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Localization of carbohydrate determinants common to Biomphalaria glabrata as well as to sporocysts and miracidia of Schistosoma mansoni

Published online by Cambridge University Press:  29 May 2008

T. LEHR ,
K. BEUERLEIN ,
M. J. DOENHOFF ,
C. G. GREVELDING  and
R. GEYER
T. LEHR
Affiliation:
Institute of Biochemistry, Faculty of Medicine, University of Giessen, Germany
K. BEUERLEIN
Affiliation:
Rudolf-Buchheim-Institute of Pharmacology, Faculty of Medicine, University of Giessen, Germany
M. J. DOENHOFF
Affiliation:
School of Biology, University of Nottingham, Nottingham, UK
C. G. GREVELDING
Affiliation:
Institute of Parasitology, Faculty of Veterinary Medicine, University of Giessen, Germany
R. GEYER*
Affiliation:
Institute of Biochemistry, Faculty of Medicine, University of Giessen, Germany
*
*Corresponding author: Institute of Biochemistry, Faculty of Medicine, University of Giessen, Friedrichstrasse 24, D-35392 Giessen, Germany. Tel: +49 641 99 47400. Fax: +49 641 99 47409. E-mail: [email protected]
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Summary

The presence of antigenic carbohydrate epitopes shared by Biomphalaria glabrata as well as by the sporocysts and miracidia representing snail-pathogenic larval stages of Schistosoma mansoni was assayed by immunohistochemical staining of paraformaldehyde-fixed tissues. To this end, both polyclonal rabbit antiserum raised against soluble egg antigens (SEA) of S. mansoni and monoclonal antibodies recognizing the carbohydrate epitopes LDN [GalNAc(β1-4)GlcNAc(β1-)], F-LDN [Fuc(α1-3)GalNAc(β1-4)GlcNAc(β1-)], LDN-F [GalNAc(β1-4)[Fuc(α1-3)]GlcNAc(β1-)], LDN-DF [GalNAc(β1-4)[Fuc(α1-2)Fuc(α1-3)]GlcNAc(β1-)] and Lewis X [Gal(β1-4)[Fuc(α1-3)]GlcNAc(β1-)] were used. Intriguingly, anti-SEA serum as well as anti-F-LDN antibodies displayed significant binding in the foot region, anterior tissue and the hepatopancreas of uninfected snails, whereas the Lewis X epitope was only weakly detectable in the latter tissue. In contrast, increased binding of antibodies recognizing LDN, LDN-F and LDN-DF was observed in infected snail tissue, in particular in regions involved in sporocystogenesis, in addition to an enhanced binding of anti-SEA serum and antibodies reacting with F-LDN. A pronounced expression of most of these carbohydrate antigens was also observed at the surface of miracidia. Hence, the detection of shared carbohydrate determinants in uninfected snail tissue, sporocysts and miracidia may support the hypothesis of carbohydrate-based molecular mimicry as a survival strategy of S. mansoni.

Keywords

Biomphalaria glabrataSchistosoma mansonimiracidiaimmunohistochemistrycarbohydrate epitopesmolecular mimicry
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 8 , July 2008 , pp. 931 - 942
Copyright
Copyright © 2008 Cambridge University Press

