Pro-inflammatory effect in mice of CvL, a lectin from the marine sponge Cliona varians.
ABSTRACT CvL, a lectin from the marine sponge Cliona varians agglutinated type A papainized erythrocytes and was strongly inhibited by d-galactose and sucrose. Models of leukocyte migration in vivo were used to study the inflammatory activity of CvL through of mouse paw oedema and peritonitis. Effect of CvL on peritoneal macrophage activation was analysed. Effects of corticoids and NSAIDS drugs were also evaluated on peritonitis stimulated by CvL. Results showed that mouse hind-paw oedema induced by subplantar injections of CvL was dose dependent until 50 microg/cavity. This CvL dose when administered into mouse peritoneal cavities induced maxima cell migration (9283 cells/microL) at 24 h after injection. This effect was preferentially inhibited by incubation of CvL with the carbohydrates d-galactose followed by sucrose. Pre-treatment of mice with 3% thioglycolate increases the peritoneal macrophage population 2.3 times, and enhanced the neutrophil migration after 24 h CvL injection (75.8%, p<0.001) and no significant effect was observed in the presence of fMLP. Finally, pre-treatment of mice with dexamethasone (cytokine antagonist) decreased (65.6%, p<0.001), diclofenac (non-selective NSAID) decreased (34.5%, p<0.001) and Celecoxib (selective NSAID) had no effect on leukocyte migration after submission at peritonitis stimulated by CvL, respectively. Summarizing, data suggest that CvL shows pro-inflammatory activity, inducing neutrophil migration probably by pathway on resident macrophage activation and on chemotaxis mediated by cytokines.
- SourceAvailable from: int-res.comDiseases of Aquatic Organisms - DISEASE AQUAT ORG. 01/1994; 20:127-136.
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ABSTRACT: A novel lectin from Talisia esculenta seeds (TEL) has recently been purified and characterized. In this study we investigated the proinflammatory activity of TEL in mice using both the air-pouch and peritoneal cavity as well as paw oedema models. TEL (10-40 microg) induced significant neutrophil and mononuclear cell recruitment when injected into either mouse air-pouch or peritoneal cavity. The neutrophil accumulation into the air-pouch was dose- and time-dependent with a maximal response at 16 h, returning to control levels at 72 h whereas maximal mononuclear cell accumulation was observed at 24 h after TEL injection. The same profile of neutrophil accumulation was observed when this lectin was injected into mouse peritoneal cavity, although the maximal mononuclear cell recruitment was observed 48 h after TEL injection. Additionally, TEL (12.5-200 microg/paw) caused a dose-dependent mice paw, as evaluated at 4 h after the lectin injection. D-mannose, better than D-glucose, significantly inhibited TEL-induced neutrophil migration into the peritoneal cavity or air-pouch. D-galactose had no effect on TEL-induced neutrophil migration in either cavity studied. On the other hand, D-mannose slightly inhibited the TEL-induced paw oedema, whereas neither D-glucose nor D-galactose affected this phenomenon. In conclusion, our data show that TEL induces neutrophil and mononuclear cell accumulation by a mechanism related to their specific sugar-binding properties.Toxicon 10/2003; 42(3):275-80. · 2.92 Impact Factor
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ABSTRACT: A lectin from the Adriatic sponge Haliclona cratera was purified by ion-exchange and gel chromatography. The molecular mass of the lectin is approximately 29 kDa. Purified lectin is rich in hydrophobic and basic amino acids and has an isoelectric point at pH 8.6. H. cratera lectin is relatively heat- and pH-stable. It agglutinates native and trypsinized, papainized and neuraminidase-treated human A, B, O, AB and sheep erythrocytes, and the hemagglutinating activity is independent of Ca(2+), Mn(2+) and Mg(2+) ions; D-galactose and N-acetyl-D-galactosamine are found to be moderate inhibitors of the activity. H. cratera lectin displays cytotoxic effect on HeLa and FemX cells and weak mitogenic effect on human T-lymphocytes pretreated with phytohemagglutinin (PHA).Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology 07/2002; 132(2):213-21. · 2.71 Impact Factor
Pro-inflammatory effect in mice of CvL, a lectin from the
marine sponge Cliona varians
Alexandre F.S. Queiroza, Raniere M. Mourab, Jannison K.C. Ribeiroc, Ibson L. Lyrac,
Dayse C.S. Cunhac, Elizeu A. Santosc, Maurício. P. de-Salesc,⁎
aDepartamento de Biofísica e Farmacologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil
bDepartamento de Bioquímica e Biologia Molecular, Centro de Ciências, Universidade Federal do Ceará, Fortaleza, CE, Brazil
