GNA was able to bind to the luminal surface of the midgut
epithelial cells within the planthopper, probably recognising
cell surface carbohydrate moieties of glycoproteins and/or
other glycoconjugates in the gut. For instance, the mannose-
containing glycopolypeptide ferritin acts as the most
abundant binding protein for GNA in the midgut of rice
brown planthoppers (Du et al., 2000). Moreover the
immunolabelling GNA assay revealed its presence in the
fat bodies, the ovarioles, and throughout the haemolymph
suggesting that GNA was able to cross the midgut epithelial
barrier and pass into the insect’s circulatory system
resulting in a systemic toxic effect (Powell et al., 1998).
Resistance to proteolytic degradation and binding of
ASAL (mannose-binding leaf garlic lectin) to gut receptors
in the luminal epithelium of two important homopteran
insect pests, the mustard aphid (Lypaphis erysimi; Aphidi-
dae: Homoptera) and the red cotton bug (Dysdercus
cingulatus; Hemiptera: Pyrrhocoridae) also correlated with
its insecticidal activities (Bandyopadhyay et al., 2001).
ASAL bound to the carbohydrate residue of the 55 and
45 kDa brush border membrane vesicle receptor proteins in
the case of aphid and bug, respectively, possibly decreasing
the insect membrane permeability. Zhu-Salzman and
Salzman (2001) studying the digestion of recombinant
GSII and its mutant protein variants with two purified
cathepsin L-like gut proteases of C. maculatus larvae
suggested that carbohydrate binding to the insect gut and
proteolytic resistance are independent properties of rGSII.
However they concluded that both properties facilitate GSII
efficacy as a plant defensive molecule. GNA and ConA
when included in artificial diets offered to the tomato moth
(Lacanobia oleracea; Lepidoptera: Noctuidae) larvae accu-
mulated in the gut, Malpighian tubules and haemolymph
indicating that both lectins were internalised and distributed
systemically after binding to glycoproteins present along the
insect digestive tract (Fitches et al., 2001a).
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 393
Table 1
Plant lectins with oral toxicity to insect
Lectin (plant source) Insect Host Reference
Mannose specific
ASA (Allium sativum)Laodelpha striatellus (rice
small brown planthopper);
Nilaparvata lugens (rice
brown planthopper);
Rice Powell et al., 1995
Myzus persicae (peach-
potato aphid)
Peach, potato Sauvion et al., 1996
Dysdercus cingulatus (red
cotton bug); D. koenigii (red
cotton bug)
Cotton, okra, maize, pearl Roy et al., 2002
ASA I, II D. cingulatus;D. koenigii Cotton, okra, maize, millet Roy et al., 2002
ASAL (Allium sativum—leaf) D. cingulatus;Lipaphis erysimi
(mustard aphid)
Cotton, okra, maize, pearl Bandyopadhyay et al.,
CEA (Colocasia esculenta)D. cingulatus;D. Koenigii Cotton, okra, maize, pearl Roy et al., 2002
DEA (Differenbachia sequina)D. Cingulatus;D. Koenigii Cotton, okra, maize, pearl Roy et al., 2002
GNA (Galanthus nivalis)Callosobruchus maculatus
(bruchid weevil)
Cowpea Gatehouse et al., 1991
Acyrthosiphon pisum (pea aphid) Pea Rahbe
´et al., 1995
Antitrogus sanguineus
(sugarcane whitegrub)
Sugarcane Allsopp and McGhie,
Aulacorthum solani
(glasshouse potato aphid)
Potato Down et al., 1996
M. persiacae Peach, potato Sauvion et al., 1996
Lacanobia oleracea (tomato moth) Tomato Fitches and Gatehouse,
1998; Fitches et al.,
Maruca vitrata (legume pod-bore) Cowpea Machuka et al., 1999
Tarophagous proserpina
(taro planthopper)
Taro Powell, 2001
L. striatellus Rice Loc et al., 2002
N. lugens Rice Powell et al., 1995,
1998; Loc et al., 2002
KPA (Koelreuteria paniculata)Anagasta kuehniella (Mediterranean
flour moth); C. maculatus
Beans, grains, fruits, nuts Macedo et al., 2003
LOA (Listera ovata)M. vitrata Cowpea Machuka et al., 1999
NPA (Narcissus pseudonarcissus)N. lugens Rice Powell et al., 1995
M. persiacae Peach, potato Sauvion et al., 1996
Mannose/glucose specific
ConA (Canavalia ensiformis)A. pisum Pea Rahbe
´and Febvay,
A. pisum Pea Rahbe
´et al., 1995
Aphis gossypii (cotton and
melon aphid)
Cotton, mellon Rahbe
´et al., 1995
Aulacorthum solani (glasshouse
and potato aphid)
Potato Rahbe
´et al., 1995
Macrosiphum albifrons
(lupin aphid)
Lupin Rahbe
´et al., 1995
Macrosiphum euphorbiae
(potato aphid)
Apple, bean, broccoli, papaya Rahbe
´et al., 1995
M. persiacae Peach, potato Rahbe
´et al., 1995;
Sauvion et al., 1996;
Gatehouse et al., 1999
L. oleracea Tomato Fitches and Gatehouse,
1998; Gatehouse et al.,
1999; Fitches et al.,
(continued on next page)
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403394
A toxic dose of GNA was also able to induce
morphological changes in the midgut region of planthoppers
with disruption of the microvilli brush border region (Powell
et al., 1998). Habibi et al. (2000) showed that the gut
epithelial cells of Lygus hesperus (Hemiptera: Miridae), the
Western tarnished plant bug, were severely disrupted by
PHA. Strong binding of PHA to the brush border microvilli
of the midgut at the first and third, but not the second
ventriculus, and lectin internalisation were detected.
Moreover the first ventriculus showed severe disruption,
disorganisation and swelling toward the proximal and distal
gut lumen regions which were completely closed. Complete
closure of the gut lumen also occurred in the hindgut region
as a consequence of severe disruption and swelling of
hindgut epithelial cells. However, only slight disruption
with enlargement of nuclei occurred in the foregut epithelial
cells clearly indicating that Lygus hesperus contains PHA
receptors in three specific regions of its digestive tract.
Table 1 (continued)
Lectin (plant source) Insect Host Reference
T. proserpina Taro Powell, 2001
LCA (Lens culinaris)A. pisum Pea Rahbe
´et al., 1995
PSA (Pisum sativum)A. pisum Pea Rahbe
´et al., 1995
Hypera postica (clover leaf weevil) Alfafa, lucerne Elden, 2000
N-acetyl-D-glucosamine specific
ACA (Amaranthus caudatus)A. pisum Pea Rahbe
´et al., 1995
BSA (Bandeiraea simplicifolia)Diabrotica undecimpunctata (Southern
corn rootworm); Ostrinia nubilaris
(European corn borer)
Corn Czapla and Lang, 1990
BSAII A. pisum Pea Rahbe
´et al., 1995
GSII (Griffonia simplicifolia)C. maculatus Cowpea Zhu et al., 1996;
Zhu-Salzman et al.,
1998; Zhu-Salzman
and Salzman, 2001
PAA (Phytolacca americana)D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
TEL (Talisia esculenta)C. maculatus; Zabrotes subfasciatus
(Mexican dry bean weevil)
Beans Macedo et al., 2002
WGA (Triticum aestivum)D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
Antitrogus sanguineus (sugarcane whitegrub) Sugarcane Allsopp and McGhie, 1996
H. postica Alfafa Elden, 2000
L. erysimi Mustard Kanrar et al., 2002
Galactose specific
AHA (Artocarpus hirsuta)Tribolium castaneum (red flour beetle) Large number of grains Gurjar et al., 2000
AIA (Artocarpus integrifolia)D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
GHA (Glechoma hederacea - leaf) Leptinotorsa decemlineata (colorado
potato beetle)
Potato Wang et al., 2003
(Ricinus communis)D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
YBA (Sphenostylis stenocarpa)Clavigralla tomentosicollis (coreid bug) Vigna spp. Okeola and Machuka,
C. maculatus;M. vitrata Cowpea Machuka et al., 2000
N-acetyl-D-galactosamine specific
ACA (Amaranthus caudatus)A. pisum Pea Rahbe
´et al., 1995
BFA (Brassica fructiculosa)Brevicoryne brassicae (cabbage aphid) Broccoli, Brussels sprouts,
cauliflower, head cabbage
Cole, 1994
BPA (Bauhinia purpurea)D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
CFA (Codium fragile)D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
EHA (Eranthis hyemalis)D. undecimpunctata Corn Kumar et al., 1993
MPA (Maclura pomifera)D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
PTA (Psophocarpus tetragonolobus)C. maculatus Cowpea Gatehouse et al., 1991
N. lugens Rice Powell, 2001
SNA-II (Sambucus nigra)A. pisum Pea Rahbe
´et al., 1995
VVA D. undecimpunctata;O. nubilaris Corn Czapla and Lang, 1990
PHA (Phaseolus vulgaris)L. hesperus (Western tarnished plant bug) Cotton, alfafa, legumes Habibi et al., 2000
Sugar specificity is represented by the best monosaccharide inhibitor.
Complex carbohydrate structure bearing terminal galactose residues (Goldstein and Poretz, 1986).
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 395
Another additional antinutritional complication for the
insects fed on lectin-containing artificial diets of plants,
which also occurs in lectin-fed higher animals, is the
possibility that lectins may destabilise insect metabolism
by interfering with gut enzymatic function either
indirectly or by binding to glycosylated digestive enzymes
in the gut (Van Damme et al., 1998). Orally-fed GNA and
ConA, for example, affected the activities of soluble and
brush border membrane enzymes in the midgut of
Lacanobia oleracea larvae. Furthermore significantly
elevated total aminopeptidase activity, both in terms of
total activity per larval gut and activity per mg gut
protein, was observed. Similarly, both GNA and ConA
treatments resulted in elevated levels of trypsin activity
per gut. GNA, but not ConA, induced a significant
increase in a-glucosidase activity per gut. Thus lectins
upon binding to the gut may indirectly affect the enzyme
regulatory mechanisms as a consequence of perturbation
of the peritrophic matrix and/or brush border membrane
environment (Fitches and Gatehouse, 1998).
