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Cercarial surface saccharides of six trematode species from the pond snail, Lymnaea stagnalis
... Hypoderaeum conoideum is a generalist parasite and several species of the genus Lymnaea Lamarck, 1799 may act as first intermediate hosts in Europe (Mathias, 1924(Mathias, , 1925Dubois, 1929;Rees, 1932;Wesenberg-Lund, 1934;Wikgren, 1956;Meyer, 1964;Williams, 1966;Smirnova & Ibrasheva, 1967;Skovronsky, 1984;Grabda-Kazubska & Kiseliene, 1990;Adam & Lewis, 1993;Haas et al., 1995;Horak & Mikes, 1995;Niewiadomska et al., 1997;Toledo et al., 1998bToledo et al., , 1999a. Mathias (1925) quantitatively assessed the infectivity of H. conoideum miracidia in relation to five molluscan species (members of the Lymnaeidae and Planorbidae) and showed that both Lymnaea stagnalis (Linnaeus, 1758) and L. limosa (Linnaeus, 1758) are capable of hosting this parasite under laboratory conditions. ...
The morphology of the different larval stages and life cycle of Hypoderaeum conoideum (Trematoda: Echinostomatidae) are described. The freshwater snail species Lymnaea peregra (Gastropoda: Lymnaeidae) serves as the natural first intermediate host and this and L. corvus serve as experimental first intermediate hosts. These and other freshwater snails, such as Physella acuta and Gyraulus chinensis, in turn serve as second intermediate hosts. Adult worms were obtained from chicks and ducks, but not from rats, mice and golden hamsters. The morphology of the larval stages is compared with previous work on H. conoideum. Several aspects of the biology of the life history stages are described with emphasis on the transmission dynamics of the free-living stages. Differential suitability of the snail species that may act as first and/or second intermediate hosts is studied and discussed.
... These results are in accordance with data produced by lectin binding studies on living T. regenti cercariae [22] and with histological sections of both of the life stages [21,42]. Moreover, comparison with other schistosomes and non-schistosome trematodes had conclusively shown that extensive fucosylation of the cercarial glycocalyx is unique, and represents a general attribute of all the schistosome species studied so far [44,45,9,22]. In the cercarial glycocalyx of Schistosoma mansoni, Fuc represents more than 50% of the overall saccharide content; other saccharides include Gal/GalNAc, Glc/GlcNAc, Man and xylose [8,11,14]; sialic acid was not confirmed [9]. ...
The invasive larvae (cercariae) of schistosomes penetrate the skin of their definitive hosts. During the invasion, they undergo dramatic ultrastructural and physiological transitions. These changes result in the development of the subsequent stage, schistosomulum, which migrates through host tissues in close contact with host’s immune system. One of the striking changes in the transforming cercariae is the shedding of their thick tegumental glycocalyx, which represents an immunoattractive structure; therefore its removal helps cercariae to avoid immune attack. A set of commercial fluorescently labeled lectin probes, their saccharide inhibitors and monoclonal antibodies against the trisaccharide Lewis-X antigen (LeX, CD15) were used to characterize changes in the surface saccharide composition of the neuropathogenic avian schistosome Trichobilharzia regenti during the transformation of cercariae to schistosomula, both in vitro and in vivo. The effect of various lectins on glycocalyx shedding was evaluated microscopically. The involvement of peptidases and their inhibitors on the shedding of glycocalyx was investigated using T. regenti recombinant cathepsin B2 and a set of peptidase inhibitors. The surface glycocalyx of T. regenti cercariae was rich in fucose and mannose/glucose residues. After the transformation of cercariae in vitro or in vivo within their specific duck host, reduction and vanishing of these epitopes was observed, and galactose/N-acetylgalactosamine emerged. The presence of LeX was not observed on the cercariae, but the antigen was gradually expressed from the anterior part of the body in the developing schistosomula. Some lectins which bind to the cercarial surface also induced secretion from the acetabular penetration glands. Seven lectins induced the shedding of glycocalyx by cercariae, among which five bound strongly to cercarial surface; the effect could be blocked by saccharide inhibitors. Mannose-binding protein, part of the lectin pathway of the complement system, also bound to cercariae and schistosomula, but had little effect on glycocalyx shedding. Our study did not confirm the involvement of proteolysis in glycocalyx shedding.