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References

Bankfalvi, A., Navabi, H., Bier, B., Bocker, W., Jasani, B. and Schmid, K. W. (1994). Wet autoclave pretreatment for antigen retrieval in diagnostic immunohistochemistry. Journal of Pathology 174, 223–228.Google Scholar
Bayne, C. J., Boswell, C. A., Loker, E. S. and Yui, M. A. (1985). Plasma components which mediate cellular defences in the gastropod mollusc Biomphalaria glabrata. Developmental and Comparative Immunology 9, 523–530.CrossRefGoogle ScholarPubMed
Bayne, C. J., Loker, E. S. and Yui, M. A. (1986). Interactions between the plasma proteins of Biomphalaria glabrata (Gastropoda) and the sporocyst tegument of Schistosoma mansoni (Trematoda). Parasitology 92, 653–664.CrossRefGoogle ScholarPubMed
Bickle, Q. D. and Andrews, B. J. (1988). Characterisation of Schistosoma mansoni monoclonal antibodies which block in-vitro killing: failure to demonstrate blockage of immunity in vivo. Parasite Immunology 10, 151–168.CrossRefGoogle ScholarPubMed
Borges, C. M. and Andrade, Z. A. (2003). Extra-cellular matrix changes in Schistosoma mansoni-infected Biomphalaria glabrata. Memorias do Instituto Oswaldo Cruz 98, 135–139.CrossRefGoogle ScholarPubMed
Chiang, C. P. and Caulfield, J. P. (1988). Schistosoma mansoni: ultrastructural demonstration of a miracidial glycocalyx that cross-reacts with antibodies raised against the cercarial glycocalyx. Experimental Parasitology 67, 63–72.CrossRefGoogle ScholarPubMed
Damian, R. T. (1989). Molecular mimicry: parasite evasion and host defense. Current Topics in Microbiology and Immunology 145, 101–115.Google ScholarPubMed
De Souza, C. P., Cunha Rde, C. and Andrade, Z. A. (1995). Development of Schistosoma mansoni in Biomphalaria tenagophila, Biomphalaria straminea and Biomphalaria glabrata. Revista do Instituto de Medicina Tropical de Sao Paulo 37, 201–206.Google Scholar
Dissous, C. and Capron, A. (1989). Schistosoma mansoni and its intermediate host Biomphalaria glabrata express a common 39 kilodalton acidic protein. Molecular and Biochemical Parasitology 32, 49–56.CrossRefGoogle ScholarPubMed
Dissous, C., Grzych, J. M. and Capron, A. (1986). Schistosoma mansoni shares a protective oligosaccharide epitope with freshwater and marine snails. Nature, London 323, 443–445.CrossRefGoogle ScholarPubMed
Dunne, D. W., Agnew, A. M., Mohda, J. and Doenhoff, M. J. (1986). Schistosoma mansoni egg antigens: preparation of rabbit antisera with monospecific immunoprecipitating activity, and their use in antigen characterization. Parasite Immunology 8, 575–586.CrossRefGoogle ScholarPubMed
El-Ansary, A. (2003). Biochemical and immunological adaptation in schistosome parasitism. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 136, 227–243.CrossRefGoogle ScholarPubMed
El-Ansary, A. and Al-Daihan, S. (2006). Important aspects of Biomphalaria snail-schistosome interactions as targets for antischistosome drug. Medical Science Monitor 12, RA 282–292.Google ScholarPubMed
Gordon, M. B., Howard, L. and Compton, D. A. (2001). Chromosome movement in mitosis requires microtubule anchorage at spindle poles. Journal of Cell Biology 152, 425–434.CrossRefGoogle ScholarPubMed
Grevelding, C. G., Sommer, G. and Kunz, W. (1997). Female-specific gene expression in Schistosoma mansoni is regulated by pairing. Parasitology 115, 635–640.CrossRefGoogle ScholarPubMed
Hokke, C. H. and Deelder, A. M. (2001). Schistosome glycoconjugates in host-parasite interplay. Glycoconjugate Journal 18, 573–587.Google Scholar
Hokke, C. H., Deelder, A. M., Hoffmann, K. F. and Wuhrer, M. (2007). Glycomics-driven discoveries in schistosome research. Experimental Parasitology 117, 275–283.CrossRefGoogle ScholarPubMed
Jeong, K. H., Lie, K. J. and Heyneman, D. (1983). The ultrastructure of the amebocyte-producing organ in Biomphalaria glabrata. Developmental and Comparative Immunology 7, 217–228.CrossRefGoogle ScholarPubMed
Kantelhardt, S. R., Wuhrer, M., Dennis, R. D., Doenhoff, M. J., Bickle, Q. and Geyer, R. (2002). Fuc(alpha1–>3)GalNAc-: the major antigenic motif of Schistosoma mansoni glycolipids implicated in infection sera and keyhole-limpet haemocyanin cross-reactivity. The Biochemical Journal 366, 217–223.CrossRefGoogle Scholar
Khoo, K. H., Chatterjee, D., Caulfield, J. P., Morris, H. R. and Dell, A. (1997). Structural mapping of the glycans from the egg glycoproteins of Schistosoma mansoni and Schistosoma japonicum: identification of novel core structures and terminal sequences. Glycobiology 7, 663–677.CrossRefGoogle ScholarPubMed
Köster, B. and Strand, M. (1994). Schistosoma mansoni: immunolocalization of two different fucose-containing carbohydrate epitopes. Parasitology 108, 433–446.CrossRefGoogle ScholarPubMed
Lehr, T., Geyer, H., Maass, K., Doenhoff, M. J. and Geyer, R. (2007). Structural characterization of N-glycans from the freshwater snail Biomphalaria glabrata cross-reacting with Schistosoma mansoni glycoconjugates. Glycobiology 17, 82–103.CrossRefGoogle ScholarPubMed