The major insecticide resistance mechanism in the
brown planthopper Nilaparvata lugens involves overpro-
duction of esterase isoenzymes. All the esterases purified
from an insecticide resistant strain of this insect were shown
to be glycosylated. As GNA, MAA (Maackia amurensis
agglutinin) and DAS (Diffenbachia sequina agglutinin) bind
to this family of esterases at the terminally linked mannose
(Small and Hemingway, 2000). It is possible that in trans-
genic plants expressing mannose-binding lectins, if they
were not fully effective in protecting the plant against the
brown planthopper (or other insecticide resistant pest), they
could interact with and inhibit the enzymes thereby
Table 2
Plant species transformed with lectin genes to confer resistance against insects
Transformed plant Lectin
Target pest Reference
Maize WGA Ostrinia nubilaris;
Diabrotica undecimpunctata
Maddock et al., 1991
Mustard (B. juncea) WGA Lipaphis erysimi Kanrar et al., 2002
Arabidopsis thaliana PHA-E, L
Lacanobia oleracea Fitches et al., 2001b
Potato GNA Aulacorthum solani Down et al., 1996
Potato GNA Myzus persicae Gatehouse et al., 1996;
Couty et al., 2001b
Potato GNA L. oleracea Fitches et al., 1997;
Gatehouse et al., 1997
Potato GNA L. oleracea Bell et al., 1999, 2001;
Down et al., 2001
Potato GNA Aphidius ervi (parasitoid
of M. persicae)
Couty et al., 2001b
Potato ConA L. oleracea;M. persicae Gatehouse et al., 1999
Rice GNA Nilaparvata lugens Rao et al., 1998; Foissac et al.,
2000; Tinjuangjun et al., 2000;
Maqbool et al., 2001; Tang et al.,
2001; Loc et al., 2002
Rice GNA Nephotettix virescens (green
Foissac et al., 2000
Rice GNA Cnaphalocrocis medinalis (rice
leaffolder); Scirpophaga incertulas
(yellow stemborer)
Maqbool et al., 2001
Rice GNA Laodelphax striatellus (rice small
brown planthopper)
Sun et al., 2002; Wu et al., 2002
Sugarcane GNA Eoreuma loftini (Mexican rice borer);
Diatraea saccharalis (sugarcane borer)
Setamou et al., 2002
Sugarcane GNA Parallorhogas pyralophagus (parasitoid
of E. loftini)
Tomov and Bernal, 2003
Tobacco PSA Heliothis virescens (tobacco budworm) Boulter et al., 1990
Tobacco GNA M. persicae Hilder et al., 1995
Tobacco GNA Helicoverpa zea (cotton bollworm) Wang and Guo, 1999
Wheat GNA Sitobion avenae (grain aphid) Stoger et al., 1999
For lectin abbreviations see Table 1.
Transgenic Arabidopsis plants expressing the Phaseolus vulgaris erythro- and leucoagglutinating isolectins (PHA-E and PHA-L) either at
0.4–0.6% of total soluble proteins were not toxic to L. oleracea.
First demonstration of insect enhanced resistance of transgenic plants expressing a foreign lectin.
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403396
rendering the insect more susceptible to the action of
insecticide. This could reduce the amounts of pesticide used.
Despite the large number and varieties of insecticidal
plant lectins described (Table 1) the real allure of this field
of research is the possibility of using plant lectins as potent
control agents to engineer crop plants for insect resistance
(Jouanin et al., 1998; Vaughan et al., 1999). Currently, the
two major groups of plant-derived genes used to confer
insect resistance on crops are those of inhibitors of digestive
enzymes (proteases and amylase inhibitors) and lectins
(Schuler et al., 1998). Several bioassay studies of lectin-
expressing plants, in particular GNA-containing, have been
reported recently (Hilder et al., 1995; Down et al., 1996;
Gatehouse et al., 1996; Czapla, 1997; Rao et al., 1998;
Foissac et al., 2000; Couty et al., 2001a). Overall, transgenic
plants expressing high levels of lectins exhibited some
degree of resistance to the target insect. It is worth
mentioning that the great interest on transgenic crop plants
expressing the gene for GNA or other mannose-binding
lectins such as ASA resides in the fact that although these
lectins show toxicity against species of various insect orders
they are non toxic to mammals and birds (Powell et al.,
1995; Down et al., 1996; Bandyopadhyay et al., 2001).
Therefore GNA has been transferred and expressed in
several crop plants (Table 2).
In parallel studies on the possible toxic or antinutritive
effects of lectins, being considered for introduction into
transgenic crops, on parasitoids of insect pests have been
carried out to evaluate the ecological problems that such
transgenic plants could bring to dependent secondary
species or symbiotes in the field (Bell et al., 1999, 2001;
Down et al., 2000; Couty et al., 2001bc; Tomov and Bernal,
2003). Fortunately, the studies conducted so far with this
purpose have demonstrated that the effects of lectins on
parasitoids are not acute. For example, no acute toxicity of
GNA-containing aphid towards its parasitoid two-spot
ladybird (Adalia bipunctata L.; Coleoptera: Coccinellidae)
larvae fed on Myzus persicae (Homoptera: Aphididae) was
observed, although there were small effects on development
which led the authors to hypothesise that dietary GNA had
reduced the nutritive quality of the aphids thereby limiting
subsequent nutrient intake by the ladybirds and slowing
their development (Down et al., 2000). The results obtained
by Couty et al. (2001b) indicated that GNA delivered via
artificial diet to M. persicae was transferred to its parasitoid
Aphidius ervi (Hymenoptera: Aphidiidae) and that the
parasitoid larvae excreted most of the ingested GNA in
the meconium. Tomov and Bernal (2003) concluded that
although GNA transgenic sugarcane, ingested via Eoreuma
loftini tissues, was not acutely toxic to Parallorhogas
pyralophagus (Hymenoptera: Braconidae), sublethal effects
on life history parameters occurred both in the first and
second generation of the parasitoid. These effects might be
considered in a broader context to determine their possible
ecological significance.
8. Conclusions
Lectins are highly antinutritional and/or toxic substances
being detrimental to various plant-eating organisms. This
property is associated, in part, to their high resistance to
proteolysis in gastrointestinal tract of monogastric, rumi-
nants and insects, to their capacity of binding to epithelial
cells lining the small intestine and to their ability to
modulate intestinal and systemic metabolism. It has been
extensively demonstrated that plant lectins are effective
biological agents against insect attack. In fact, insect-
resistant plants produced by expression of lectin genes in
transgenic plants are already a reality. This approach could
increase crop productivity and reduce the usage of pesticide.
However, few lectins tested for this purpose have been
specifically selected on the basis that they convey high
resistance to disease or predators in plants, whilst simul-
taneously having a low toxicity to higher mammals,
including man. Hence, future research priority must be
given to finding other lectins with these above character-
istics hoping to draw definitive conclusions to two basic
questions: (a) What effects do lectins have in a diet? (b)
What effects do insect-resistant transgenic plants have when
pest and their parasitoids or symbiotes encounter them in the
This work was supported by Conselho Nacional de
Desenvolvimento Cientı
´fico e Tecnolo
´gico (CNPq), Pro-
grama de Apoio a Nu
´cleos de Excele
ˆncia (PRONEX),
˜o de Aperfeic¸oamento de Pessoal de Nı
Superior (CAPES), Programa Nacional de Cooperac¸a
ˆmica (PROCAD) and Fundac¸a
Pesquisa do Estado do Ceara
Aletor, V.A., Fetuga, B.L., 1985. Responses of the rats hepatic and
serum transaminases to lectin extracted from lima bean
(Phaseolus lunatus). Z. Tierphysiol. Tierer. 54, 249–252.
Allsopp, P.G., McGhie, T.K., 1996. Snowdrop and wheatgerm
lectins and avidin as antimetabolities for the control of
sugarcane whitegrubs. Entomol. Exp. Appl. 80, 409414.
Baintner, K., Jakab, G., Gyori, Z., Kiss, P., 2000. Binding of FITC-
labelled lectins to the gastrointestinal epithelium of the rat.
Pathol. Oncol. Res. 2000, 179 183.
Bandyopadhyay, S., Roy, A., Das, S., 2001. Binding of garlic
(Allium sativum) leaf lectin to the gut receptors of homopteran
pests is correlated to its insecticidal activity. Plant Sci. 161,
Barbieri, L., Battelli, M.G., Stirpe, F., 1993. Ribosome-inactivating
proteins from plants. Biochim. Biophys. Acta 1154, 237 282.
Bardocz, S., Ewen, S.W.B., Grant, G., Pusztai, A., 1995. Lectins as
growth factors of the small intestine and the gut. In: Pusztai, A.,
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 397
Bardocz, S. (Eds.), Lectins: Biomedical Perspectives, Taylor
and Francis, London, pp. 103116.
Bardocz, S., Grant, G., Pusztai, A., Franklin, M.F., Carvalho,
A.F.F.U., 1996. The effect of phytohaemagglutinin on the
growth, body composition, and plasma insulin of the rat at
different dietary concentrations. Brit. J. Nutr. 76, 613– 626.
Begbie, R., King, T.P., 1985. The interaction of dietary lectin with
porcine small intestine and production of lectin-specific
antibodies, In: Bog-Hansen, T.C., Breborovicz, J. (Eds.),
Lectins: Biology, Biochemistry, Clinical Biochemistry, Walter
de Gruyter, Berlin, pp. 1527.
Bell, H.A., Fitches, E.C., Down, R.E., Marris, G.C., Edwards, J.P.,
Gatehouse, J.A., Gatehouse, A.M.R., 1999. The effect of
snowdrop lectin (GNA) delivered via artificial diet and
transgenic plants on Eulophus pennicornis (Hymenoptera:
Eulophidae), a parasitoid of the tomato moth Lacanobia oleracea
(Lepidoptera: Noctuidae). J. Insect Physiol. 45, 983991.
Bell, H.A., Fitches, E.C., Marris, G.C., Bell, J., Edwards, J.P.,
Gatehouse, J.A., Gatehouse, A.M.R., 2001. Transgenic, G.N.A.
expressing potato plants augment the beneficial biocontrol of
Lacanobia oleracea (Lepidoptera; Noctuidae) by the parasitoid
Eulophus pennicornis (Hymenoptera; Eulophidae). Transgenic
Res. 10, 3542.
Bender, A.E., Reaidi, G.B., 1982. Toxicity of kidney beans
(Phaseolus vulgaris) with particular reference to lectins.
J. Plant Foods 4, 1522.
Boulter, D., Edwards, G.A., Gatehouse, A.M.R., Gatehouse, J.A.,
Hilder, V.A., 1990. Additive protective effects of incorporating
two different higher plant derived insect resistance genes in
transgenic tobacco plants. Crop Prot. 9, 351 354.
Boyd, W.C., Reguera, R.M., 1949. Studies on haemagglutinins
present in seeds of some representatives of the family
Leguminoseae. J. Immunol. 62, 333339.
Boyd, W.C., Shapleigh, E., 1954. Separation of individuals of any
blood group into secretors and non-secretors by use of a plant
agglutinin (lectin). Blood 9, 11951198.
Brady, P.G., Vannier, A.M., Banwell, J.G., 1978. Identification of
the dietary lectin, wheat germ agglutinin, in human intestinal
contents. Gastroenterology 75, 236– 239.
Broekaert, W.F., Allen, A.K., Peumans, W.J., 1987. Separation and
partial characterization of isolectins with different subunit
compositions from Datura stramonium seeds. FEBS Lett. 220,
116– 120.