... On the cercarial body surface we found the presence of non-reducing residues of mannose and/or glucose, Nacetylglucosamine, N-acetylgalactosamine and galactose, recognised respectively by ConA, WGA, SBA and PNA. Furthermore, the glycosylation of the body and tail surface is different, as found in other studied trematode species (Nanduri et al. 1991, Horák 1995, Horák & Mikeš 1995, Iakovleva & Gorbushin 2005, Podhorský et al. 2009). Cercariae of F. hepatica spend a short time in the intermediate host. ...
The presence and distribution of surface carbohydrates in the tissues of Galba truncatula snails uninfected or after infection with Fasciola hepatica as well as on the surface of the snail-pathogenic larval stages of the parasite were studied by lectin labelling assay. This is an attempt to find similarities that indicate possible mimicry, utilised by the parasite as an evasion strategy in this snail-trematode system. Different binding patterns were identified on head-foot-mantle, hepatopancreas, genital glands, renopericardial complex of the host as well as of the snail-pathogenic larval stages of F. hepatica. The infection with F. hepatica leads to changes of labelling with Glycine max in the head-mantle cells and Arachis hypogaea in the tubular epithelium of the hepatopancreas. The lectin binding on the other snail tissues is not changed by the development of the larvae. Our data clearly demonstrated the similarity in labelling of G. truncatula tissues and the surface of the snail-pathogenic larval stages of F. hepatica. The role of glycosylation of the contact surfaces of both organisms in relation to the host-parasite interactions is also discussed.
... On the cercarial body surface we found the presence of non-reducing residues of mannose and/or glucose, Nacetylglucosamine, N-acetylgalactosamine and galactose, recognised respectively by ConA, WGA, SBA and PNA. Furthermore, the glycosylation of the body and tail surface is different, as found in other studied trematode species (Nanduri et al. 1991, Horák 1995, Horák & Mikeš 1995, Iakovleva & Gorbushin 2005, Podhorský et al. 2009). Cercariae of F. hepatica spend a short time in the intermediate host. ...
Glycoconjugates are involved in the intracellular signalling and play a fundamental role in the functioning of the central nervous system of mollusca. The aim of this study was to investigate the presence and distribution of carbohydrate residues in the nerve ganglia of non-infected Galba truncatula snails and after infection with liver fluke Fasciola hepatica. Using lectin labelling on tissue sections it was found that the parasite infection produces changes in glycosylation patterns of the ganglia. These results will contribute to the clarification of the snail-parasite interactions and to identify targets for control of this important trematode infection in the future.
... The thick glycocalyx that served as a protective layer for the free-living cercaria is shed, as its carbohydrate-rich composition is a target of the host complement cascade. In the schistosome species studied so far, the glycocalyx is markedly rich in fucose residues (154,196197198). There is an obvious loss of saccharide moieties at the surfaces of transformed schistosomula of T. szidati and T. regenti, leading to reduced immunoreactivity and attractiveness for fucose-specific lectins (154, 155, 199, 200). ...
... The thick glycocalyx that served as a protective layer for the free-living cercaria is shed, as its carbohydrate-rich composition is a target of the host complement cascade. In the schistosome species studied so far, the glycocalyx is markedly rich in fucose residues (154,(196)(197)(198). There is an obvious loss of saccharide moieties at the surfaces of transformed schistosomula of T. szidati and T. regenti, leading to reduced immunoreactivity and attractiveness for fucose-specific lectins (154,155,199,200). ...
Cercarial dermatitis (swimmer's itch) is a condition caused by infective larvae (cercariae) of a species-rich group of mammalian and avian schistosomes. Over the last decade, it has been reported in areas that previously had few or no cases of dermatitis and is thus considered an emerging disease. It is obvious that avian schistosomes are responsible for the majority of reported dermatitis outbreaks around the world, and thus they are the primary focus of this review. Although they infect humans, they do not mature and usually die in the skin. Experimental infections of avian schistosomes in mice show that in previously exposed hosts, there is a strong skin immune reaction that kills the schistosome. However, penetration of larvae into naive mice can result in temporary migration from the skin. This is of particular interest because the worms are able to migrate to different organs, for example, the lungs in the case of visceral schistosomes and the central nervous system in the case of nasal schistosomes. The risk of such migration and accompanying disorders needs to be clarified for humans and animals of interest (e.g., dogs). Herein we compiled the most comprehensive review of the diversity, immunology, and epidemiology of avian schistosomes causing cercarial dermatitis.
Copyright © 2015, American Society for Microbiology. All Rights Reserved.
