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The in vitro transformation of the miracidium to the mother sporocyst of Schistosoma margrebowiei; changes in the parasite surface and implications for interactions with snail plasma factors

Published online by Cambridge University Press:  06 April 2009

B. E. Daniel
Affiliation:
Biology Department, Medawar Building, University College London, Gower Street, LondonWC1E 6BT
T. M. Preston
Affiliation:
Biology Department, Medawar Building, University College London, Gower Street, LondonWC1E 6BT
V. R. Southgate
Affiliation:
The Natural History Museum, Cromwell Road, LondonSW7 5BD

Summary

The in vitro transformation of the miracidium to the mother sporocyst of Schistosoma margrebowiei was initiated by placing the miracidium in mammalian physiological saline. The transformation occurs in stages: the cilia cease beating; the ciliated plates become detached from the intercellular ridges and underlying muscle layers; the intercellular ridges spread over the body surface eventually forming a new tegument; the sporocyst changes from an ovoid to a tubular shape in about 48 h at room temperature. The surfaces of the miracidium, sporocyst and cercaria of S. margrebowiei display stage-specific carbohydrates on their surfaces as indicated by lectin staining. Ricin120 stains the cilia alone of the miracidium whereas peanut agglutinin stains the larval surface except for the cilia. The intercellular ridges of the miracidium stain with concanavalin A and wheat germ agglutinin, and these lectins stain the entire surface of the mature mother sporocyst. The cercaria is the only larval stage which stains positively with asparagus pea lectin. Bulinus nasutus is incompatible with Schistosoma margrebowiei; the haemolymph of this snail contains an agglutinin which agglutinates a wide variety of mammalian erythrocytes including those of human ABO blood groups. The haemagglutinin titre of B. nasutus plasma is reduced after incubation with miracidia of S. margrebowiei indicating that the agglutinin is absorbed onto the surface of this larval stage but not that of the mother sporocyst or cercaria. The possible roles of agglutinins in host–parasite interactions together with the significance of the differences in the surface carbohydrates of the larval stages are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Bayne, C. J. (1983). Molluscan immunobiology. In The Mollusca, Vol. 5, Physiology Part 2 (ed. Saleuddin, A. S. M. & Wilbur, K. M.), pp. 429–60. New York: Academic Press.Google Scholar
Bayne, C. J., Buckley, P. M. & Dewan, P. C. (1980). Schistosoma mansoni: Cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistant Biomphalaria glabrata. Experimental Parasitology 50, 409–16.CrossRefGoogle ScholarPubMed
Bayne, C. J., Loker, E. S. & Yui, M. A. (1986). Interactions between the plasma proteins of Biomphalaria glabrata (Gastropoda) and the sporocyst tegument of Schistosoma mansoni (Trematoda). Parasitology 92, 653–64.CrossRefGoogle ScholarPubMed
Chernin, E. (1963). Observations on hearts explanted in vitro from the snail Australorbis glabratus. Journal of Parasitology 19, 353–64.CrossRefGoogle Scholar
Daniel, B. E. (1990). Host–parasite interactions: snails of the genus Bulinus and Schistosoma margrebowiei. Ph.D. thesis, University of London.Google Scholar
Dunn, T. S. & Yoshino, T. P. (1988). Schistosoma mansoni: Origin and expression of a tegumental surface antigen on the miracidium and primary sporocyst. Experimental Parasitology 67, 167–75.CrossRefGoogle ScholarPubMed
Foster, L. A. & Bogitsh, B. J. (1986). Utilisation of the heme moiety of hemoglobin by Schistosoma mansoni schistosomules in vitro. Journal of Parasitology 72, 669–76.CrossRefGoogle ScholarPubMed
Granath, W. O. & Yoshino, T. P. (1984). Schistosoma mansoni: passive transfer of resistance by serum in the vector snail, Biomphalaria glabrata. Experimental Parasitology 58, 188–93.CrossRefGoogle ScholarPubMed