Bryk, S.G., Gheri, G., 2002. Lectin histochemistry of enterocytes
sugar residues in the gut of the chick embryo and of the
newborn. Ital. J. Anat. Embryol. 107, 37 49.
Carbonaro, M., Cappelloni, M., Nicoli, S., Lucarini, M., Carnovale,
E., 1997. Solubility-digestibility relationship of legume pro-
teins. J. Agric. Food Chem. 45, 33873394.
Carbonaro, M., Grant, G., Cappeloni, M., Pusztai, A., 2000.
Perspectives into factors limiting in vivo digestion of legume
proteins: antinutritional compounds or storage proteins?
J. Agric. Food Chem. 48, 742749.
Carlini, C.R., Grossi-de-Sa
´, M.F., 2002. Plant toxic proteins with
insecticidal properties. A review on their potentialities as
bioinsecticides. Toxicon 20, 1515–1539.
Caygill, J.C., 1999. Antinutritional compounds: background and
introduction. In: Caygill, J.C., Mueller-Harvey, I. (Eds.),
Secondary Plant Products: Antinutritional and Beneficial
Actions in Animal Feeding, Nottingham University Press,
Nottingham, UK, pp. 16.
Chrispeels, M.J., Raikhel, N.V., 1991. Lectins, lectin genes, and
their role in plant defense. Plant Cell 3, 191.
Cole, R.A., 1994. Isolation of a chitin-binding lectin with
insecticidal activity in chemically-defined synthetic diets from
two wild Brassica species with resistance to cabbage aphid
Brevicoryne brassicae. Entomol. Exp. Appl. 72, 181187.
Cordain, L., Toohey, L., Smith, M.J., Hickey, M.S., 2000.
Modulation of immune function by dietary lectins in rheumatoid
arthritis. Brit. J. Nutr. 83, 207217.
Couty, A., de-la-Vina, G., Clark, S.J., Kaiser, L., Pham, D.M.H.,
Poppy, G.M., 2001a. Direct and indirect sublethal effects of
Galanthus nivalis agglutinin (GNA) on the development of a
potato-aphid parasitoid, Aphelinus abdominalis (Hymenoptera:
Aphelinidae). J. Insect Physiol. 47, 553561.
Couty, A., Down, R.E., Gatehouse, A.M.R., Kaiser, L., Pham-
Delegue, M.H., Poppy, G.M., 2001b. Effects of artificial diet
containing GNA and GNA-expressing potatoes on the devel-
opment of the aphid parasitoid Aphidius ervi Haliday (Hyme-
noptera: Aphidiidae). J. Insect Physiol. 47, 1357 1366.
Couty, A., Clark, S.J., Poppy, G.M., 2001c. Are fecundity and
longevity of female Aphelinus abdominalis affected by devel-
opment in GNA-dosed Macrosiphum euphorbiae? Physiol.
Entomol. 26, 287293.
Cuadrado, C., Grant, G., Rubio, L., Muzquiz, M., Bardocz, S.,
Pusztai, A., 2002. Nutritional utilization by the rat of diets based
on lentil (Lens culinaris) seed meal or its fractions. J. Agric.
Food Chem. 50, 4371–4376.
Czapla, T.H., 1997. Plant lectins as insect control proteins in
transgenic plants. In: Carozzi, N., Koziel, M. (Eds.), Advances
in Insect Control: The Role of Transgenic Plants, Taylor and
Francis, Basingstoke, UK, pp. 123– 138.
Czapla, T.H., Lang, B.A., 1990. Effect of plant lectins on the larval
development of European corn borer (Lepidoptera: Pyralidae)
and southern corn rootworm (Coleoptera: Crysomelidae).
J. Econ. Entomol. 83, 24802485.
Does, M.P., Houterman, P.M., Dekker, H.L., Cornelissen, B.J.C.,
1999. Processing, targeting, and antifungal activity of stinging
nettle agglutinin in transgenic tobacco. Plant Physiol. 120,
Douglas, M.W., Parsons, C.M., Hymowitz, T., 1999. Nutritional
evaluation of lectin-free soybeans for poultry. Poultry Sci. 78,
Down, R.E., Gatehouse, A.M.R., Hamilton, W.D.O., Gatehouse,
J.A., 1996. Snowdrop lectin inhibits development and decreases
fecundity of the glasshouse potato aphid (Aulacorthum solani)
when administered in vivo and via transgenic plants both in
laboratory and glasshouse trials. J. Insect Physiol. 42,
Down, R.E., Ford, L., Woodhouse, S.D., Raemaekers, R.J.M.,
Leitch, B., Gatehouse, J.A., Gatehouse, A.M.R., 2000. Snow-
drop lectin (GNA) has no acute toxic effects on a beneficial
insect predator, the 2-spot ladybird (Adalia bipunctata L.).
J. Insect Physiol. 46, 379 391.
Down, R.E., Ford, L., Bedford, S.J., Gatehouse, L.N., Newell, C.,
Gatehouse, J.A., Gatehouse, A.M.R., 2001. Influence of plant
development and environment on transgene expression in potato
and consequences for insect resistance. Transgenic Res. 10,
Du, J., Foissac, X., Carss, A., Gatehouse, A.M.R., Gatehouse, J.A.,
2000. Ferritin acts as the most abundant binding protein for
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403398
snowdrop lectin in the midgut of rice brown planthoppers
(Nilaparvata lugens). Insect Biochem. Mol. Biol. 30, 297–305.
Duranti, M., Gius, C., 1997. Legume seeds: protein content and
nutritional value. Field Crop Res. 53, 31– 45.
El-Adawy, T.A., 2002. Nutritional composition and antinutritional
factors of chickpeas (Cicer arietinum L.) undergoing different
cooking methods and germination. Plant Food Hum. Nutr. 57,
Elden, T.C., 2000. Influence of a cysteine proteinase inhibitor on
alfafa weevil (Coleptera: Curculionidae) growth and develop-
ment over successive generations. J. Entomol. Sci. 35, 70 76.
Endo, Y., Tsurugi, K., 1987. RNA N-glycosidase activity of ricin A-
chain: mechanism of action of the toxic lectin ricin on
eukaryotic ribosomes. J. Biol. Chem. 263, 87358739.
Erickson, R.H., Kim, J., Sleisenger, M.H., Kim, Y.S., 1985. Effects
of lectins on the activity of brush border membrane-bound
enzymes of rat small intestine. J. Pediatr. Gastroenter. Nutr. 4,
984– 991.
Fitches, E., Gatehouse, J.A., 1998. A comparison of the short and
long term effects of insecticidal lectins on the activities of
soluble and brush border enzymes of tomato moth larvae
(Laconobia oleracea). J. Insect Physiol. 44, 1213– 1224.
Fitches, E., Gatehouse, A.M.R., Gatehouse, J.A., 1997. Effects of
snowdrop lectin (GNA) delivered via artificial diet and
transgenic plant on the development of tomato moth (Lacanobia
oleracea) larvae in laboratory and glasshouse trials. J. Insect
Physiol. 8, 727–739.
Fitches, E., Woodhouse, S.D., Edwards, J.P., Gatehouse, J.A.,
2001a. In vitro and in vivo binding of snowdrop (Galanthus
nivalis agglutinin; GNA) and jackbean (Canavalia ensiformis;
Con A) lectins within tomato moth (Lacanobia oleracea) larvae;
mechanisms of insecticidal action. J. Insect Physiol. 47,
777– 787.
Fitches, E., Ilett, C., Gatehouse, A.M.R., Gatehouse, L.N., Greene,
R., Edwards, J.P., Gatehouse, J.A., 2001b. The effects of
Phaseolus vulgaris erythro- and leucoagglutinating isolectins
(PHA-E and PHA-L) delivered via artificial diet and transgenic
plants on the growth and development of tomato moth
(Lacanobia oleracea) larvae; lectin binding to gut glycoproteins
in vitro and in vivo. J. Insect Physiol. 47, 1389– 1398.
Fitzgerald, A.J., Jordinson, M., Rhodes, J.M., Singh, R., Calam, J.,
Goodlad, R.A., 2001. Comparison of the effects of concanava-
lin-A and epidermal growth factor on epithelial cell prolifer-
ation in the rat intestine. Aliment. Pharm. Therap. 15,
1077– 1084.
Foissac, X., Loc, N.T., Christou, P., Gatehouse, A.M.R., Gatehouse,
J.A., 2000. Resistance to green leafhopper (Nephotettix
virescens) and brown planthopper (Nilaparvata lugens)in
transgenic rice expressing snowdrop lectin (Galanthus nivalis
agglutinin; GNA). J. Insect Physiol. 46, 573 583.
Friedman, M., 1996. Nutritional value of proteins from different
food sources: a review. J. Agric. Food Chem. 44, 6 20.
Gatehouse, A.M.R., Howe, D.S., Flemming, J.E., Hilder, V.A.,
Gatehouse, J.A., 1991. Biochemical basis of insect resistance in
winged bean (Psophocarpus tetragonolobus) seeds. J. Sci. Food
Agric. 55, 6374.
Gatehouse, A.M.R., Powell, K.S., Van Damme, E.J.M., Peumans,
W.J., Gatehouse, J.A., 1995. Insecticidal properties of plant
lectins: their potential in plant protection. In: Pustzai, A.,
Bardocz, S. (Eds.), Lectins: Biomedical Perspectives, Taylor
and Francis, London, pp. 3558.
Gatehouse, A.M.R., Down, R.E., Powell, K.S., Sauvion, N., Rahbe
Y., Newell, C.A., Merryweather, A., Hamilton, W.D.O.,
Gatehouse, J.A., 1996. Transgenic potato plants with enhanced
resistance to the peach-potato aphid Mirzus persicae. Entomol.
Exp. Appl. 79, 295307.
Gatehouse, A.M., Davison, G.M., Newell, C.A., Hamilton, W.D.O.,
Burgess, E.P.J., Gilbert, R.J.C., Gatehouse, J.A., 1997. Trans-
genic potato plants with enhanced resistance to the tomato moth,
Lacanobia oleracea: growth room trials. Mol. Breed. 3, 49 63.
Gatehouse, A.M., Davison, G.M., Stewart, J.N., Gatehouse, L.N.,
Kumar, A., Geoghegan, I.E., Birch, A.N.E., Gatehouse, J.A.,
1999. Concanavalin A inhibits development of tomato moth
(Lacanobia oleracea) and peach-potato aphid (Myzus persicae)
when expressed in transgenic potato plants. Mol. Breed. 5,
Gilbert, R.J., 1988. Healthy eating day. Commun. Dis. Rep. 33,
Goldstein, I.J., Poretz, R.D., 1986. Isolation, physicochemical
characterization, and carbohydrate-binding specificity of lec-
tins. In: Liener, I.E., Sharon, N., Goldstein, I.J. (Eds.), The
Lectins, Academic Press, Orlando, pp. 33247.