cDepartamento de Bioquímica, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus Universitário, 59072-970, Natal, RN, Brazil
Received 21 August 2007; received in revised form 18 September 2007; accepted 18 September 2007
Available online 26 September 2007
CvL, a lectin from the marine sponge Cliona varians agglutinated type A papainized erythrocytes and was strongly inhibited by D-galactose
and sucrose. Models of leukocyte migration in vivo were used to study the inflammatory activity of CvL through of mouse paw oedema and
peritonitis. Effect of CvL on peritoneal macrophage activation was analysed. Effects of corticoids and NSAIDS drugs were also evaluated on
peritonitis stimulated by CvL. Results showed that mouse hind-paw oedema induced by subplantar injections of CvL was dose dependent until
50 μg/cavity. This CvL dose when administered into mouse peritoneal cavities induced maxima cell migration (9283 cells/μL) at 24 h after
injection. This effect was preferentially inhibited by incubation of CvL with the carbohydrates D-galactose followed by sucrose. Pre-treatment of
mice with 3% thioglycolate increases the peritoneal macrophage population 2.3 times, and enhanced the neutrophil migration after 24 h CvL
injection (75.8%, pb0.001) and no significant effect was observed in the presence of fMLP. Finally, pre-treatment of mice with dexamethasone
(cytokine antagonist) decreased (65.6%, pb0.001), diclofenac (non-selective NSAID) decreased (34.5%, pb0.001) and Celecoxib (selective
NSAID) had no effect on leukocyte migration after submission at peritonitis stimulated by CvL, respectively. Summarizing, data suggest that CvL
shows pro-inflammatory activity, inducing neutrophil migration probably by pathway on resident macrophage activation and on chemotaxis
mediated by cytokines.
© 2007 Elsevier Inc. All rights reserved.
Keywords: Marine sponge; Cliona varians; Leukocyte migration; Paw oedema; Peritonitis
possessing an ability to specifically bind carbohydrate moieties
in vitro migration of specific leukocytes migration in various
Coelho et al., 2006; Napimoga et al., 2007).
The inflammatory process is a phenomenon that involves
vascular and cellular events and can be defined as a generalized,
nonspecific but beneficial response of tissues to injury due to
bacteria, virus, and/or parasites, chemical irritants, ultraviolet
light irradiation, and nondigestive particles (O'Byrne et al.,
2000; O'Byrne and Dalgleish, 2001; Dalgleish and O'Byrne,
2002), which can initiate this process that leads to chronic and
acute diseases in mammalians. This complex process involves a
variety of leukocyte type cells (macrophage, mononuclear cells
and neutrophil) and probably dozens of inflammatory mole-
cules, such as nitric oxide (NO), pro-inflammatory cytokines
(TNF-a, IL-1, IL-12, IFN-γ), and chemokines (Key et al., 1982;
Adams and Hamilton, 1984). Adhesion to the endothelium is a
prerequisite for the movement of leukocytes from blood into
affected tissues (Colditz 1985), that is mediated by membrane
lectins in association with carbohydrate moieties present in
specific leukocytes, providing the adhesion to vascular endo-
thelial cells and the emigration of leukocytes to tissues, that is a
feature of the inflammatory process (Tedder et al., 1995).
Available online at www.sciencedirect.com
Comparative Biochemistry and Physiology, Part C 147 (2008) 216–221
⁎Corresponding author. Tel.: +55 84 32153415; fax: +55 84 32119208.
E-mail address: email@example.com (M.P. de-Sales).
1532-0456/$ - see front matter © 2007 Elsevier Inc. All rights reserved.
In marine animals, only a few phyla have been screened for
the presence and distribution of lectins. In particular,the number
of lectins that have isolated from invertebrate organisms is quite
small as compared with the great variety of lectins isolated from
plant origin and have been limited to those partially character-
Since the discovery of hemagglutinins in sponges by Dodd et al.
(1968), there have been some reports on the purification and
partial characterization of lectins from the oldest multicellular
animals (Bretting and Kabat, 1976; Diehlseifert et al., 1985;
Kamiya et al., 1986; Kamiya et al., 1990).
The biotechnological potential of Cliona varians sponge,
based in proteins, was first showed by us when Moura et al.
(2006) demonstrated that a lectin purified from C. varians (CvL)
displayed a cytotoxic effect on gram positive bacteria, such as
Bacillus subtilis and Staphylococcus aureus and agglutinated
Leishmania chagasi promastigotes. These findings were indica-
tiveofthe physiological defense roles ofCvL andits possibleuse
in the antibiosis of bacteria and protozoa pathogenic.