Lemos, Q. T. (1999). Contribution to the histology of Biomphalaria glabrata. Revista da Sociedade Brasileira de Medicina Tropical 32, 343–347.CrossRefGoogle Scholar
Lemos, Q. T. and Andrade, Z. A. (2001). Sequential histological changes in Biomphalaria glabrata during the course of Schistosoma mansoni infection. Memorias do Instituto Oswaldo Cruz 96, 719–721.CrossRefGoogle ScholarPubMed
Loker, E. S., Adema, C. M., Zhang, S. M. and Kepler, T. B. (2004). Invertebrate immune systems–not homogeneous, not simple, not well understood. Immunological Reviews 198, 10–24.CrossRefGoogle Scholar
Loker, E. S. and Bayne, C. J. (1986). Immunity to trematode larvae in the snail Biomphalaria. Symposia of the Zoological Society of London 56, 199–220.Google Scholar
Mascie-Taylor, C. G. and Karim, E. (2003). The burden of chronic disease. Science 302, 1921–1922.CrossRefGoogle ScholarPubMed
Nyame, A. K., Yoshino, T. P. and Cummings, R. D. (2002). Differential expression of LacdiNAc, fucosylated LacdiNAc, and Lewis X Glycan antigens in intramolluscan stages of Schistosoma mansoni. Journal of Parasitology 88, 890–897.CrossRefGoogle ScholarPubMed
Ogbadoyi, E., Ersfeld, K., Robinson, D., Sherwin, T. and Gull, K. (2000). Architecture of the Trypanosoma brucei nucleus during interphase and mitosis. Chromosoma 108, 501–513.CrossRefGoogle ScholarPubMed
Pan, S. C. (1980). The fine structure of the miracidium of Schistosoma mansoni. Journal of Invertebrate Pathology 36, 307–372.CrossRefGoogle ScholarPubMed
Pearce, E. J. (2005). Priming of the immune response by schistosome eggs. Parasite Immunology 27, 265–270.CrossRefGoogle ScholarPubMed
Pinheiro, J., Maldonado, A. and Lanfredi, R. M. (2004). Light and scanning electron microscopy of the miracidium of Echinostoma paraensei (Trematoda, Echinostomatidae). Veterinary Parasitology 121, 265–275.CrossRefGoogle ScholarPubMed
Robijn, M. L., Wuhrer, M., Kornelis, D., Deelder, A. M., Geyer, R. and Hokke, C. H. (2005). Mapping fucosylated epitopes on glycoproteins and glycolipids of Schistosoma mansoni cercariae, adult worms and eggs. Parasitology 130, 67–77.CrossRefGoogle ScholarPubMed
Romeis, B. (1989). Mikroskopische Technik, Urban and Schwarzenberg, München, Wien, Baltimore.Google Scholar
Sire, C., Rognon, A. and Theron, A. (1998). Failure of Schistosoma mansoni to reinfect Biomphalaria glabrata snails: acquired humoral resistance or intra-specific larval antagonism? Parasitology 117, 117–122.CrossRefGoogle ScholarPubMed
Spray, F. J. and Granath, W. O. Jr. (1990). Differential binding of hemolymph proteins from schistosome-resistant and -susceptible Biomphalaria glabrata to Schistosoma mansoni sporocysts. Journal of Parasitology 76, 225–229.CrossRefGoogle ScholarPubMed
Van Leeuwen, F. (1986). Pitfalls in immunocytochemistry with special reference to the specificity problems in the localization of neuropeptides. American Journal of Anatomy 175, 363–377.CrossRefGoogle Scholar
Van Remoortere, A., Hokke, C. H., Van Dam, G. J., Van Die, I., Deelder, A. M. and Van Den Eijnden, D. H. (2000). Various stages of Schistosoma express LewisX, LacdiNAc, GalNAcβ1-4 (Fucα1-3)GlcNAc and GalNAcβ1-4(Fucα1-2Fucα1-3)GlcNAc carbohydrate epitopes: detection with monoclonal antibodies that are characterized by enzymatically synthesized neoglycoproteins. Glycobiology 10, 601–609.CrossRefGoogle Scholar
Wuhrer, M., Dennis, R. D., Doenhoff, M. J., Bickle, Q., Lochnit, G. and Geyer, R. (1999). Immunochemical characterisation of Schistosoma mansoni glycolipid antigens. Molecular and Biochemical Parasitology 103, 155–169.CrossRefGoogle ScholarPubMed
Wuhrer, M., Dennis, R. D., Doenhoff, M. J. and Geyer, R. (2000 a). A fucose-containing epitope is shared by keyhole limpet haemocyanin and Schistosoma mansoni glycosphingolipids. Molecular and Biochemical Parasitology 110, 237–246.CrossRefGoogle ScholarPubMed
Wuhrer, M., Dennis, R. D., Doenhoff, M. J., Lochnit, G. and Geyer, R. (2000 b). Schistosoma mansoni cercarial glycolipids are dominated by Lewis X and pseudo-Lewis Y structures. Glycobiology 10, 89–101.CrossRefGoogle ScholarPubMed
Wuhrer, M. and Geyer, R. (2006). Glycoconjugate structures. In Parasitic Flatworms – Molecular Biology, Biochemistry, Immunology and Parasitology (ed. Maule, A. G. and Marks, N. J.), pp. 408–422. CAB International, Wallingford, UK.Google Scholar
Wuhrer, M., Kantelhardt, S. R., Dennis, R. D., Doenhoff, M. J., Lochnit, G. and Geyer, R. (2002). Characterization of glycosphingolipids from Schistosoma mansoni eggs carrying Fuc(α1-3)GalNAc-, GalNAc(β1-4)[Fuc(α1-3)]GlcNAc- and Gal(β1-4)[Fuc(α1-3)]GlcNAc- (Lewis X) terminal structures. European Journal of Biochemistry 269, 481–493.Google Scholar
Yoshino, T. P. and Boswell, C. A. (1986). Antigen sharing between larval trematodes and their snail hosts: how real a phenomenon in immune evasion. Symposia of the Zoological Society of London 56, 221–238.Google Scholar