Goldstein, I.J., Winter, H.C., Poretz, R.D., 1997. Plant lectins: tools
for the studying of complex carbohydrates. In: Montreuil, J.,
Vliegenthart, J.F.G., Schacter, H. (Eds.), Glycoproteins II,
Elsevier, Amsterdam, pp. 403474.
Grangeiro, T.B., Schriefer, A., Calvete, J.J., Raida, M., Urbanke, C.,
Barral-Netto, M., Cavada, B.S., 1997. Molecular cloning and
characterization of ConBr, the lectin of Canavalia brasiliensis
seeds. Eur. J. Biochem. 248, 43 48.
Grant, G., 1991. Lectins. In: D’Mello, J.P.F., Duffus, C.M. (Eds.),
Toxic Substances in Crop Plants, pp. 4967, The Royal Society
of Chemistry.
Grant, G., 1999. Plant lectins. In: Caygill, J.C., Mueller-Harvey, I.
(Eds.), Secondary Plant Products: Antinutritional and Beneficial
Actions in Animal Feeding, Nottingham University Press,
Nottingham, UK, pp. 87110.
Grant, G., More, L.J., McKenzie, N.H., Stewart, J.C., Pusztai, A.,
1983. A survey of the nutritional and haemagglutination
properties of legume seeds generally available in the UK. Brit.
J. Nutr. 50, 207214.
Grant, G., Greer, F., McKenzie, N.H., Pusztai, A., 1985. The
nutritional response of mature rats to kidney bean (Phaseolus
vulgaris) lectins. J. Sci. Food Agric. 36, 409 414.
Grant, G., Oliveira, J.T.A., de Dorward, P.M., Annand, M.G.,
Waldron, M., Pusztai, A., 1987. Metabolic and hormonal
changes in rats resulting from consumption of kidney bean
(Phaseolus vulgaris) or soyabean (Glycine max). Nutr. Rep. Int.
36, 763– 772.
Grant, G., More, L.J., McKenzie, N.H., Dorward, P.M., Buchan,
W.C., Telek, L., Pusztai, A., 1995. Nutritional and haemagglu-
tination properties of several tropical seeds. J. Agric. Sci. 124,
Grant, G., Edwards, J.E., Ewan, E.C., Murray, S., Atkinson, T.,
Farningham, D.A.H., Pusztai, A., 1999. Secretion of pancreatic
digestive enzymes induced in rats by first-time oral exposure to
kidney bean E
lectin is mediated only in part by
cholecystokinin (CCK). Pancreas 19, 382389.
Grant, G., Alonso, R., Edwards, J.E., Murray, S., 2000. Dietary soya
beans and kidney beans stimulate secretion of cholecystokinin
and pancreatic digestive enzymes in 400-day-old Hooded-Lister
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 399
rats but only soya beans induce growth of the pancreas. Pancreas
20, 305–312.
Gupta, A., Sandhu, R.S., 1998. Effect of garlic agglutinin and garlic
extracts on the rat jejunum. Nutr. Res. 18, 841850.
Gurjar, M.M., Gaikwad, S.M., Salokhe, S.G., Mukherjee, S., Khan,
M.I., 2000. Growth inhibition and total loss of reproductive
potential in Tribolium castaneum by Artocarpus hirsut lectin.
Invertebr. Reprod. Dev. 38, 9598.
Haas, H., Falcone, F.H., Schramm, G., Haisch, K., Gibbs, B.F.,
Klaucke, J., Poppelmann, M., Becker, W.M., Gabius, H.J.,
Schlaak, M., 1999. Dietary lectins can induce in vitro release of
IL-4 and IL-13 from human basophils. Eur. J. Immunol. 29,
918– 927.
Habibi, J., Backus, E.A., Huesing, J.E., 2000. Effects of phytohe-
magglutinin (PHA) on the structure of midgut epithelial cells
and localization of its binding sites in western tarnished plant
bug, Lygus hesperus Knight. J. Insect Physiol. 46, 611 619.
Hajos, G., Gelencser, E., Pusztai, A., Grant, G., Sakhri, M.,
Bardocz, S., 1995. Biological effects and survival of trypsin-
inhibitors and the agglutinin from soybean in the small intestine
of the rat. J. Agric. Food Chem. 43, 165170.
Hara, T., Mukunoki, Y., Tsukamoto, I., Miyoshi, M., Hasegawa, K.,
1984. Susceptibility of kintoki bean lectin to digestive enzymes
in vitro and its behaviour in the digestive organs of mouse in
vivo. J. Nutr. Sci. Vitaminol. 30, 381 394.
Harper, S.M., Crenshaw, R.W., Mullins, M.A., Privalle, L.S., 1995.
Lectin binding to insect brush border membranes. J. Econ. Ecol.
88, 1197–1202.
Herzig, K.H., Bardocz, S., Grant, G., Nustede, R., Folsch, U.R.,
Pusztai, A., 1997. Kidney bean lectin is a potent cholecystokinin
releasing stimulus in the rat inducing pancreatic growth. Gut 41,
333– 338.
Higuchi, M., Suga, M., Iwai, K., 1983. Participation of lectin in
biological effects of raw winged bean seeds on rats. Agric. Biol.
Chem. 47, 1979–1986.
Higuchi, M., Tsuchiya, I., Iwai, K., 1984. Growth inhibition and
small intestinal lesions in rats alter after feeding with isolated
winged bean lectin. Agric. Biol. Chem. 48, 695 701.
Hilder, V.A., Boulter, D., 1999. Genetic engineering of crop plants
for insect resistance—a critical review. Crop Prot. 18, 177 –191.
Hilder, V.A., Powell, K.S., Gatehouse, A.M.R., Gatehouse, J.A.,
Gatehouse, L.N., Shi, Y., Hamilton, W.D.O., Merryweather, A.,
Newell, C.A., Timans, J.C., 1995. Expression of snowdrop
lectin in transgenic tobacco plants resulted in added protection
against aphids. Transgenic Res. 4, 18 25.
Huisman, J., van der Poel, A.F.B., Van Leeuwen, P., Verstegen,
M.W.A., 1990a. Comparison of growth, nitrogen-metabolism
and organ weights in piglets and rats fed on diets containing
Phaseolus vulgaris beans. Brit. J. Nutr. 64, 743753.
Huisman, J., van der Poel, A.F.B., Mouwen, J.M.V.M., Vanweer-
den, E.J., 1990b. Effect of variable protein contents in diets
containing Phaseolus vulgaris beans on performance, organ
weights and blood variables in piglets, rats and chickens. Brit.
J. Nutr. 64, 755764.
´, W.G., 1960. Studies on phytotoxins in beans. Arzneimittel
Forschung 10, 10121016.
Jordinson, M., Playford, R.J., Calam, J., 1997. Effects of a panel of
lectins on cholecystokinin release in rats. Am. J. Physiol. 273,
946– 950.
Jordinson, M., Goodlad, R.A., Brynes, A., Bliss, P., Ghatei, M.A.,
Bloom, S.R., Fitzgerald, A., Grant, G., Bardocz, S., Pusztai, A.,
Pignatelli, M., Calam, J., 1999. Gastrointestinal responses to a
panel of lectins in rats maintained on total parenteral nutrition.
Am. J. Physiol. 276, 12351242.
Jouanin, L., Bonade, B.M., Girard, C., Morrot, G., Giband, M.,
1998. Transgenic plants for insect resistance. Plant Sci. 131,
Kanrar, S., Venkateswari, J., Kirti, P.B., Chopra, V.L., 2002.
Transgenic Indian mustard (Brassica juncea) with resistance to
the mustard aphid (Lipaphis erysimi Kalt.). Plant Cell Rep. 20,
Kelsall, A., Fitzgerald, A.J., Howard, C.V., Evans, R.C., Singh, R.,
Rhodes, J.M., Goodlad, R.A., 2002. Dietary lectins can
stimulate pancreatic growth in the rat. Int. J. Exp. Pathol. 83,
Kilpatrick, D.C., Pusztai, A., Grant, G., Graham, C., Ewen, S.W.B.,
1985. Tomato lectin resists digestion in the mammalian
alimentary canal and binds to intestinal villi without deleterious
effects. FEBS Lett. 185, 299– 305.
´s, K., Burghardt, B., Kisfalvi, K., Bardocz, S., Pusztai, A.,
Varga, G., 2000. Diverse effects of phytohaemagglutinin on
gastrointestinal secretions in rats. J. Physiol. 94, 31 36.
´s, K., Szalmay, G., Bardocz, S., Pusztai, A., Varga, G., 2001.
Phytohaemagglutinin inhibits gastric acid but not pepsin
secretion in conscius rats. J. Physiol. 95, 309314.
Koshte, V.L., Vandijk, W., Vanderstelt, M.E., Aalberse, R.C., 1990.
Isolation and characterization of BanLec-I, a mannoside-
binding lectin from Musa paradisiac (banana). Biochem. J.
272, 721– 726.
Koshte, V.L., Aalbers, M., Calkhoven, P.G., Aalberse, R.C., 1992.
The Potent IgG4-inducing antigen in banana is a mannose-
binding lectin, BanLec-I. Int. Arch. Allergy Immunol. 97,
Kritchevsky, D., Tepper, S.A., Klurfeld, D.M., 1998. Lectin may
contribute to the atherogenicity of peanut oil. Lipids 33,
Kumar, M.A., Timm, D.E., Neet, K.E., Owen, W.G., Peumans,
W.J., Rao, A.G., 1993. Characterization of the lectin from the
bulbs of Eranthis hyemalis (winter aconite) as an inhibitor of
protein synthesis. J. Biol. Chem. 268, 25176 25183.
Lajolo, F.M., Genovese, M.I., 2002. Nutritional significance of
lectins and enzyme inhibitors from legumes. J. Agric. Food
Chem. 50, 6592–6598.
Lavelle, E.C., 2001. Targeted delivery of drugs to the gastrointes-
tinal tract. Crit. Rev. Ther. Drug 18, 341386.
Lavelle, E.C., Grant, G., Pusztai, A., Pfuller, U., O’Hagan, D.T.,
2000. Mucosal immunogenicity of plant lectins in mice.
Immunology 2000, 3037.
Lavelle, E.C., Grant, G., Pusztai, A., Pfuller, U., O’Hagan, D.T.,
2001. The identification of plant lectins with mucosal adjuvant
activity. Immunology 102, 7786.
Leontowicz, H., Leontowicz, M., Kostyra, H., Kulasek, G., Gralak,
M.A., Krzeminski, R., Podgurniak, M., 2001. Effects of raw or
extruded legume seeds on some functional and morphological
gut parameters in rats. J. Anim. Feed Sci. 10, 169 183.
Liener, I.E., 1953. Soyin, a toxic protein from the soybean.
I. Inhibition of rat growth. J. Nutr. 49, 529 539.
Liener, I.E., 1986. Nutritional significance of lectins in the diet. In:
Liener, I.E., Sharon, N., Goldstein, I.J. (Eds.), The Lectins,
Academic Press, London, pp. 527552.
