Skip to main content
SpringerLink
Log in

Carbohydrate Mimicry of the Parasite in the Himasthla elongata (Trematoda: Echinostomatidae)—Littorina littorea (Mollusca: Prosobranchia) System

  • Comparative and Ontogenic Biochemistry and Immunology
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

Using labeled lectins, a comparative study of the surface of tegument of Himasthla elongata at different stages of development cycle (daughter rediae, cercariae, and metacercariae) and glycocalyx of plasma membranes of hemocytes of molluscs Littorina littorea and Mytilus edulis that are the first and second intermediate hosts of this trematode species, respectively, has been carried out. It is found that in the course of the development cycle of the parasite there occurs a change of the set of terminal sacharides of the glycocalyx of the H. elongata tegument surface as well as differences are revealed in the pattern of binding of three out of five tested lectins with hemocytes of blue mussel and periwinkle. At the same time, the presence of similar carbohydrate determinants on the surface of hemocytes of L. littorea and daughter rediae of H. elongata is shown. The established similarity in composition of glycocalyx of hemocytes of the mollusc and the trematode parthenitae is, most likely, a result of coevolution of the parasite and the host and is of the adaptive nature. Use of the mechanism of the carbohydrate mimicry by parthenitae of this species allows them to avoid attacking by effector cells of the internal defense system of the mollusc-host.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Adema, C.M. and Loker, E.S., Specificity and Immunobiology of Larval Digenean-Snail Associations, Advances in Trematode Biology, Fried, B. and Graczyk, T.K.,. Eds., New York: CRC, 1997, pp. 230–263.

    Google Scholar 

  2. Fryer, S.E. and Bayne, C.J., Host-Parasite Interactions in Molluscs, Prog. Mol. Subcell. Biol., 1996, vol. 15, pp. 131–153.

    CAS  PubMed  Google Scholar 

  3. van Dam, G.J., Claas, F., Yazdanbakhsh, M., Kruize, Y.C.M., van Keulen, A.C.I., Falcao Ferreira, S.T.M., Rotmans, J.P., and Decider, A.M., Schistosoma mansoni Excretory Circulating Cathodic Antigen Shares Lewis-X Epitopes with a Human Granulocyte Surface Antigen and Evokes Host Antibodies Mediating Complement-Dependent Lysis of Granulocytes, Blood, 1996, vol. 88, pp. 4246–4251.

    PubMed  Google Scholar 

  4. Wuhrer, M., Berkefeld, C., Dennis, R.D., Idris, M.A., and Geyer, R., The Liver Flukes Fasciola gigantica and Fasciola hepatica Express the Leucocyte Cluster of Differentiation Marker CD77 (Globotriaosylceramide) in Their Tegument, Biol. Chem., 2001, vol. 382, pp. 195–207.

    Article  CAS  PubMed  Google Scholar 

  5. Weston, D.S. and Kemp, W.M., Schistosoma mansoni— Comparision of Cloned Tropomyosin Antigens Shared between Adult Parasite and Biomphalaria glabrata, Exp. Parasitol., 1993, vol. 76, pp. 358–370.

    Article  CAS  PubMed  Google Scholar 

  6. Bayne, C.J. and Stephens, J.A., Schistosoma mansoni and Biomphalaria glabrata Share Epitopes: Antibodies to Sporocysts Bind Host Snail Hemocytes, J. Invertebr. Pathol., 1983, vol. 42, pp. 221–223.

    Article  CAS  PubMed  Google Scholar 

  7. Yoshino, T.P. and Bayne, C.J., Mimicry of Snail Host Antigens by Miracidia and Primary Sporocysts of Schistosoma mansoni, Parasite Immunol., 1983, vol. 5, pp. 317–328.

    CAS  PubMed  Google Scholar 

  8. Granath, W.O., Jr. and Aspevig, J.E., Comparison of Hemocyte Components from Schistosoma mansoni (Trematoda)— Susceptible and Resistant Biomphalaria glabrata (Gastropoda) That Cross-React with Larval Schistosome Surface Proteins, Comp. Biochem. Physiol. B., 1993, vol. 104, pp. 675–680.

