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Changes in the surface antigen profile of Schistosoma mansoniduring maturation from cercaria to adult worm

Published online by Cambridge University Press:  06 April 2009

Gilberto Payares
Affiliation:
Divisions of Parasitology and Mill Hill, London NW7 1AA
Diane J. McLaren
Affiliation:
Divisions of Parasitology and Mill Hill, London NW7 1AA
W. H. Evans
Affiliation:
Biochemistry National Institute for Medical Research, Mill Hill, London NW7 1AA
S. R. Smithers
Affiliation:
Divisions of Parasitology and Mill Hill, London NW7 1AA

Extract

Antigenic proteins on the surfaces of different developmental stages of Schistosoma mansoni were radio-iodinated by the lodogen-catalysed method and identified by immunoprecipitation with a panel of antisera. The sera comprised specific immune serum from mice harbouring a chronic schistosome infection or vaccinated with γ-irradiated cercariae; serum from rabbits immunized with adult schistosome tegumental outer membranes or a partially purified Mr32K glycoprotein from adult worm membranes; and a monoclonal antibody recognizing an Mr20 K antigen on the surface of schistosomula. The Mr38–32 K glycoproteins were the major antigens identified in surface-labelled cercariae and their probable association with the glycocalyx is discussed. Schistosomula transformed from cercariae either mechanically or by penetration of host skin in vitro, expressed a similar pattern of surface antigens to that identified for cercariae, but low molecular weight antigens of Mr20, 17 and 15 K were also detected. The Mr38–32 K glycoproteins, although present on newly transformed schistoso mula, were progressively replaced with time, by a single dominant glycoprotein (Mr 32 K) expressing identical epitopes to those on the Mr 38–32 K complex. Moreover, the data confirm that the Mr 32 K glycoprotein persists on the tegument after in vivo maturation and is conserved, together with Mr 20 and 15 K antigens, through to the adult stage. New antigens (Mr 97 and 25 K) were also detected during in vivo maturation and were present in late-stage schistosomes recovered from infected hosts. In addition, the enzyme alkaline phosphatase is expressed on the surfaces of 3-week-old liver worms as a dominant antigen (Mr 65 K); this feature may be related to nutritional and/or physiological processes in the tegument of this metabolically active stage of development.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1985