Liener, I.E., 1994. Implication of antinutritional components in
soybean foods. Crit. Rev. Food Sci. Nutr. 34, 31 67.
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403400
Liener, I., Young, M., Lovrien, R., 1986. Lectins inhibit digestive
enzymes and so survive alimentary passage. FASEB J. 45,
1573– 1573.
Lis, H., Sharon, N., 1998. Lectins: carbohydrate-specific proteins
that mediate cellular recognition. Chem. Rev. 98, 637 674.
Loc, N.T., Tinjuangjun, P., Gatehouse, A.M.R., Christou, P.,
Gatehouse, J.A., 2002. Linear transgene constructs lacking
vector backbone sequences generate transgenic rice plants
which accumulate higher levels of proteins conferring insect
resistance. Mol. Breed. 9, 231244.
Macedo, M.L.R., Mello, G.C., Freire, M.G.M., Novello, J.C.,
Marangoni, S., Matos, D.G.G., 2002. Effect of a trypsin
inhibitor from Dimorphandra mollis seeds on the development
of Callosobruchus maculatus larval. Plant Physiol. Bioch. 40,
891– 898.
Macedo, M.L.R., Freire, M.G.M., Cabrini, E.C., Toyama, M.H.,
Novello, J.C., Marangoni, S., 2003. A trypsin inhibitor from
Peltophorum dubium seeds active against pest proteases and its
effects on the survival of Anagasta kuehniellla (Lepidoptera:
Pyralidae). Biochim. Biophys. Acta 1621, 170182.
Machuka, J., Van Damme, E.J.M., Peumans, W.J., Jackai, L.E.N.,
1999. Effect of plant lectins on survival development of the pod
borer Maruca vitrata. Entomol. Exp. Appl. 93, 179187.
Machuka, J.S., Okeola, O.G., Chrispeels, M.J., Jackai, L.E.N., 2000.
The African yam bean seed lectin affects the development of the
cowpea weevil but does not affect the development of larvae of
the legume pod borer. Phytochemistry 53, 667674.
Maddock, S.E., Hufman, G., Isenhour, D.J., Roth, B.A., Raikhel,
N.V., Howard, J.A., Czapla, T.H., 1991. Expression in maize
plants of wheatgerm agglutinin, a novel source of insect
resistance, Third International Congress in Plant Molecular
Biology, Tucson, Arizona.
Maqbool, S.B., Riazuddin, S., Loc, N.T., Gatehouse, A.M.R.,
Gatehouse, J.A., Christou, P., 2001. Expression of multiple
insecticidal genes confers broad resistance against a range of
different rice pests. Mol. Breed 7, 85– 93.
Murdock, L.L., Shade, R.E., 2002. Lectins and protease inhibitors
as plant defense against insects. J. Agric. Food Chem. 50,
6605– 6611.
Nachbar, M.S., Oppenheim, J.D., 1980. Lectins in the United States
diet: a survey of lectins in commonly consumed foods and a
review of the literature. Am. J. Clin. Nutr. 33, 23382345.
Nakata, S., Kimura, T., 1985. Effect of ingested toxic bean lectins
on the gastrointestinal tract in the rat. J. Nutr. 115, 1621 1629.
Noah, N.D., Bender, A.E., Reaidi, G.B., Gilbert, R.J., 1980. Food
poisoning from red kidney beans. Brit. Med. J. 281, 236 237.
Nowell, P.C., 1960. Phytohemagglutinin: an initiator of mitosis in
cultures of normal human leukocytes. Cancer Res. 20, 462 –466.
Oka, Y., Chet, I., Spiegel, Y., 1997. Accumulation of lectins in
cereal roots invaded by the cereal cyst nematode Heterodera
avenae. Physiol. Mol. Plant P. 51, 333 345.
Okeola, O.G., Machuka, J., 2001. Biological effects of African yam
bean lectins on Clavigralla tomentosicollis (Hemiptera: Cor-
eidae). J. Econ. Entomol. 94, 724 729.
Oliveira, J.T.A., Pusztai, A., Grant, G., 1988. Changes in organs and
tissues induced by feeding of purified kidney Bean (Phaseolus
vulgaris) lectins. Nutr. Res. 8, 943947.
Oliveira, J.T.A., Vasconcelos, I.M., Gondim, M.J.L., Cavada, B.S.,
Moreira, R.A., Santos, C.F., Moreira, L.I.M., 1994. Canavalia
brasiliensis seeds. Protein quality and nutritional implications of
dietary lectin. J. Sci. Food Agric. 64, 417 424.
Oliveira, J.T.A., Vasconcelos, I.M., Bezerra, L.C.N.M., Silveira,
S.B., Monteiro, A.C.O., Moreira, R.A., 2000. Composition and
nutritional properties of seeds from Pachira aquatica Aubl,
Sterculia striata St Hil et Naud and Terminalia catappa Linn.
Food Chem. 70, 185191.
Olsnes, S., Wesche, J., Falnes, P., 1999. Binding, uptake, routing
and translocation of toxins with intracellular sites of action. In:
Alouf, J.E., Freer, J.H. (Eds.), The Comprehensive Sourcebook
of Bacterial Protein Toxins, Academic Press, London, pp.
Otte, J.M., Chen, C., Brunke, G., Kiehne, K., Schimitz, F., Foelsch,
U.R., Herzig, K.H., 2001. Mechanisms of lectin (phytohemag-
glutinin)-induced growth in small intestinal epithelial cells.
Digestion 64, 169178.
Palmer, R.M., Pusztai, A., Bain, P., Grant, G., 1987. Changes in
rates of tissue protein synthesis in rats induced in vivo by
consumption of kidney bean lectins. Comp. Biochem. Phys. 88,
Peumans, W.J., Van Damme, E.J.M., 1994. The role of lectins in the
plant defense against insects. In: Van Driessche, E., Fisher, J.,
Beeckmans, S., Bog-Hansen, T.C. (Eds.), Lectins: Biology,
Biochemistry, Clinical Biochemistry, Textop, Hellerup, Den-
mark, pp. 128141.
Peumans, W.J., Van Damme, J.M., 1995. Lectins as plant defense
proteins. Plant Physiol. 109, 347 352.
Peumans, W.J., Winter, H.C., Bemer, V., Van Leuven, F.,
Goldstein, I.J., Truffa-Cachi, P., Van Damme, E.J.M., 1997.
Isolation of a novel plant lectin with an unusual specificity from
Calystegia sepium. Glycoconj. J. 14, 259–265.
Powell, K.S., 2001. Antimetabolic effects of plant lectins
towards nymphal stages of the planthoppers Tarophagous
proserpina and Nilaparvata lugens. Entomol. Exp. Appl. 99,
Powell, K.S., Gatehouse, A.M.R., Hilder, V.A., Van Damme,
E.J.M., Peumans, W.J., Boonjawat, J., Horsham, K., Gatehouse,
J.A., 1995. Different antimetabolic effects of related lectins
towards nymphal stages of Nilaparvata lugens. Entomol. Exp.
Appl. 75, 6165.
Powell, K.S., Spence, J., Bharathi, M., Gatehouse, J.A., Gatehouse,
A.M.R., 1998. Immunohistochemical and developmental
studies to elucidate the mechanism of action of the snowdrop
lectin on the rice brown planthopper, Nilaparvata lugens (Stal).
J. Insect Physiol. 44, 529 539.
Preet, K., Punia, D., 2000. Proximate composition, phytic acid,
polyphenols and digestibility (in vitro) of four brown cowpea
varieties. Int. J. Food Sci. Nutr. 51, 189 193.
Pryme, I.F., Pusztai, A., Bardocz, S., Ewen, S.W.B., 1998. The
induction of gut hyperplasia by phytohaemagglutinin in the diet
and limitation of tumour growth. Histol. Histopathol. 13,
Pryme, I.F., Pusztai, A., Bardocz, S., Ewen, S.W.B., 1999. A
combination of dietary protein depletion and PHA-induced gut
growth reduce the mass of a murine non-Hodgkin lymphoma.
Cancer Lett. 139, 145–152.
Pusztai, A., 1989. Effects on gut structure, function and metabolism
of dietary lectins. The nutritional toxicity of the kidney bean
lectin. In: Franz, H., (Ed.), Advances in Lectin Research, VEB
Verlag Volk und Gesundheit, Berlin, pp. 74 86.
Pusztai, A., 1991. General effects on animal cells. In: Pusztai, A.,
(Ed.), Plant Lectins, Cambridge University Press, Cambridge,
pp. 105– 205.
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 401
Pusztai, A., Bardocz, S., 1996. Biological effects of plant lectins on
the gastrointestinal tract: metabolic consequences and appli-
cations. Trends Glycosci. Glyc. 8, 149 165.
Pusztai, A., Clarke, E.M.W., King, T.P., 1979. The nutritional
toxicity of Phaseolus vulgaris lectins. Proc. Nutr. Soc. 38,
115– 120.
Pusztai, A., Oliveira de, J.T.A., Bardocz, S., Grant, G., Wallace,
H.M., 1988. Dietary kidney bean lectin-induced hyperplasia and
increased polyamine content of the small intestine. In: Bog-
Hansen, T.C., Freed, D.L.J. (Eds.), Lectins, Biology, Biochem-
istry and Clinical Biochemistry, Sigma Library, St Louis, MO,
pp. 117–120.
Pusztai, A., Greer, F., Grant, G., 1989. Specific uptake of dietary
lectins into the systemic circulation of rats. Biochem. Soc. T. 17,
481– 482.
Pusztai, A., Grant, G., Spencer, R.J., Duguid, T.J., Brown, D.S.,
Ewen, S.W.B., Peumans, W.J., Van Damme, E.J.M., Bardocz,
S., 1993a. Kidney bean lectin-induced Escherichia coli over-
growth in the small-intestine is blocked by GNA, a mannose-
specific lectin. J. Appl. Bacteriol. 75, 360 368.
Pusztai, A., Ewen, S.W.B., Grant, G., Brown, D.S., Stewart, J.C.,
Peumans, W.J., Van Damme, E.J.M., Bardocz, S., 1993b.
Antinutritive effects of wheat-germ-agglutinin and other N-
acetylglucosamine-specific lectins. Brit. J. Nutr. 70,
313– 321.
Pusztai, A., Ewen, S.W.B., Carvalho, A.F.U., Grant, G., Brantner,
K., Bardocz, S., 1995. Dietary lectins affect hormone balance of
body and modulate its general metabolism. In: Singer, M.V.,
Ziegller, R., Rohr, G. (Eds.), Gastrointestinal Tract and
Endocrine System, Kluwer Academic Publishers, Lancaster,
pp. 457–463.
Pusztai, A., Koninkx, J., Hendriks, H., Kok, W., Hulscher, S., Van
Damme, E.J.M., Peumans, W.J., Grant, G., Bardocz, S., 1996.
