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Antigenic variation in parasites

Published online by Cambridge University Press:  23 August 2011

M.J. Turner
Affiliation:
MRC Biochemical Parasitology Unit, The Molteno Institute, University of Cambridge, Downing Street, Cambridge CB2 3EE

Extract

Antigenic variation is a powerful survival strategy adapted by certain species of parasitic protozoa to allow them to survive in the immunized host. It is exemplified by the African trypanosomes, which provide far and away the best characterized and most studied system of this kind. Why have the trypanosomes developed antigenic variation to such a sophisticated level? Because the trypanosome lives its life in the bloodstream of its mammalian host and is therefore in continuous conflict with the host's immune system. Antigenic variation represents its whole survival strategy, with some help provided by its ability to immunosuppress the host. The importance of antigenic variation to the trypanosome is underscored by the estimate that up to 10% of the trypanosome genome may be devoted to variant antigen genes (Van der Ploeg et al. 1982). Most other parasitic protozoa prefer a less confrontational existence and usually adopt an intracellular home for at least a part of their life-cycle within the mammalian host. That being the case, do other parasitic protozoa need antigenic variation within their armorarium ? The answer seems to be yes, although the reasons why are by no means clear. For example, the stages in the life-cycle which exhibit antigenic variation might be expected to be those which are released free into the bloodstream – in malaria, sporozoites and merozoites, for example. Yet there seems to be no evidence for phenotypic variation at all in these stages. Rather, it is the intracellular stages which, in both Plasmodium and Babesia, seem to elaborate molecules which are expressed at the surface of the parasitized cell, and which are capable of both eliciting an immune response and of avoiding the con- sequences of such a response by phenotypic antigenic variation. Why are such antigens expressed, and what is their functional significance?