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References

REFERENCES

Brink, L. H., Krueger, K. & Harris, C. (1980). Stage specific antigens of Schistosoma mansoni. In The Host Invader Interplay. Proceedings of the 3rd International Symposium on Biochemistry of Parasites and Host Parasite Relationships, (ed. van den Bossche, H.), pp. 393404. Elsevier/North-holland.Google Scholar
Brink, L. H., Mclaren, D. J. & Smithers, S. R. (1977). Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 74, 7386.CrossRefGoogle ScholarPubMed
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–47.Google Scholar
Cleog, J. A. & Smithers, S. R. (1972). The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 7998.CrossRefGoogle Scholar
Coles, G. C. (1973). The metabolism of schistosomes: a review. International Journal for Biochemistry 4, 319–37.CrossRefGoogle Scholar
Dissous, C., Dissous, C. & Capron, A. (1981). Isolation and characterization of surface antigens from Schistosoma mansoni schistosomula. Molecular and Biochemical Parasitology 3, 215–25.Google Scholar
Eacoli, N. & Payares, O. (1974). Schistosomamansoni: Early antimonial treatment of infected mice. Experimental Parasitology 35, 171–8.Google Scholar
Fraker, P. J. & Speck, J. C. Jr. (1978). Protein and cell membrane iodination with sparingly soluble chloramide 1, 3, 4, 6-tetrachloro-3, 6-diphenylgiucorulyl. Biochemical Biophysical Research Communications 80, 849–57.CrossRefGoogle Scholar
Haseeb, M. A., Eveland, L. K. & Fried, B. (1984). Histochemical lipid studies on Schistosoma mansoni adults maintained in situ and in vitro. International Journal for Parasitology 14, 83–8.Google Scholar
Hayunga, E. G., Murrell, K. D., Taylor, D. W. & Vannier, W. E. (1979). Isolation and charac terisation of surface antigens from Schistosoma mansoni. I. Evaluation of techniques for radio isotope labelling of surface proteins from adult worms. Journal of Parasitology 65, 488–96.CrossRefGoogle Scholar
Hockley, D. J. & Mclaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 1325.CrossRefGoogle ScholarPubMed
Incani, R. N. & McLaren, D. J. (1983). Ultrastructural observations on the in vitro interaction of rat neutrophils with schistosomula of Schistosoma mansoni in the presence of antibody and/or complement. Parasitology 86, 345–57.CrossRefGoogle ScholarPubMed
Kent, N. H. (1963). Comparative immunochemistry of larval and adult forms of Schistosoma mansoni. Annals of the New York Academy of Sciences 113, 100–13.Google Scholar
Knight, M., Simpson, A. J. G., Payares, G., Chaudri, M. & Smithers, S. R. (1984). Cell-free synthesis of Schistosoma mansoni surface antigens: stage specificity of their expression. EMBO Journal 3, 213–1 9.CrossRefGoogle ScholarPubMed
Kusel, J. R. (1972). Protein composition and protein synthesis in the surface membranes of Schistosoma mansoni. Parasitology 65 55–9.CrossRefGoogle ScholarPubMed
Lazdins, J. K., Stein, M. J., David, J. R., & Sher, A. (1982). Schistosoma mansoni: rapid isolation and purification of schistosomula of different redevelopmental stages by centrifugation on discon tinuous density gradients of Percoll. Experimental Parasitology 53, 3944.Google Scholar
McLaren, D. J. (1980). Schistosoma mansoni: The parasite surface in relation to host immunity. In Tropical Medicine Research Studies, vol. 1, (ed. Brown, K. N.), Chichester: Research Studies Press. John Wiley.Google Scholar
McLaren, D. J. & Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature, London 269, 147–9.Google Scholar
McLaren, D. J. & Terry, R. J. (1982). The protective role of acquired host antigens during schistosome maturation. Parasite Immunology 4, 129–48.Google Scholar
Payares, G., Smithers, S. R. & Evans, W. H. (1984). Tegumental alkaline phosphatase from adult Schistosoma mansoni: Purification and topographical location. Molecular and Biochemical Parasitology 13, 343–60.CrossRefGoogle ScholarPubMed
Payares, G., Mclaren, D. J., Evans, W. H. & Smithers, S. R. (1985). Antigenicity and immunogenicity of the tegumental outer membrane of adult Schistosoma mansoni. Parasite Immunology (in the Press).Google Scholar
Philipp, M. & Rumjanek, F. D. (1984). Antigenic and dynamic properties of helminth surface structures. Molecular and Biochemical Parasitology 10, 245–68.Google Scholar
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E., Mota-Santos, T. A., Figueiredo, E. A. & Pellegrino, J. (1974). Schistosonia mansoni defined system for stepwise transformation of cercariae to schistosomula in vitro. Experimental Parasitology 36, 360–72.Google Scholar
Roberts, S. M., Aitken, R., Vojvodic, M., Wells, E. & Wilson, R. A. (1983). Identification of exposed components on the surface of adult Schistosoma mansoni by lactoperoxidase-catalysed iodination. Molecular and Biochemical Parasitology 9, 129–43.CrossRefGoogle ScholarPubMed
Rumjanek, F. D., Mclaren, D. J. & Smituers, S. R. (1983). Serum-induced expression of a surface protein in schistosomula of Schistosoma mansoni: a possible receptor for lipid uptake. Molecular and Biochemical Parasilology 9, 337–50.CrossRefGoogle ScholarPubMed
Samuelson, J. C., Caulfield, J. P. & David, J. R. (1980). Schistosoma mansoni: post-transformational changes in schistosomula grown in vitro and in mice. Experimental Parasitology 50, 369–83.CrossRefGoogle ScholarPubMed
Shah, J. & Ramasamy, R. (1982). Surface antigens on cercariae, schistosomula and adult worms of Schistosoma mansoni. International Journal for Parasitology 12, 451–61.Google Scholar
Simpson, A. J. G., James, S. L. & Sher, A. (1983). Identification of surface antigens of schistosomula of Schistosoma mansoni recognised by antibodies from mice immunized by chronic infection and by exposure to highly irradiated cercariae. Infection and Immunity 41, 591–7.CrossRefGoogle ScholarPubMed
Simpson, A. J. G., Payares, G., Walker, T., Knight, M. & Smithers, S. R. (1984). The modulation of expression of polypeptide surface antigens on developing schistosomula of Schistosoma mansoniü. Journal of Immunology 133, 2725–30.Google Scholar
Simpson, A. J. G., Schryer, M. D., Cesari, I. M., Evans, W. H. & Smithers, S. R. (1981). Isolation and partial characterization of the tegumental outer membrane of adult Schistosoma mansoni. Parasitology 83, 163–77.Google Scholar
Smith, T. M. & Brooks, T. J. (1969). Lipid fractions in adult Schistosoma mansoni. Parasitology 59, 293–8.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Gammage, K. (1980). Recovery of Schistosoma mansoni from the skin, lungs and hepatic portal system of naive mice and mice previously exposed to S. mansoni: evidence for two phases of parasite attrition in immune mice. Parasitology 80, 289300.Google Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695700.Google Scholar
Strrewalt, M. A., Cousin, C. E. & Dorsey, C. H. (1983). Schistosoma mamsoni: stimulus and transformation of cercariae into schistosomules. Experimental Parasitology 56, 358–68.Google Scholar
Tavares, C. A. P., de Rossi, R., Payares, G., Simpson, A. J. G., McLaren, D. J. & Smithers, S. R. (1984). A monoclonal antibody raised against adult Schistososna mansoni which recognizes a surface antigen on schistosomula. Zeitschrift für Parasitenkunde 70, 189–97.Google Scholar
Towbin, H., Stahelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacry lamide gets to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–4.Google Scholar