Effect of the insecticidal Galanthus nivalis agglutinin on
metabolism and the activities of brush border enzymes in the
rat small intestine. J. Nutr. Biochem. 7, 677 682.
Pusztai, A., George, G., Gelencsar, E., Ewen, S.W.B., Pfueller, U.,
Eifler, R., Bardocz, S., 1998. Effects of an orally administered
mistletoe (type-2 RIP) lectin on growth, body composition,
small intestinal structure, and insulin levels in young rats.
J. Nutr. Biochem. 9, 3136.
´, Y., Febvay, G., 1993. Protein toxicity to aphids—an in
vitro test on Acyrthosiphon pisum. Entomol. Exp. Appl. 67,
149– 160.
´, Y., Sauvion, N., Febvay, G., Peumans, W.J., Gatehouse,
A.M.R., 1995. Toxicity of lectins and processing of ingested
proteins in the pea aphid Acyrthosiphon pisum. Entomol. Exp.
Appl. 76, 143155.
Radberg, K., Biernat, M., Linderoth, A., Zabielski, R., Pierzy-
nowski, S.G., Westrom, B.R., 2001. Enteral exposure to crude
red kidney bean lectin induces maturation of the gut in suckling
pigs. J. Anim. Sci. 79, 26692678.
Rao, K.V., Rathore, K.S., Hodges, T.K., Fu, X., Stoger, E.,
Sudhakar, D., Williams, S., Christou, P., Bharathi, M., Bown,
D.P., Powell, K.S., Spence, J., Gatehouse, A.M.R., Gatehouse,
J.A., 1998. Expression of snowdrop lectin (GNA) in transgenic
rice plants confers resistance to rice brown planthopper. Plant J.
15, 469–477.
Ratanapo, S., Ngamjunyaporn, W., Chulavatnatol, M., 1998. Sialic
acid binding lectins from leaf of mulberry (Morus alba). Plant
Sci. 139, 141148.
Renkonnen, K.O., 1948. Studies on hemagglutinins present in seeds
of some representatives of the family Leguminoseae. Ann. Med.
Exp. Fenn. 26, 66.
Reynoso-Camacho, R., De-Mejia, E.G., Loarca-Pina, G., 2003.
Purification and acute toxicity of a lectin extracted from tepary
bean (Phaseolus acutifolius). Food Chem. Toxicol. 41, 2127.
Rios, F.J.B., Cavada, B.S., Medeiros, D.A., Moreira, R.A.,
Vasconcelos, I.M., Oliveira, J.T.A., 1996. Digestibility of
plant lectins from Canavalia, Cratylia, Dioclea and Artocarpus
Genera. In: Van Driessche, E., Rouge
´, P., Beeckmans, S., Bog-
Hansen, T.C. (Eds.), Lectins: Biology, Biochemistry, Clinical
Biochemistry, Textop, Denmark, pp. 277–284.
Ripoll, C., Favery, B., Lecomte, P., Van Damme, E., Peumans, W.,
Abad, P., Jouanin, L., 2003. Evaluation of the ability of lectin
from snowdrop (Galanthus nivalis) to protect plants against
root-knot nematodes. Plant Sci. 164, 517523.
Rouanet, J.M., Besancon, P., Lafont, J., 1983. Effect of lectins from
leguminous seeds on rat duodenal enterokinase activity.
Experientia 39, 1356–1358.
Roy, A., Banerjee, S., Majumder, P., Das, S., 2002. Efficiency of
mannose-binding plant lectins in controlling a homopteran
insect, the red cotton bug. J. Agric. Food Chem. 50, 67756779.
¨diger, H., 1998. Plant lectins—more than just tools for
glycoscientists: occurrence, structure and possible functions of
plant lectins. Acta Anat. 161, 130 152.
Santos, L.F.L., 2001. Toxina da salsa (Ipomoea asarifolia R. et
Schult.): aspectos bioquı
´micos, estruturais, funcionais e poten-
cial biotecnolo
´gico. Doctoral thesis. Federal University of
´, Fortaleza, Brazil, pp. 142.
Sasaki, M., Fitzgerald, A.J., Grant, G., Ghatei, M.A., Wright, N.A.,
Goodlad, R.A., 2002. Lectins can reverse the distal intestinal
atrophy associated with elemental diets in mice. Aliment.
Pharm. Therap. 16, 633642.
Sauvion, N., Rahbe
´, Y., Peumans, W.J., Van Damme, E.J.M.,
Gatehouse, J.A., Gatehouse, A.M.R., 1996. Effects of GNA and
other mannose binding lectins on development and fecundity of
the peach-potato aphid Myzus persicae. Entomol. Exp. Appl. 79,
Sayegh, A.I., Ritter, R.C., 2003. Cholecystokinin activates specific
enteric neurons in the rat small intestine. Peptides 24, 237 –244.
Schuler, T.H., Poppy, G.M., Kerry, B.R., Denholm, I., 1998. Insect-
resistant transgenic plants. Trends Biotechnol. 16, 168174.
Setamou, M., Bernal, J.S., Legaspi, J.C., Mirkov, T.E., Legaspi,
B.C. Jr., 2002. Evaluation of lectin-expressing transgenic
sugarcane against stalkborers (Lepidoptera: Pyralidae): effects
on life history parameters. J. Econ. Entomol. 95, 469 477.
Sgarbieri, V.C., 1996. Propriedades nutricionais das proteı
´nas. In:
Sgarbieri, V.C., (Ed.), Proteinas em Alimentos Prote
Propriedades, Degradac¸o
˜es e Modificac¸o
˜es, Livraria Varela
Ltda, Sa
˜o Paulo, pp. 337386.
Small, G.J., Hemingway, J., 2000. Molecular characterization of the
amplified carboxylesterase gene associated with organopho-
sphorus insecticide resistance in the brown planthopper,
Nilaparvata lugens. Insect Mol. Biol. 9, 647– 653.
Stillmark, H., 1888. Ueber Ricin, ein giftiges Ferment aus dem
Samen von Ricinus communis L. und einigen anderen
Euphorbiaceen. Arb. Pharmak. Inst. Dorpat 3, 59 151.
Stoger, E., Williams, S., Christou, P., Down, R.E., Gatehouse, J.A.,
1999. Expression of the insecticidal lectin from snowdrop
(Galanthus nivalis agglutinin; GNA) in transgenic wheat plants:
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403402
effects on predation by the grain aphid Sitobion avenae. Mol.
Breed. 5, 6573.
Sun, X., Wu, A., Tang, K., 2002. Transgenic rice lines with
enhanced resistance to the small brown planthopper. Crop Prot.
21, 511–514.
Tang, K., Zhao, E., Sun, X., Wan, B., Qi, H., Lu, X., 2001.
Production of transgenic rice homozygous lines with enhanced
resistance to the rice brown planthopper. Acta Biotechnol. 21,
117– 128.
Tchernychev, B., Wilchek, M., 1996. Natural human antibodies to
dietary lectins. FEBS Lett. 397, 139142.
Thompson, L.U., Tenebaum, A.V., Hui, H., 1986. Effect of lectins
and the mixing of proteins on rate of protein digestibility. J. Food
Sci. 51, 150152.
Tinjuangjun, P., Loc, N.T., Gatehouse, A.M.R., Gatehouse, J.A.,
Christou, P., 2000. Enhanced insect resistance in Thai rice
varieties generated by particle bombardment. Mol. Breed. 6,
391– 399.
Tomov, B.W., Bernal, J.S., 2003. Effects of GNA transgenic
sugarcane on life history parameters of Parallorhogas pyralo-
phagus (Marsh) (Hymenoptera: Braconidae), a parasitoid of
Mexican rice borer. J. Econ. Entomol. 96, 570 576.
Triadou, N., Audran, E., 1983. Interaction of the brush-border
hydrolases of the human small intestine with lectins. Digestion
27, 17.
Van Damme, E.J.M., Peumans, W.J., Barre, A., Rouge
´, P., 1998.
Plant lectins: a composite of several distinct families of
structurally and evolutionary related proteins with diverse
biological role. Crit. Rev. Plant Sci. 17, 575692.
Van Damme, E.J.M., Hao, Q., Charels, D., Barre, A., Rouge
´, P.,
Van Leuven, F., Peumans, W.J., 2000. Characterization and
molecular cloning of two different type 2 ribosome-inactivating
proteins from the monocotyledonous plant Polygonatum multi-
florum. Eur. J. Biochem. 267, 2746 2759.
Vasconcelos, I.M., Maia, A.A.B., Siebra, E.A., Oliveira, J.T.A.,
Carvalho, A.F.F.U., Melo, V.M.M., Carlini, C.R., Castelar,
L.I.M., 2001. Nutritional study of two Brazilian soybean
(Glycine max) cultivars differing in the contents of antinutri-
tional and toxic proteins. J. Nutr. Biochem. 12, 1 8.
Vaughan, A., Hilder, V.A., Boulter, D., 1999. Genetic engineering
of crop plants for insect resistance—a critical review. Crop Prot.
18, 177– 191.
Wang, Z.B., Guo, S.D., 1999. Expression of two insect resistant
genes cryIA (bandc) GNA in transgenic tobacco plants results in
added protection against both cotton bollworm and aphids.
Chinese Sci. Bull. 44, 20512058.
Wang, W., Hause, B., Peumans, W.J., Smagghe, G., Mackie, A.,
Fraser, R., Van Damme, E.J.M., 2003. The Tn antigen-specific
lectin from ground ivi is an insecticidal protein with an unusual
physiology. Plant Physiol. 132, 13221334.
Williams, P.E.V., Pusztai, A., MacDearmid, A., Innes, G.M., 1984.
The use of kidney beans (Phaseolus vulgaris) as protein
supplements in diets for young rapidly growing beef steers.
Anim. Feed Sci. Tech. 12, 1 10.
Wilson, A.B., King, T.P., Clarke, E.M.W., Pusztai, A., 1980.
Kidney bean (Phaseolus vulgaris) lectin-induced lesions in the
small intestine. II. Microbiological studies. J. Comp. Pathol. 90,
Wu, A., Sun, X., Pang, Y., Tang, K., 2002. Homozygous transgenic
rice lines expressing GNA with enhanced resistance to the rice
sap-sucking pest Laodelphax striatellus. Plant Breed. 121,
Zhu, K., Huesing, J.E., Shade, R.E., Bressan, R.A., Hasegawa, P.M.,
Murdock, L.L., 1996. An insecticidal N-acetylglucosamine-
specific lectin gene from Griffonia simplicifolia (Leguminosae).
Plant Physiol. 110, 195 202.
Zhu-Salzman, K., Salzman, R., 2001. A functional mechanic of the
plant defensive Griffonia simplicifolia lectin II: resistance to
proteolysis is independent of glycoconjugate binding in the
insect gut. J. Econ. Entomol. 94, 12801284.