Type
Research Article
Copyright
Copyright © Cambridge University Press 1984

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References

REFERENCES

Barbour, A. G., Tessier, S. L. & Stoenner, H. G. (1982). Variable major proteins of Borrelia hermsii. Journal of Experimental Medicine 156, 1312–24.CrossRefGoogle Scholar
Barnwell, J. W., Howard, R. J. & Miller, L. H. (1982). Influence of the spleen on the expression of surface antigens on parasitised erythrocytes. In Malaria and the Red Cell Surface, Ciba Foundation Symposium 94, pp. 117–36. London: Pitman.Google Scholar
Barry, J. D., Crowe, J. S. & Vickerman, K. (1983). Instability of the Trypanosoma brucei rhodesiense metacyclic variable antigen repertoire. Nature, London 306, 699701.CrossRefGoogle ScholarPubMed
Barry, J. D. & Emery, P. L. (1984). Parasite development and host responses during the establishment of Trypanosoma brucei infection transmitted by tsetse fly. Parasitology 88, 6784.CrossRefGoogle ScholarPubMed
Borst, P. & Cross, G. A. M. (1982). Molecular basis for trypanosome antigenic variation. Cell 29, 291303.CrossRefGoogle ScholarPubMed
Brown, K. N. & Brown, I. N. (1965). Immunity to malaria: antigenic variation in chronic infections of P. knowlesi. Nature, London 208, 1286–8.CrossRefGoogle Scholar
Brown, I. N., Brown, K. N. & Hills, L. A. (1968). Immunity to malaria: the antibody response to antigenic variation by Plasmodium knowlesi. Immunology 14, 127–38.Google ScholarPubMed
Brown, K. N. (1973). Antibody induced variation in malaria parasites. Nature, London 242, 4950.CrossRefGoogle ScholarPubMed
Callow, L. L. & Mellors, L. T. (1966). A new vaccine for B. argentina infection, prepared in splenectomized calves. Australian Veterinary Journal 42, 464–5.CrossRefGoogle Scholar
Capbern, A., Giroud, C., Baltz, T. & Mattern, P. (1977). Trypanosoma equiperdum: étude des variations antigeniques en cours de la trypanosomose experimental du lapin. Experimental Parasitology 42, 613.CrossRefGoogle Scholar
Cardoso De Almeida, M. L. & Turner, M. J. (1983). The membrane form of variant surface glycoproteins of Trypanosoma brucei. Nature, London 302, 349–52.CrossRefGoogle ScholarPubMed
Cross, G. A. M. (1975). Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitology 71, 393417.CrossRefGoogle ScholarPubMed
Crowe, J. S., Barry, J. D., Luckins, A. G., Ross, C. A. & Vickerman, K. (1983). All metacyclic variable antigen types of Trypanosoma congolense identified using monoclonal antibodies. Nature, London 306, 389–91.CrossRefGoogle ScholarPubMed
Curnow, J. A. (1973). Studies on antigenic changes and strain differences in Babesia argentina infections. Australian Veterinary Journal 49, 279–83.CrossRefGoogle ScholarPubMed
Doyle, J. J., Hirumi, H., Hirumi, K., Lupton, E. N. & Cross, G. A. M. (1980). Antigenic variation in clones of animal infective Trypanosoma brucei derived and cloned in vitro. Parasitology 80, 359–70.CrossRefGoogle ScholarPubMed
Epstein, N., Miller, L. H., Kaushel, D. C., Udeinya, I. J., Rener, J., Howard, R. J., Asofsky, R., Aikawa, M. & Hess, R. L. (1981). Monoclonal antibodies against a specific surface determinant on malarial (Plasmodium knowlesi) merozoites block erythrocyte invasion. Journal of Immunology 127, 212–17.CrossRefGoogle ScholarPubMed
Ferguson, M. A. J. & Cross, G. A. M. (1984). Myristylation of the membrane form of a Trypanosoma brucei variant surface glycoprotein. Journal of Biological Chemistry (in the Press).CrossRefGoogle Scholar
Gray, A. R. (1965). Antigenic variation in clones of Trypanosoma brucei. I. Immunological relationships of the clones. Annals of Tropical Medicine and Parasitology 59, 2736.CrossRefGoogle ScholarPubMed
Hajduk, S. L. & Vickerman, K. (1981). Antigenic variation in cyclically transmitted Trypanosoma brucei. Variable antigen type composition of metacyclic trypanosome populations from the salivary glands of Glossina morsitans. Parasitology 83, 595607.CrossRefGoogle Scholar
Holder, A. A. (1983). Carbohydrate is linked through ethanolamine to the C-terminal amino acid of Trypanosoma brucei variant surface glycoprotein. The Biochemical Journal 209, 261–2.CrossRefGoogle Scholar