    Article  PubMed  Google Scholar 

  9. Bayne, C.J., Boswell, C.A., and Yui, M.A., Widespread Antigenic Cross-Reactivity between Plasma Proteins of a Gastropod, and Its Trematode Parasite, Dev. Comp. Immunol., 1987, vol. 11, pp. 321–329.

    Article  CAS  PubMed  Google Scholar 

  10. Horak, P. and van der Knaap, W.P.W., Lectins in Snail—Trematode Interactions: a Review, Fol. Parasitol., 1997, vol. 44, pp. 161–172.

    CAS  Google Scholar 

  11. Gorbushin, A.M. and Shaposhnikowa, T.G., In vitro Culture of the Avian Echinostome Himasthla elongata: from Redia to Marita, Exp. Parasitol., 2002, vol. 101, pp. 234–239.

    Article  CAS  PubMed  Google Scholar 

  12. Deme, R., Horak, P., and Zelck, U., Hemocyte Surface Saccharides of Lymnaea stagnalis, the Intermediate Host of Trichobilharzia szidati, Helminthol., 1995, vol. 33, pp. 83.

    Google Scholar 

  13. Dikkeboom, R., Tijnagel, J.M.G.H., and van der Knaap, W.P.W., Monoclonal Antibody Recognized Hemocyte Subpopulations in Juvenile and Adult Lymnaea stagnalis: Functional Characteristics and Lectin Binding, Dev. Comp. Immunol., 1989, vol. 12, pp. 17–32.

    Article  Google Scholar 

  14. Wolmarans, C.T. and Yssel, E., Use of SEM and Lectins to Study Bulinus africanus Leukocyte Groups and Their in vitro Behavior over a Time Period, J. Invertebr. Pathol., 1990, vol. 56, pp. 1–7.

    Article  Google Scholar 

  15. Yoshino, T.P., Lectins and Antibodies as Molecular Probes of Molluscan Hemocyte Surface Membranes, Dev. Comp. Immunol., 1983, vol. 7, pp. 641–644.

    Article  CAS  Google Scholar 

  16. Zelck, U. and Becker, W., Biomphalaria glabrata: Influence of Calcium, Lectins, and Plasma Factors on in vitro Phagocytic Behavior of Hemocytes of Noninfected or Schistosoma mansoni-Infected Snails, Exp. Parasit., 1992, vol. 75, pp. 126–136.

    Article  CAS  PubMed  Google Scholar 

  17. Brewer, C.F., Marcus, D.M., Grollman, A.P., and Sternlicht, H., Interactions of Saccharides with Concanavalin A. Relation between Calcium Ions and the Binding of Saccharides to Concanavalin A, J. Biol. Chem., 1974, vol. 249, pp. 4614–4616.

    CAS  PubMed  Google Scholar 

  18. Pipe, R.K., Differential Binding of Lectins to Haemocytes of the Mussel Mytilus edulis, Cell Tissue Res., 1990, vol. 261, pp. 261–268.

    Article  CAS  Google Scholar 

  19. Yoshino, T.P., Cheng, T.C., and Renwrantz, L.R., Lectin and Human Blood Group Determinants of Schistosoma mansoni: Alteration Following in vitro Transformation of Miracidium to Mother Sporocyst, J. Parasitol., 1977, vol. 63, pp. 818–824.

    CAS  PubMed  Google Scholar 

  20. Simpson, A.J. and Smithers, S.R., Characterization of the Exposed Carbohydrates on the Surface Membrane of Adult Schistosoma mansoni by Analysis of Lectin Binding, Parasitol., 1980, vol. 81, pp. 1–15.

    CAS  Google Scholar 

  21. Under, E. and Huldt, G., Distribution of Exposed and Hidden Carbohydrates of Schistosoma mansoni Adult Worms Demonstrated by Selective Binding of Fluorochrome-Conjugated Lectins, Parasitol., 1982, vol. 85, pp. 503–509.