Narasimhan, M., Bressan, R.A., Hasegawa, P.M., Murdock,
L.L., 1998. Carbohydrate binding and resistance to proteolysis
control insecticidal activity of Griffonia simplicifolia lectin II.
Proc. Natl Acad. Sci. USA 95, 1512315128.
I.M. Vasconcelos, J.T.A. Oliveira / Toxicon 44 (2004) 385–403 403
... In many bacteria they intervene in pathogenic processes (13,14) and most of them are cytotoxic to intestinal cells usually by forming pores in the plasma membrane hence known as pore-forming toxins (PFTs) (13,15,16). On the other hand, plant enterotoxins are mostly toxic lectins, particularly abundant in seeds, that play a role in the defense against herbivory (17)(18)(19). Both bacteria Abbreviations: MACPF, Membrane Attack Complex/Perforin; PFT, pore-forming toxin; PVF, perivitelline fluid; PV2, perivitellin-2; SAXS, small angle X-ray scattering; CD, circular dichroism; BSA, bovine serum albumin; ISAD, image surface area difference; TEER, transepithelial electric resistance; PPs, Peyer's patches; i.p, intraperitoneally; CT, cholera toxin; Stxs, Shiga toxins; LT, heat-labile enterotoxin; HlyA, alpha-hemolysin; PsSC, scalarin. ...
... Both bacteria Abbreviations: MACPF, Membrane Attack Complex/Perforin; PFT, pore-forming toxin; PVF, perivitelline fluid; PV2, perivitellin-2; SAXS, small angle X-ray scattering; CD, circular dichroism; BSA, bovine serum albumin; ISAD, image surface area difference; TEER, transepithelial electric resistance; PPs, Peyer's patches; i.p, intraperitoneally; CT, cholera toxin; Stxs, Shiga toxins; LT, heat-labile enterotoxin; HlyA, alpha-hemolysin; PsSC, scalarin. and plant enterotoxins adversely affect gut physiology and/or morphology usually by cytotoxicity on intestinal cells, disruption of the brush border, and changes in the digestive, absorptive, protective or secretory functions, that could eventually lead to death (14,17,19). Moreover, some bacterial enterotoxins elicit inflammatory processes and immune system activation in mammals (14,15). ...
... In the present work, we were also able to detect orally ingested PmPV2 attached to the enterocyte glycocalyx of small intestine, indicating that the toxin reaches the intestinal mucosa in an active form. Binding to the mucosal surface may further protect this egg toxin from luminal digestive proteases as reported for plant enterotoxins (19). After binding, PmPV2 induced strong morphophysiological changes in the small intestine mucosa in <24 h. ...
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Gastropod Molluscs rely exclusively on the innate immune system to protect from pathogens, defending their embryos through maternally transferred effectors. In this regard, Pomacea snail eggs, in addition to immune defenses, have evolved the perivitellin-2 or PV2 combining two immune proteins into a neurotoxin: a lectin and a pore-forming protein from the Membrane Attack Complex/Perforin (MACPF) family. This binary structure resembles AB-toxins, a group of toxins otherwise restricted to bacteria and plants. Many of these are enterotoxins, leading us to explore this activity in PV2. Enterotoxins found in bacteria and plants act mainly as pore-forming toxins and toxic lectins, respectively. In animals, although both pore-forming proteins and lectins are ubiquitous, no enterotoxins have been reported. Considering that Pomacea snail eggs ingestion induce morpho-physiological changes in the intestinal mucosa of rodents and is cytotoxic to intestinal cells in culture, we seek for the factor causing these effects and identified PmPV2 from Pomacea maculata eggs. We characterized the enterotoxic activity of PmPV2 through in vitro and in vivo assays. We determined that it withstands the gastrointestinal environment and resisted a wide pH range and enzymatic proteolysis. After binding to Caco-2 cells it promoted changes in surface morphology and an increase in membrane roughness. It was also cytotoxic to both epithelial and immune cells from the digestive system of mammals. It induced enterocyte death by a lytic mechanism and disrupted enterocyte monolayers in a dose-dependent manner. Further, after oral administration to mice PmPV2 attached to enterocytes and induced large dose-dependent morphological changes on their small intestine mucosa, reducing the absorptive surface. Additionally, PmPV2 was detected in the Peyer's patches where it activated lymphoid follicles and triggered apoptosis. We also provide evidence that the toxin can traverse the intestinal barrier and induce oral adaptive immunity with evidence of circulating antibody response. As a whole, these results indicate that PmPV2 is a true enterotoxin, a role that has never been reported to lectins or perforin in animals. This extends by convergent evolution the presence of plant- and bacteria-like enterotoxins to animals, thus expanding the diversity of functions of MACPF proteins in nature.
... calcium and vitamin B-12, and contribute to the development of inflammatory, gastrointestinal, hormonal, and autoimmune conditions in some people(Akande, Doma, Agu, & Adamu, 2010;Ho, Tan, Daud, & Seow-Choen, 2012;Noonan & Savage, 1999;Vasconcelos & Oliveira, 2004). ...
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Background: While predominant dietary guidelines promote foods low in fat and high in carbohydrates, evidence links high carbohydrate consumption to adverse health effects in populations that are metabolically challenged by (pre)diabetes or metabolic syndrome. An increasing number of people report eating diets that limit carbohydrates. These diets are known as low carb or ketogenic diets. There is emerging advocacy of a specific variant of a ketogenic diet, the zero-carb diet, which aims to severely limit, or even exclude entirely, carbohydrate consumption. However, little empirical research has been dedicated to exploring the determinants of zero-carb diets and the views of the people that follow them. Objective: This study aimed to investigate the perspectives and experiences of people following zero-carb diets for at least 6 months. The study also aimed to elicit the salient beliefs that shape uptake and adherence to the diet. Methods: Zero-carb dieters (N = 170) recruited from a social media platform completed an open-ended survey comprising questions on beliefs and motives of following a zero-carb diet. Participant responses were thematically analysed. Results: Participants were driven by health concerns to uptake the diet and adhered to the diet for its health benefits. Moreover, participants also expressed a strong social identity and belongingness to the zero-carb community. Challenges largely centred on social stigma, lack of support from health-care providers and significant others, limited access to, and high cost of, foods, and lack of empirical support for the diet. Despite these challenges, participants reported strong intentions to follow the diet indefinitely. Conclusions: We recommend further research into the health benefits of zero-carb diets across settings and populations, and into developing guidelines for healthcare professionals to support individuals wishing to follow zero-carb diets.
... Experiments in neonatal rats have shown that anti-nutritional factors, such as lectins, block intestinal absorption (145), and oral provocation with the lectin PHA severely decreases endocytosis immediately after exposure (146,147), due to the binding to the epithelial surface (146,148,149). Hence, PHA is thought to have blocked epithelial "receptors" needed for endocytosis. ...
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The gut is an efficient barrier which protects against the passage of pathogenic microorganisms and potential harmful macromolecules into the body, in addition to its primary function of nutrient digestion and absorption. Contrary to the restricted macromolecular passage in adulthood, enhanced transfer takes place across the intestines during early life, due to the high endocytic capacity of the immature intestinal epithelial cells during the fetal and/or neonatal periods. The timing and extent of this enhanced endocytic capacity is dependent on animal species, with a prominent non-selective intestinal macromolecular transfer in newborn ungulates, e.g., pigs, during the first few days of life, and a selective transfer of mainly immunoglobulin G (IgG), mediated by the FcRn receptor, in suckling rodents, e.g., rats and mice. In primates, maternal IgG is transferred during fetal life via the placenta, and intestinal macromolecular transfer is largely restricted in human neonates. The period of intestinal macromolecular transmission provides passive immune protection through the transfer of IgG antibodies from an immune competent mother; and may even have extra-immune beneficial effects on organ maturation in the offspring. Moreover, intestinal transfer during the fetal/neonatal periods results in increased exposure to microbial and food antigens which are then presented to the underlying immune system, which is both naïve and immature. This likely stimulates the maturation of the immune system and shifts the response toward tolerance induction instead of activation or inflammation, as usually seen in adulthood. Ingestion of mother's milk and the dietary transition to complex food at weaning, as well as the transient changes in the gut microbiota during the neonatal period, are also involved in the resulting immune response. Any disturbances in timing and/or balance of these parallel processes, i.e., intestinal epithelial maturation, luminal microbial colonization and mucosal immune maturation due to, e.g., preterm birth, infection, antibiotic use or nutrient changes during the neonatal period, might affect the establishment of the immune system in the infant. This review will focus on how differing developmental processes in the intestinal epithelium affect the macromolecular passage in different species and the possible impact of such passage on the establishment of immunity during the critical perinatal period in young mammals.
... The nematicidal effects of bean and soybean hulls may be attributed to the presence of lectins, commonly found in legumes (Vasconcelos & Oliveira, 2004;Corredor et al., 2016). This protein reduces nematode movement in soil by altering the conformation of nematode chemoreceptors, thereby affecting the ability of nematodes to locate and penetrate plant roots (Marban-Mendoza et al., 1987;Gaofu et al., 2008). ...
Nematodes of the genus Meloidogyne are one of the major limiting factors in tomato production and a challenging problem in organic systems. This study aimed to investigate the effect of agro-industrial wastes, their forms of application and doses on tomato plants inoculated with Meloidogyne javanica . First, nematodes were multiplied on tomato under glasshouse conditions to simulate a naturally infested environment. At 60 days after inoculation, plant shoots were removed, new seedlings were transplanted into the pots, and the soil was amended with agro-industrial wastes. Treatments were as follows: rice husk, common bean hull, soybean hull, orange bagasse, poultry litter and waste mixture (wastes mixed in equal proportions) applied in three different forms (raw, powdered and biodigester effluent). A non-treated control and a composted waste mixture were also assessed. At 60 days after transplanting, plants were evaluated for nematode parameters. Powdered bean hulls, soybean hulls, orange bagasse and waste mixture provided the best results and were selected for dose-response investigations. A second experiment was conducted in two periods using, in addition to the selected wastes, a mixture of powdered bean hulls, soybean hulls and orange bagasse. Wastes were applied at doses of 0 (control), 2, 4, 6 and 8 t ha ⁻¹ . Powdered bean hulls, soybean hulls, orange bagasse and waste mixtures at 5 t ha ⁻¹ gave the best nematode control, with reductions of 55-100%. The optimal doses for vegetative growth were 4 t ha ⁻¹ in the first period and 5 t ha ⁻¹ in the second period.
... pea, lentil, bean [Phaseolus vulgaris], peanut [Arachis hypogaea] and soybean). Lectins are resistant to digestion and, when ingested, are known to bind to the cell linings of the digestive tract where they can prevent the absorption of digested proteins and other nutrients (Peumans & Van Damme, 1995;Vasconcelos & Oliveira, 2004). They are mostly found in the outer layers of seeds (e.g. ...