In this study we purified a lectin from invertebrate of marine
origin and investigated its effect on the neutrophil migration
in peritoneal macrophages and emigrant neutrophils activation.
2. Materials and methods
The Animal Care Unit of the Universidade Federal do Ceará,
Fortaleza, CE, Brazil supplied Winstar mice, weighing 25–35 g.
The animals had free access to food and water and were kept in
standardized environmental conditions on a 12/12-h light/dark
cycle. Before each test, the animals were fasted for at least 12 h.
Adult specimens of the marine sponge C. varians were
collected in the littoral of Santa Rita beach, Extremoz located at
Rio Grande do Norte state, Brazil. Specimens were collected
and transported in ice to the laboratory and stored at 20 °C until
2.2. Purification of marine sponge C. varians lectin (CvL)
Methodology developed by Moura et al. (2006) was used to
purify CvL from C. varians marine sponge. The haemagglu-
tinating activity was assayed in microtiter V plates (Nunc Brand
products, Denmark) according to a twofold serial dilution
procedure (Debray et al., 1981). The erythrocytes used were
treated with papain according to Benevides et al.(1998).
2.3. CvL-induced rat paw oedema
Acute inflammation was tested on oedema induced by CvL
in mice. Animals, allocated to treatment in groups of six, were
injected into the plantar surface of the right hind paw of the mice
(100 μL containing 5, 10 and 50 μg of CvL, dissolved in 0.15 M
NaCl). While the contralateral paw was injected with 100 μL
saline solution. Carrageenan (0.1 mL of a 1% 0.15 M NaCl) was
injected into the plantar surface of the right hind paw of the mice
(control). The paws were amputated at the tarsocrural joint and
weighted on an analytical balance (Freire et al., 2003) and
difference between the left and the right paw oedema indicated
the degree of inflammation after a period of 4 h. The average
(mean±S.E.M.) increase in paw oedema of each group was
2.4. Stimulation of leukocyte migration into peritoneal cavities
CvL was injected intraperitoneally (i.p.) at 50 μg/cavity in
0.1 mL of 0.15 M NaCl in six mice. Two control groups were
made with six mice each: negative control group received the
offMLPinsubstitution ofthe lectinsolution. Four, 12, 24, 48, 72
and 96 h later, animals were sacrificed and peritoneal cells
harvested by washing each peritoneal cavity with 3 mL of saline
containing 5 UI/mL heparin. Total cell counts were performed as
described elsewhere (Desouza and Ferreira, 1985). The results
were reported as mean±S.E.M. of the number of cells per mL of
peritoneal wash. The average (mean±S.E.M.) of each group was
2.5. Effect of D-galactose, D-sucrose and D-fructose on the cell
migration induced by CvL
CvL (50 μg) was dissolved in 100 μL of sterile saline solution
containing either 0.2 M D-galactose or 0.2 M D-sucrose or 0.2 M
D-fructose and incubated by 30 min and injected into mice
peritonealcavities.Theeffects were evaluated24hafter injection
and compared to the saline-treated control group and group
treated with the carbohydrates. The average (mean±S.E.M.) of
each group was calculated.
2.6. Increase of the peritoneal macrophage population by
treatment with thioglycolate
Thioglycolate (3%, w/v; 100 μL i.p.) was injected into the
peritoneal cavities and, after 4 days, peritoneal macrophages
were collected, counted and compared to those from a group of
non-treated animals (control) (Ribeiro et al., 1991). Saline
(100 μL /cavity) or CvL (50 μg/cavity in 100 μL of saline), was
then injected into mice (control and Tg treated), and 24 h later,
the neutrophil migration was evaluated. The average (mean±
S.E.M.) of each group was calculated.
2.7. Effect of pharmacological modulators on the neutrophil
migration induced by CvL
The following drugs were used: (1) cytokine antagonist
dexamethasone (0.5 mg/kg); (2) selective NSAID Celecoxib
(2.8 mg/kg); (3) non-selective NSAID diclofenac (1 mg/kg).
(50 μg/100 μL) was injected in the saline-treated animals and in
animals previously treated with pharmacological modulators.
Neutrophil migration was evaluated 4 h after injections and
compared to the respective controls.