... Once in the snail, the larvae of Trichobilharzia must avoid snail defence reactions; if the parasite is unable to do this, or the snail is resistant to infection, then these larvae are destroyed by strong immune reac-tions (mainly by hemocytes forming a capsule around the parasite). Therefore, the larvae employ several strategies like molecular masking and mimicry (Roder, Bourns & Singhal, 1977;Van der Knaap et al., 1985;Horák, 1995;Horák & Mikeš, 1995;Horák & Van der Knaap, 1997) or suppress activities of hemocytes (De Jong-Brink, Bergamin-Sassen & Solis Soto, 2001;Horák & Kolářová, 2005). In addition, the physiology of parasitised snails is affected, e.g., the receptors for several snail hormones involved in regulation of reproduction are blocked by schistosomin, a peptide produced by snail hemocytes and connective tissue cells in response to infection (De Jong-Brink et al., 2001;Horák & Kolářová, 2005). ...
1. Birds and snails are suitable hosts for many parasites, including helminths in general and trematodes in particular. Among trematodes, members of the family Schistosomatidae with two-host life cycles (snails as intermediate hosts and birds as definitive hosts) are successful and abundant pathogens. Their transmission between birds and snails in nature can be influenced by many abiotic and biotic factors.
2. In snails, the prevalence of schistosome infections and production of cercariae can be influenced by host immunological susceptibility/physiological suitability, snail age/size, interspecific competition of trematode larvae, etc. Schistosomes are able to survive in overwintering snails, serving as a source of infection in spring.
3. Birds may also differ in susceptibility to and prevalence rates of schistosome infections. They are long-range vectors of schistosomes.
4. Climate changes influence behaviour of migratory birds, lead to shifts in season- or temperature-dependent processes in snails and schistosomes, and influence the frequency of schistosome transmission and intensity of infection. Also, eutrophication can increase the growth of snail populations and transmission of bird schistosomes.
5. Dispersal of bird schistosomes to new regions and an increased availability (local abundance) of the snail hosts, together with the use of new water reservoirs (e.g., in higher latitudes) for recreational purposes, may contribute to a higher number of outbreaks of cercarial dermatitis.
... Surface glycosylation of T. regenti and T. szidati cercariae was previously described (Horák and Mikeš 1995, Horák et al. 1997, Frýzková 2004, Blažová and Horák 2005 showing differences in binding of particular lectins (see Table III for comparison). In our study, the reactions of most lectins with particular species were identical (11 lectins: LTA, JAC, PSA, HPA, DBA, GSL, GSL-II, SJA, PHA-E, PHA-L, BS-II). ...
Cercariae of bird schistosomes are traditionally considered to be very similar in their morphological characteristics. In
order to solve the problem, we tested some methods which might be suitable for cercarial differentiation. Fourteen isolates
of three Trichobilharzia species (T. szidati, T. franki, T. regenti) occurring sympatrically in Central Europe were used. Dimensions of individual cercariae do not represent a useful criterion
for identification, because the intraspecific variability exceeds the interspecific one. On the other hand, chaetotaxy appears
a promising way for discrimination, although some sensory papillae do not stain sufficiently with silver nitrate. The papillary
pattern (i.e. number and relative position of papillae) is specific for all Trichobilharzia species studied by us. Therefore, we compiled an identification key for the three Trichobilharzia species. In addition, we tried to find species-specific surface saccharide epitopes; none of the labeled lectin probes can
be used as a speciesspecific marker.
... Hypoderaeum conoideum is a generalist parasite and several species of the genus Lymnaea Lamarck, 1799 may act as first intermediate hosts in Europe (Mathias, 1924(Mathias, , 1925Dubois, 1929;Rees, 1932;Wesenberg-Lund, 1934;Wikgren, 1956;Meyer, 1964;Williams, 1966;Smirnova & Ibrasheva, 1967;Skovronsky, 1984;Grabda-Kazubska & Kiseliene, 1990;Adam & Lewis, 1993;Haas et al., 1995;Horak & Mikes, 1995;Niewiadomska et al., 1997;Toledo et al., 1998bToledo et al., , 1999a. Mathias (1925) quantitatively assessed the infectivity of H. conoideum miracidia in relation to five molluscan species (members of the Lymnaeidae and Planorbidae) and showed that both Lymnaea stagnalis (Linnaeus, 1758) and L. limosa (Linnaeus, 1758) are capable of hosting this parasite under laboratory conditions. ...