Background: Proteins are essential macronutrients of the human diet. Currently, major dietary sources in developed countries are of animal origin. However, the association of red meat consumption to the increased risks of some health conditions and its unsustainable pressure on the environment have increased the interest in plant proteins as healthier and sustainable alternatives. Of these, legumes have a great potential, but part of their proteins are indigestible due to interaction with other components such as phytate and polyphenols. As such, the quest to improve protein accessibility has become of interest to many researchers. Germination is proposed to be a bioprocess method to improve protein digestibility and protein biological properties. Scope and approach: This review discusses the importance of plant proteins and the hindrance of protein digestibility. This paper also highlights the role of germination in the deactivation of antinutritional factors, hydrolysis of indigestible proteins, and improvement of properties and content of proteins of different legume seeds. Key findings and conclusions: Protein digestibility is dependent on the nature of antinutritional factors (e.g. trypsin inhibitors and phytate) in the food matrix. Germination represses the activity of trypsin inhibitors and removes the phytate-related inhibition through hydrolysis. Protein content increases in germinated seeds when compared to non-germinated ones, suggesting that proteins were either hydrolysed or dissociated from antinutritional factors. Germination seems like an adequate bioprocessing method to improve the content and nutritional quality of legume seed proteins.
... Although lecithin concentration is reduced by heat, its susceptibility depends on its nature; thus, lecithin requires longer heating period for complete denaturation (Rüdiger and Gabius 2001). Appetite and weight losses and eventually mortality are the most common clinical signs in animals fed plant-derived lecithins (Vasconcelos and Oliveira 2004). In the present study, only weight loss was observed as a characteristic clinical sign of lecithin presence. ...
The study aimed to evaluate heat-treated bean residue meal (Phaseolus vulgaris)—BRM—as an alternative protein source in diets for Nile tilapia fish. A completely randomized design was used, totaling four (n = 4) dietary treatments: diet without BRM (CON), raw BRM (RBRM) and heat-treated BRM at 100 °C for 15 min (BRM15), and 30 min (BRM30) before inclusion in diets. Nile tilapia fingerlings (1.3 g initial weight) were hand-fed the experimental diets for 66 days, divided equally into three meals per day. Performance parameters, body composition, nutrient retention, and physical characteristics of diets were evaluated. Growth and feed conversion were lower (P < 0.05) in fish fed BRM. Protein productive value was higher (P < 0.05) in fish fed CON diet than in fish receiving BRM. However, 30 min heat treatment of BRM increased (P < 0.05) protein retention in fish. Fish fed BRM30 also had higher protein content (P < 0.05) and reduced body lipid content (P < 0.05) than those fed CON diet. The physical characteristics (durability, dry matter leaching, waterproof time, and water stability time) were significantly improved (P < 0.05) in the BRM30 diet compared with other dietary treatments. The dietary inclusion of BRM at the level of 15% is not recommended for tilapia due to low growth performance and feed efficiency, regardless of preheating treatment. However, research on longer heat treatment time is needed due to the improvements observed in nutrient retention and physical characteristics of diets.
Today global agriculture is facing downfall in total production and one of the critical factors for less productivity is food crop damages caused by insects and pests. Food availability is one of the major objectives to make food security attainable to people of the world and thereby huge money is spent every year to control the population of crop-damaging insects. Despite all the insect–pest control measures, there are considerable losses in agricultural crops every year. A chunk of money is spent worldwide on the use of agrochemicals which not only pollute the environment but also pose severe threats to human and animal health. Additionally, their injudicious and indiscriminate uses have also become responsible for resurgence and resistance in insects in many corners of the world. Therefore, it becomes necessary to control the population densities of crop-damaging insects by employing more programmed, eco-friendly, and effective crop protection strategies.
Plant parasitic nematodes are responsible for causing significant damages to various commercial crops. At present, several management strategies are applied such as biological, chemical, organic, cultural, nanobiotechnology to control pathogenic nematodes. Use of nematicides of chemical origin are although effective, on another hand it causes environmental perturbations. The emerging of two novel techniques, nanotechnology and biotechnology has resolved many concerns that prevail with the traditional strategies of nematode managements in plants and environment. Nanotechnology based agricultural systems have developed with a worthy scope to manage phytonematodes using drug-carrier and a controllable drug targeting and releasing system as it can enhance the quality of life and world’s economy. Through advancement in nanotechnology, there are a number of state of-the-art techniques available including applications of several types of nanoparticles as protectants and carriers in the form of ‘nanonematicide’. Several pathogenic phytonematodes are very effectively managed with the means of nanotechnology. Genetic engineering have evolved as a promising field in the management of plant pathogenic nematodes by the means of gene cloning and gene modification of host plants. Various transgenics plants have been developed so far against plant pathogenic nematodes. The key objective of the genetic manipulation would be to control all possible physiological and biological activities of nematode due to the counter effect of host plants by possessing resistance gene/s on the basis of gene for gene concept. There are several proteinase inhibitors genes which have been identified and transferred into host plants to create resistance against pathogenic nematodes. Nematicidal proteins are also considered as “anti-nematode proteins” can directly inhibit the multiplication of pathogenic nematodes. Protein from Bacillus thuringiensis, lectins and some antibodies are regarded as nematicidal proteins. Similarly, other house-keeping genes have been manipulated through RNA interference technique. There are many benefits from the integration of both disciplines i.e. nanotechnology and biotechnology for the management of pathogenic nematodes. Some important issues are yet to be addressed which needs proper and extensive research
An insecticidal mannose binding lectin gene of Withania somnifera, WsMBP1 was constitutively expressed in tobacco plants. Instar-wise study on the response of Hyblaea puera larvae to the total protein extracted from transgenic tobacco was conducted and survivability percent was 33.33% and 55.55% in the first and the second instars, respectively. Minimum survivability of 22.22% was registered in the third instar. Further, two-fold reduction was observed in mean pre-pupal and pupal weight in the third instar larval populations fed with lectin protein compared to the control populations. The functional confirmation of the insecticidal activity of WsMBP1 established its potential as a novel gene resource for future transformation studies in developing teak genotypes tolerant to its leaf defoliator, H. puera.
Literature Review
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Aphid parasitoids are important biological control agents. The possibility arises that whilst foraging on insect-resistant transgenic plants, they are themselves at risk from direct and indirect effects of the expression of a transgene used to control the pest species. A liquid artificial diet was successfully used to deliver the snowdrop lectin (Galanthus nivalis agglutinin; GNA) to the peach-potato aphid, Myzus persicae. Bioassays utilising artificial diet incorporating GNA, and excised leaves of the GNA-expressing transgenic potato line, GNA2#28, were performed to assess the potential effects of GNA on the development of the aphid parasitoid Aphidius ervi. The results indicate that GNA delivered via artificial diet to the aphids can be transferred through the trophic levels and has a dose-dependent effect on parasitoid development. Parasitoid larvae excreted most of the ingested GNA in the meconium but some of it was detected in the pupae. Although A. ervi development was not affected when developing within hosts feeding on transgenic potato leaves, this probably reflected sub-optimal expression of the toxin in the transgenic potato line used
Transgenic rice lines containing the snowdrop (Galanthus nivalis) lectin gene (GNA) were investigated for the stability of expression of the GNA gene in the sixth (R6) generation. Western blot analysis revealed that GNA was stably expressed among the R6 individual plants at comparable levels with those from their parental lines. Insect bioassay tests of two independent transgenic rice homozygous R6 lines (Nos. 1 and 2) showed that both lines caused significant inhibition to the rice small brown planthopper (Laodelphax striatellus, SBPH) by decreasing SBPH survival, overall fecundity and retarding its development. These SBPH-resistant lines have been incorporated into a rice insect resistance breeding program for the control of SBPH. This is the first report that transgenic rice lines expressing GNA conferred enhanced resistance to SBPH.
Possible factors responsible for the initiation of mitotic activity in “gradient” cultures of leukocytes from normal human blood were investigated. Variations of temperature, pH, oxygen tension, carbon dioxide tension, plasma and cell concentrations, as well as the amount of agitation, over at least as wide a range as might be encountered in vivo, produced only moderate quantitative changes in mitotic activity. The mucoprotein plant extract, phytohemagglutinin (PHA), employed originally as a means of separating the leukocytes from whole blood in preparing the cultures, was found to be a specific initiator of mitotic activity: in its presence, cell division occurred; in its absence, no mitoses appeared. The studies suggest that the mitogenic action of PHA does not involve mitosis per se but rather the stage preceding mitosis—the alteration of circulating monocytes and large lymphocytes to a state wherein they are capable of division. The relationship of this mitogenic action of PHA to mitotic and premitotic processes in the body remains to be investigated. © 1960, American Association for Cancer Research. All rights reserved.
The influence of leupeptin, a cysteine and serine proteinase inhibitor, on alfalfa weevil, Hypera postica (Gyllenhal), growth and development was investigated over nine successive generations. Concern that ingestion of proteinase inhibitors by phytophagous insects could induce production of inhibitor-insensitive proteinase activity initiated this investigation. The percent alfalfa weevil larval, pupal and adult survival, and defoliation was significantly lower on alfalfa foliage treated with leupeptin than on untreated foliage in all nine generations tested. Main effects for generations and treatment times generation were nonsignificant for all variables. This study demonstrates that after nine generations leupeptin, when compared to an untreated control, does not lose its ability to significantly inhibit alfalfa weevil growth and development. This suggests that the alfalfa weevil did not utilize or induce other proteinases (digestive enzymes) to compensate for inhibition of one of its major proteinases.
The effects of extruding soya bean, faba bean and pea seeds on trypsin inhibitor (TI) and lectin activities, dry matter and protein digestibilities, pancreatic trypsin activity, relative weight of rat internal organs, and microbiology and histology of the jejunum were studied. Wistar rats were fed semipurified diets containing 10% of legume seeds: raw (R) or extruded at 150°C (E). Extrusion reduced TI activity of soya bean seeds from 31.3 to 23.0, faba bean from 2.1 to 0.7, and pea from 2.3 to 0.3 TIU/mg. Extrusion of soya bean seeds also reduced agglutination activity against guinea pig erythrocytes. Extrusion of soya bean, but not of pea and faba bean, improved apparent digestibility of dry matter and protein (P≤0.01). Pancreas weight (0.392% BW) and trypsin activity (0.424 U/total pancreas) were the highest in rats fed the diet with raw soya bean. Extrusion increased (P≤0.05) trypsin activity in the pancreas of rats fed on all seeds (mean value 2777 vs 3212 U/100 g protein) and decreased (P≤0.05) total protein content (mean 13.0 vs 10.6 mg/pancreas) as well as the relative weight of the pancreas. Significant differences were found between the relative weights of several organs in rats fed on pea, faba bean or soya bean diets. Extrusion of faba bean reduced the E. coll count in the small intestine and tended to decrease damage to intestinal villi.