217 A.F.S. Queiroz et al. / Comparative Biochemistry and Physiology, Part C 147 (2008) 216–221
2.8. Statistical analysis
All results were expressed as mean values±S.E.M. for n
experiments. Statistical evaluation was undertaken by analysis
comparisons. A p value of less than 0.001 was considered
3.1. Induction of mice paw oedema by CvL
The injection of CvL (5, 10 and 50 μg/paw) induced a dose-
dependent oedema in paw mice when compared with the
negative control group (0.15 M NaCl solution) (Fig. 1) and at
50 μg/paw dose was observed higher oedema induction when
comparedwith positive control(1%Carrageenan solution).This
dose was used in posterior assays.
3.2. Induced leukocyte migration into peritoneal cavities by
of leukocyte migration, in acute phase (4 h post-injection), when
compared with negative control (saline solution) and similar to
curve had a maximal leukocyte migration at 24 h post-CvL
injection, decreasing until 48 h, maintaining constant until 72 h
level 10 times higher when compared to negative control (saline
solution) (Fig. 2).
3.3. Effect of carbohydrate on CvL-inducedleukocyte migration
CvL, dissolved in 100 μL of 0.2 M D-galactose and sucrose
and D-fructose solutions, was injected into the mouse peritoneal
cavity at the dose 50 μg/cavity. After 24 h, results showed that
D-galactose nearly abolished the CvL-induced leukocyte
migration, followed by D-glucose and D-galactose migration.
On the other hand, sucrose partly (but not significantly)
inhibited effect on CvL-induced leukocyte migration in
peritoneal cavity (Fig. 3). When injected alone into the mice
peritoneal cavity, these carbohydrates had no significant effect
in the number of leukocyte compared with saline solution.
3.4. Thioglycolatetreatment potentiates the neutrophil migration
induced by CvL
The role of macrophages on the lectin-induced neutrophil
of these cells. Intraperitoneal injection of 3% thioglycolate 72 h
before in mice increased the macrophage population 2.3 times.
with thioglycolate, increased by 77% neutrophil migration in the
peritoneal cavity (Fig. 4).
3.5. Cytokines antagonist (dexamethasone), but no selective
NSAID (Celecoxib) inhibited neutrophil migration induced
Effect of the selective NSAID (Celecoxib), non-selective
NSAID (diclofenac) and cytokine antagonist (dexamethasone)
injected i.p 1 h before administration of the CvL on induction of
neutrophil migration was tested. Selective NSAID (Celecoxib)
had no effect, whereas non-selective NSAID (diclofenac) and
dexamethasone inhibited significantly by 34.5% and 66%,
respectively, the number of neutrophils that migrated to the
peritoneal cavity of animals (Fig. 5).
Bioactive proteins such as lectins have been isolated from
various marine invertebrate, including the Porifera. The lectin,
Fig. 1. Mouse paw oedema induced by CvL. Dose-dependent oedema with
doses varying from 5 to 50 μg/paw analysed 4 h after the injection of the stimuli
(gray bars). Controls: 1% Carrageenan (black bar) and saline solution (white
bar). The data are the mean±S.E.M. of six mice.⁎pb0.01 indicate that there
were significant statistical differences compared to saline group (ANOVA–
Fig. 2. Effect of CvL on cells migration into peritoneal cavity. Time course of
leukocyte migration induced by CvL (50 μg/cavity, ●) analysed at 4, 12, 24, 48,
72 and 96 h after the injections into peritoneal cavity. Controls: Saline solution
(○) and fMLP (0.05 μg/cavity, ♦). The data were the mean±S.E.M. of six mice.
The same letters indicate that there were no significant statistical differences,
compared to saline group (pb0.01, ANOVA–Bonferroni).
218A.F.S. Queiroz et al. / Comparative Biochemistry and Physiology, Part C 147 (2008) 216–221
such as Cinachyrella alloclada (Atta et al., 1989), Pellina
1992) and Haliclona cratera (Pajic et al., 2002). The binding
property of the CvL was found to be preferential for D-galactose.
A considerable number of marine invertebrate lectins, including
those isolated from sponges, were reported to react with D-
galactose (Bretting et al., 1981; Schröder et al., 1990) and this
responses in marine animals (Yousif et al., 1994; Mistry et al.,
2001; Kurata and Hatai, 2002).