    Google Scholar 

  22. Simpson, A.J., Correa-Oliveira, R., Smithers, S.R., and Sher, A., The Exposed Carbohydrates of Schistosomula of Schistosoma mansoni and Their Modification during Maturation in vivo, Mol. Biochem. Parasitol., 1983, vol. 8, pp. 191–205.

    Article  CAS  PubMed  Google Scholar 

  23. Uchikawa, R. and Loker, E.S., Lectin-Binding Properties of the Surface of in vitro Transformed Schistosoma mansoni and Echinostoma paraensei Sporocysts, J. Parasitol., 1991, vol. 77, pp. 742–748.

    CAS  PubMed  Google Scholar 

  24. Daniel, B.E., Preston, T.M., and Southgate, V.R., The in vitro Transformation of the Miracidium to the Mother Sporocyst of Schistosoma margebowiei: Changes in the Parasite Surface and Implications for Interactions with Snail Plasma Factors, Parasitol., 1992, vol. 104, pp. 41–49.

    Google Scholar 

  25. Gerhardus, M.J.T., Baggen, J.M.C., van der Knaap, W.P.W., and Sminia, T., Analysis of Surface Carbohydrates of Trichobilharzia ocellata Miracidia and Sporocyst using Lectin Binding Techniques, Parasitol., 1991, vol. 103, pp. 51–59.

    CAS  Google Scholar 

  26. Horak, P., Developmentally Regulated Expression of Surface Carbohydrate Residues on Larval Stages of the Avian Schistosome Trichobilharzia szidati, Fol. Parasitol., 1995, vol. 42, pp. 255–265.

    CAS  Google Scholar 

  27. Schmidt, J., Glycans with N-Acetyllactosamine Type 2-Like Residues Covering Adult Schistosoma mansoni, and Glycomimesis as a Putative Mechanism of Immune Evasion, Parasitology, 1995, vol. 111, pp. 325–336.

    CAS  PubMed  Google Scholar 

  28. Zelk, U. and Becker, W., Lectin Binding to Cells of Schistosoma mansoni and Surrounding Biomphalaria glabrata Tissue, J. Invertebr. Pathol., 1990, vol. 55, pp. 93–99.

    Article  PubMed  Google Scholar 

  29. Karre, K., Express Yourself or Die: Peptides, MHC Molecules and NIC-Cells, Science, 1995, vol. 267, p. 978.

    CAS  PubMed  Google Scholar 

  30. Nanduri, J., Dennis, J.E., Rosenberry, T.L., Mahmoud, A.A., and Tartakoff, A.M., Glycocalyx of Bodies versus Tails of Schistosoma mansoni Cercariae. Lectin-Binding, Size, Charge, and Electron Microscopic Characterization, J. Biol. Chem., 1991, vol. 266, pp. 1341–1347.

    CAS  PubMed  Google Scholar 

  31. Roder, J.C., Bourns, T.K., and Singhal, S.K., Trichobilharzia ocellata: Cercariae Masked by Antigens of the Snail, Lymnaea stagnalis, Exp. Parasitol., 1977, vol. 41, pp. 206–212.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. St. Petersburg State University, St. Petersburg, Russia

    N. V. Iakovleva & A. M. Gorbushin

Authors
  1. N. V. Iakovleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. M. Gorbushin
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

__________

Translated from Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, Vol. 41, No. 2, 2005, pp. 114–118.

Original Russian Text Copyright © 2005 by Iakovleva, Gorbushin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iakovleva, N.V., Gorbushin, A.M. Carbohydrate Mimicry of the Parasite in the Himasthla elongata (Trematoda: Echinostomatidae)—Littorina littorea (Mollusca: Prosobranchia) System. J Evol Biochem Phys 41, 143–149 (2005). https://doi.org/10.1007/s10893-005-0047-x

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10893-005-0047-x

Keywords

Search

Navigation