The morphology of the different larval stages and life cycle of Hypoderaeum conoideum (Trematoda: Echinostomatidae) are described. The freshwater snail species Lymnaea peregra (Gastropoda: Lymnaeidae) serves as the natural first intermediate host and this and L. corvus serve as experimental first intermediate hosts. These and other freshwater snails, such as Physella acuta and Gyraulus chinensis, in turn serve as second intermediate hosts. Adult worms were obtained from chicks and ducks, but not from rats, mice and golden hamsters. The morphology of the larval stages is compared with previous work on H. conoideum. Several aspects of the biology of the life history stages are described with emphasis on the transmission dynamics of the free-living stages. Differential suitability of the snail species that may act as first and/or second intermediate hosts is studied and discussed.
Cercariae of Trichobilharzia szidati were examined for the presence of endogenous lections. The haemagglutination caused by the cercarial homogenate was inhibited by glycoconjugates (heparin, hyaluronic acid, lipopolysaccharide, bovine submaxillar mucin, thyroglobulin) and saccharides [lactulose, laminarin, D-galacturonic acid]. Ligand blotting with laminarin-conjugate revealed the existence of one laminarin-binding protein in the sample. This protein migrates mostly as a double-band under nonreducing conditions (48-52 kDa), and as a single-band under reducing conditions (54-56 kDa). Identical bands were recognized by specific mouse antibodies raised against agglutinins bound on mouse erythrocytes. Labeled laminarin and/or heparin reacted with postacetabular glands on histological sections. Similarly, the binding of Lotus tetragonolobus lectin as a glycoprotein ligand supported the finding that the cercarial lectin is localized in postacetabular glands. Moreover, there is an indication that a lectin is present on the cercarial surface. In agreement with affinity fluorescence, mouse antibodies to the cercarial haemagglutinins recognized the postacetabular penetration glands and the surface of cercariae.
Background: Cercariae (larva of helminth parasites) are covered by a thick glycocalyx coat, which serves as an osmotic protection during their free existence, and contain carbohydrates conjugated as glycoproteins, glycolipids and muco-polysaccharides. Although, limited studies have been made on life cycle of cercariae from fresh water snails, however, car-bohydrate studies on cercariae have not been done in Iran so far. This study was made to determine the cercariae specifica-tions from Lymnaea gedrosiana and evaluation of surface carbohydrates as receptors for host lectins in a host-parasite rela-tionship system as a model in human schistosomiasis including cercarial dermatitis in Khuzestan Province. Methods: For this purpose, snails were collected from Dezful region in Khuzestan Province and cercariae were obtained by shedding method and identified by valuable keys. Experimental infection was established in the Culex pipiens (Culicidae mosquitoes) larvae for further identification and mode of adhesion. To detect the mode of adhesion, surface carbohydrates of cercariae were detected by lentil (Lens culinaris) lectins. Results: Examined snails were infected with xiphidiocerceria of trematodes and metacercariae were obtained from Culex pipiens. Also, Mannose monosaccharides-CH2OH (CHOH) 4CHO -were detected particularly on the glands of cercariae. Conclusion: Adhesion of cercariae to their host by lectins-carbohydrates bonds is the first stage of host-parasite relation-ship. This phenomenon could be happened for animal schistosome's cercaria in cercarial dermatitis.
The lectin concanavalin A (Con A) was used as a model probe to study the behavior of molecules bound to the surface of recently transformed schistosomula of Schistosoma mansoni. Con A binding was saturable (150-180 pg/organism) and specifically competed by alpha-methyl mannoside. Both FITC-Con A and 125-I-Con A were lost from the surface of schistosomula with a halftime of 8-10 h in culture in defined medium. A comparable decrease in the binding of Con A to schistosomula cultured and then labeled with the lectin indicated that the labeling procedure itself was not inducing the observed change. Internalization of Con A was not seen by either fluorescence microscopy or electron microscope radioautography. In addition, 70-80% of the radioactivity lost from the parasite was recoverable by TCA precipitation from the culture medium as intact Con A (27,000 mol wt on SDS PAGE). Thus, the mechanism of clearance of bound Con A from the surface of cultured schistosomula is apparently by sloughing of Con A molecules intact into the culture media and not by endocytosis and degradation. Con A binding sites, visualized with hemocyanin by scanning electron microscopy, appeared homogeneously distributed over the surface of schistosomula when organisms were labeled at 4 degree C or after fixation with glutaraldehyde. However, Con A and hemocyanin formed aggregates on the surface of schistosomula when labeling was performed at 37 degrees C, which suggests that lectin binding sites have lateral mobility within the plane of the membrane. These aggregates are likely independent of metabolism by the parasite because aggregation also occurs on the surface of organisms killed with azide.