Various exogenous lectins, especially those from plant origin,
system, especially those with specificity to monosaccharides D-
galactose and D-mannose (Bento et al., 1993; Benjamin et al.,
1997; Alencar et al., 2003). In the present work we have inves-
tigated effect of a D-galactose specific lectin from marine animal
origin on the in vivo leukocyte migration, an important cellular
results showed that CvL caused a significant dose-dependent
mouse paw oedema and that at dose of 50 μg/paw was
significantly higher than 1% Carrageenan used as positive
control. Similar responses were reported for plant lectins from
Artocarpus integrifolia (SantosdeOliveira et al., 1994), Ery-
thrina velutina (Moraes et al., 1996) and Talisia esculenta (Freire
et al., 2003). Inflammatory responses induced in mice by lectin
from T. esculenta seeds (Freire et al., 2003), induced oedema
significant acute leukocyte migration 4 h after injection as
compared to saline group and was similar to fMLP group at dose
of 0.05 μg/cavity. The maximal migration was observed at 24 h
Fig. 3. Inhibitory effect of carbohydrates on CvL-induced neutrophil migration into mice peritoneal cavity. Neutrophil migration was evaluated 24 h after CvL (50 μg/
cavity) injection alone (black bar) or after incubation with 0.1 M of specific (D-galactose, sucrose and not specificcarbohydrate (D-fructose) (gray bars). The white bars
represent the neutrophil migration induced by the injection of the carbohydrate alone or saline solution. The data are the mean values±S.E.M. of six rats. The same
letters indicate that there were no significant statistical differences, compared with the results obtained in the group of animals which received CvL without incubation
with the carbohydrate (pb0.01, ANOVA–Bonferroni).
Fig. 4. AnalysisoftheparticipationofmacrophageontheneutrophilmigrationinducedbyCvL(50μg/cavity).(A)Peritonealmacrophagepopulationinnormal(saline)
or pre-treated animals with 3% thioglycolate solution (Tg) after injection with 100 μL saline. (B) Neutrophil migration induced by 100 μL saline (Sal), CvL (50 μg per
there were no significant statistical differences, compared to saline group (pb0.01, ANOVA–Bonferroni).
219A.F.S. Queiroz et al. / Comparative Biochemistry and Physiology, Part C 147 (2008) 216–221
post-injection and this migration was significantly diminished
when monosaccharide D-galactose was added together with CvL
in the peritoneal cavity, indicating that its carbohydrate binding
macrophages on the induction of CvL cells migration in mice
peritoneal cavities was evaluated. Thioglycolate treatment raised
the macrophage population 2.3 times causing elevation of
neutrophil migration induced by CvL in 77%, but it did not
modify the responsiveness to fMLP, a known direct chemoat-
lectin can modulate the neutrophil recruitment by indirect
mechanisms like other exogenous lectins from plant origin,
specially those purified from E. velutina (Moraes et al., 1996),
Glycine max (Benjamin et al., 1997), T. esculenta (Freire et al.,
2003), Vatairea macrocarpa (Alencar et al., 2003), Lonchocar-
pus sericeus (Alencar et al., 2005a), and Pisum arvense (Alencar
et al., 2005b) seeds.
The early stages of the inflammatory process, macrophages,
mast cells and lymphocytes participate in the control of neutrophil
migration. This control is mediated via release of chemotactic
factors such as leukotrienes (Rankin et al., 1990), components of
the complement system (Whaley and Ferguson, 1981), and
cytokines, mainly interleukin-1 (IL-1), IL-8, TNF-α (Staruch and
Wood, 1985; Rankin et al., 1990) and macrophages-derived
Since CvL-induced neutrophil migration seems to follow an
involved in this event were investigated, using selective NSAID
(Celecoxib), non-selective NSAID (diclofenac) and cytokine
antagonist (dexamethasone). Among these inhibitors, cytokine
antagonist (dexamethasone) reduced significantly the neutrophil
migration to the peritoneal cavity after stimulation by CvL. The
dexamethasone inhibitory effect could be explained by the
blockage of the release of chemotactic factors, stimulated by
etal.,1991).Itis thereforepostulatedthatthese findingsfavourthe
hypothesis that CvL-induced neutrophil migration could possibly
be mediated via release of cytokines by resident macrophages,
since these cells represent an important source of cytokines. The
results reported here demonstrated that the galactose/sacarose
specific lectin from C. varians sponge possesses a pro-inflamma-
tory activity, which induces neutrophil migration probably via the
release of cytokines from macrophages. These findings indicate
that lectins can be used, as tools to better understand the
mechanisms involved in inflammatory responses or cellular event
These findings showed that the isolation and characterization
of proteins from marine animals have turned into a fast growing
field in the life sciences. Many marine bioactive molecules are
attracting more and more attention due to their extensive
physiological, biological and pharmacological use. The impor-
tance of marine biotechnology has grown immensely because of
the achievements of these natural marine products.
This work was supported by Brazilian Agencies: FINEP,
CAPES and CNPq. The authors thank Dr Rosana Lucena de Sá
de Santana, pharmacists from Hemonorte, Natal, RN, Brazil, for
the generous blood bag donation.
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