Kechemir, N. & Combes, C. (1982). Développement du trématode Schistosoma haematobium après transplantation microchirurgicale chez le gastropode Planorbarius metidjensis. Comptes Rendus de l'académie des Sciences, Paris, 295, série III. 505–8.Google Scholar
Kinoti, G. K. (1971). Observations on the infection of bulinid snails with Schistosoma mattheei. Parasitology 62, 161–70.CrossRefGoogle ScholarPubMed
Linder, E. (1985). Schistosoma mansoni: visualization with fluorescent lectins of secretions and surface carbohydrates of living cercariae. Experimental Parasitology 59, 307–12.CrossRefGoogle ScholarPubMed
Loker, E. S. & Bayne, C. J. (1982). In vitro encounters between Schistosoma mansoni primary sporocysts and hemolymph components of susceptible and resistant strains of Biomphalaria glabrata. American Journal of Tropical Medicine and Hygiene 31, 9991005.CrossRefGoogle ScholarPubMed
Meuleman, E. A., Huyer, A. R. & Mooij, J. H. (1984). Maintenance of the life-cycle of Trichobilharzia ocellata via the duck Anas platyrhynchos and the pond snail Lymnaea stagnalis. Netherlands Journal of Zoology 34, 414–17.CrossRefGoogle Scholar
Meuleman, E. A., Lyaruu, D. M., Khan, M. A., Holzmann, P. J. & Sminia, T. (1978). Ultrastructural changes in the body wall of Schistosoma mansoni: during the transformation of the miracidium into the mother sporocyst in the snail host Biomphalaria pfeifferi. Zeitschrift für Parasitenkunde 56, 227–42.CrossRefGoogle ScholarPubMed
Ogbe, M. G. (1985). Aspects of the life cycle of Schistosoma margrebowiei infection in laboratory mammals. International Journal for Parasitology 15, 141–5.CrossRefGoogle ScholarPubMed
Rollinson, D. & Southgate, V. R. (1987). The genus Schistosoma: a taxonomic appraisal. In The Biology of Schistosomes: From Genes to Latrines (ed. Rollinson, D. & Simpson, A. J. G.), pp. 150. London: Academic Press.Google Scholar
Samuelson, J. C. & Caulfield, J. P. (1985). Role of pleated septate junctions in the epithelium of miracidia of Schistosoma mansoni during transformation to sporocysts in vitro. Tissue and Cell 17, 667–82.CrossRefGoogle ScholarPubMed
Samuelson, J. C., Quinn, J. J. & Caulfield, J. P. (1984). Hatching, chemokinesis and transformation of miracidia of Schistosoma mansoni. Journal of Parasitology 70, 321–31.CrossRefGoogle ScholarPubMed
Sminia, T. (1981). Gastropods. In Invertebrate Blood Cells, Vol. 1 (ed. Ratcliffe, N. A. & Rowley, A. F.), pp. 191232. New York: Academic Press.Google Scholar
Southgate, V. R. & Knowles, R. J. (1977). On Schistosoma margrebowiei Le Roux, 1933: The morphology of the egg, miracidium and cercaria, the compatibility with species of Bulinus and development in Mesocricetus auratus. Zeitschrift für Parasitenkunde 54, 233–50.CrossRefGoogle Scholar
Spray, F. J. & Granath, W. G. JR. (1990). Differential binding of hemolymph proteins from schistosome-resistant and -susceptible Biomphalaria glabrata to Schistosoma mansoni sporocysts. Journal of Parasitology 76, 225–9.CrossRefGoogle ScholarPubMed
Van Der KNAPP, W. P. W. & Loker, E. S. (1990). Immune mechanisms in trematode-snail interactions. Parasitology Today 6, 175–82.CrossRefGoogle Scholar
Watson, J. M. & Azim, M. A. (1949). Comparative efficiency of various methods of infecting mice with Schistosoma mansoni. Annals of Tropical Medicine and Hygiene 19, 292303.Google Scholar
Yoshino, T. P., Cheng, T. C. & Renwrantz, L. R. (1977). Lectin and human blood group determinants of Schistosoma mansoni: alteration following in vitro transformation of miracidium to mother sporocyst. Journal of Parasitology 63, 818–24.CrossRefGoogle ScholarPubMed
Zelck, U. & Becker, W. (1990). Lectin binding to cells of Schistosoma mansoni sporocysts and surrounding Biomphalaria glabrata tissue. Journal of Invertebrate Pathology 55, 93–9.CrossRefGoogle ScholarPubMed