The lectin concanavalin A (Con A) was used as a model probe to study the behavior of molecules bound to the surface of recently transformed schistosomula of Schistosoma mansoni. Con A binding was saturable (150-180 pg/organism) and specifically competed by alpha-methyl mannoside. Both FITC-Con A and 125-I-Con A were lost from the surface of schistosomula with a halftime of 8-10 h in culture in defined medium. A comparable decrease in the binding of Con A to schistosomula cultured and then labeled with the lectin indicated that the labeling procedure itself was not inducing the observed change. Internalization of Con A was not seen by either fluorescence microscopy or electron microscope radioautography. In addition, 70-80% of the radioactivity lost from the parasite was recoverable by TCA precipitation from the culture medium as intact Con A (27,000 mol wt on SDS PAGE). Thus, the mechanism of clearance of bound Con A from the surface of cultured schistosomula is apparently by sloughing of Con A molecules intact into the culture media and not by endocytosis and degradation. Con A binding sites, visualized with hemocyanin by scanning electron microscopy, appeared homogeneously distributed over the surface of schistosomula when organisms were labeled at 4 degree C or after fixation with glutaraldehyde. However, Con A and hemocyanin formed aggregates on the surface of schistosomula when labeling was performed at 37 degrees C, which suggests that lectin binding sites have lateral mobility within the plane of the membrane. These aggregates are likely independent of metabolism by the parasite because aggregation also occurs on the surface of organisms killed with azide.
Mother and daughter sporocysts of Tricholbilharzia ocellata, developing in the snail host Lymnaea stagnalis, were searched for substances with antigenic similarities to the snail's haemolymph. Antisera to cell-free snail haemolymph and fractions thereof were used in three different immunocytochemical staining methods, applied on sections of parasitized snails. Snail tissue was consistently stained; cercariae were stained, indicating that the applied methods were successful. Most sections through mother and daughter sporocysts were completely unstained. It is concluded that neither mother nor daughter sporocysts are masked by the antigens studied or substances mimicking these. The relevance of the present observations is discussed.
We have used two monoclonal antibodies, 128C3/3 and 504B1, to immunolocalize their carbohydrate epitopes in different developmental stages of Schistosoma mansoni. Both epitopes contain fucose: mAb 128C3/3, as we have shown previously, recognizes fucose in a novel, possibly internal linkage (Levery et al. 1992) while mAb 504B1, as we show here, bound to the Le(x) epitope, which contains fucose alpha 1-->3 linked to N-acetyl-glucosamine. The tissue expression of these epitopes was strikingly different and both elicit an immune response in infected hosts. The mAb 128C3/3-defined epitope was exposed on the surface of all larval stages but not on adult worms; however, it was found in the excretory system of adult worms of both sexes. In contrast, surface expression of the Le(x) epitope was initiated after the transformation of cercariae to schistosomula and was maintained throughout the adult life in both sexes.
Many parasites develop in invertebrate hosts that possess internal defense systems (IDS) that vigorously defined self-integrity. Invertebrates apparently do not produce a large diversity of finely tuned immunorecognition molecules but rather rely on recognition of patterns. As a consequence, requirements for immune evasion are likely to be fundamentally different in such hosts. Although parasites of invertebrates certainly employ diverse tactics to evade host IDS, this review focuses on parasite-mediated interference with the structural and functional integrity of host hemocytes and argues that this is a common strategy of immune evasion. Parasites mediating such effects on host hemocytes are termed suppressors. In some cases, interference is mediated by mutualistic symbionts carried by the suppressors. Hemocytes from infected hosts exhibit diminished adherence to substrates, impaired spreading ability, and reduced ability to participate in phagocytosis or encapsulation reactions. As a result of the action of suppressors, the host's vulnerability to opportunistic parasites is increased, a phenomenon termed acquired susceptibility. A strategy of interference is therefore risky, particularly for suppressors with relatively long development times. As a result, suppressors may provoke either a partial generalized interference or a selective interference with host IDS function, actively contribute to protection of the host to discourage growth of opportunists (termed parasite-mediated internal defense), or induce compensatory host responses that protect the host but that do not jeopardize their own development. Some parasites consistently colonize previously infected hosts and seem to be specialized opportunists.
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