Holder, A. A. & Cross, G. A. M. (1981). Glycopeptides from variant surface glycoproteins of Trypanosoma brucei. C-terminal location of antigenically cross-reacting carbohydrate moieties. Molecular and Biochemical Parasitology 2, 135–50.CrossRefGoogle ScholarPubMed
Holder, A. A. & Freeman, R. R. (1984). Blood stage Plasmodium falciparum and Plasmodium yoelii antigen characterisation. In Proceedings of the Third John Jacob Abel Symposium on Drug Development: Molecular Parasitology (ed. August, T.) (in the Press).Google Scholar
Hommel, M., David, P. H. & Olioino, L. D. (1983). Surface alterations of erythrocytes in Plasmodium falciparum malaria. Antigenic variation, antigenic diversity and the role of the spleen. Journal of Experimental Medicine 157, 1137–48.CrossRefGoogle ScholarPubMed
Howard, R. J., Barnwell, J. W. & Kao, V. (1983). Antigenic variation in Plasmodium knowlesi malaria: identification of the variant antigen on infected erythrocytes. Proceedings of the National Academy of Sciences, USA 80, 4129–33.CrossRefGoogle ScholarPubMed
Johnson, J. G. & Cross, G. A. M. (1979). Selective cleavage of variant surface glycoproteins from Trypanosoma brucei. The Biochemical Journal 178, 689–97.CrossRefGoogle ScholarPubMed
Kosinski, R. J. (1980). Antigenic variation in trypanosomes: a computer analysis of variant order. Parasitology 80, 343–57.CrossRefGoogle ScholarPubMed
Nantulya, V. M., Doyle, J. J. & Jenni, L. (1980). Studies on Trypanosoma (Nannomonas) congolense. II. Antigenic variation in three cyclically transmitted stocks. Parasitology 80, 123–31.CrossRefGoogle Scholar
Newbold, C. I., Boyle, D. B., Smith, C. C. & Brown, K. N. (1982). Monoclonal antibodies that protect in vivo against P. chabaudii recognise a 250000 daltons polypeptide. Infection and Immunology 38, 94102.Google Scholar
Nussenzweig, R. S. (1982). Progress in malaria vaccine development: characterization of protective antigens. Scandinavian Journal of Infectious Diseases, Suppl. 36, 40–5.Google ScholarPubMed
Olafson, R. W., Clarke, M. W., Kielland, S. C., Barbet, A. F. & McGuire, T. C. (1984). Amino terminal sequence homology among variable surface glycoproteins of African trypanosomes. Molecular and Biochemical Parasitology (in the Press).CrossRefGoogle Scholar
Ozaki, L. S., Svee, P., Nussenzweig, R. S., Nussenzweig, V. & Godson, G. N. (1983). Structure of the Plasmodium knowlesi gene coding for the circumsporozoite protein. Cell 34, 815–22.CrossRefGoogle ScholarPubMed
Phillips, R. S. (1971). Antigenic variation in Babesia rohdaini demonstrated by immunisation with irradiated parasites. Parasitology 63, 315–22.CrossRefGoogle ScholarPubMed
Rice-Ficht, A. C., Chen, K. K. & Donelson, J. E. (1981). Sequence homologies near the C-terminal of the variable surface glycoproteins of Trypanosoma brucei. Nature, London 294, 53–7.CrossRefGoogle Scholar
Roberts, J. A. & Tracey-Patte, P. (1975). Babesia rohdaini immunoinduction of antigenic variation. International Journal for Parasitology 5, 573–6.CrossRefGoogle ScholarPubMed
Seed, J. R. (1964). Antigenic similarity among culture forms of the brucei group of trypanosomes. Parasitology 54, 593–6.CrossRefGoogle ScholarPubMed
Seed, J. R. (1984). The ecology of antigenic variation. Journal of Protozoology (in the Press).CrossRefGoogle Scholar
Stoenner, H. G., Dodd, T. & Larsen, C. (1982). Antigenic variation of Borrelia hermsii. Journal of Experimental Medicine 156, 1297–311.CrossRefGoogle ScholarPubMed
Turner, M. J. (1982). Biochemistry of the variant surface glycoproteins of salivarian trypanosomes. Advances in Parasitology 21, 69153.CrossRefGoogle ScholarPubMed
Udeinya, I. J., Miller, L. H., McGregor, I. A. & Jensen, J. B. (1983). Plasmodium falciparum strain-specific antibody blocks binding of infected erythrocytes to amelanotic myeloma cells. Nature, London 303, 429–31.CrossRefGoogle Scholar
Van Der Ploeg, L. H. T., Valerio, D., De Lange, T., Bernards, A., Borst, P. & Grosveld, P. G. (1982). An analysis of cosmid clones of nuclear DNA from Trypanosoma brucei shows that the genes for VSGs are clustered in the genome. Nucleic Acids Research 10, 5905–23.CrossRefGoogle ScholarPubMed
Vickerman, K. (1969). On the surface coat and flagellar adhesion in trypanosomes. Journal of Cell Science 5, 163–93.CrossRefGoogle ScholarPubMed
Vickerman, K. & Barry, J. D. (1982). African trypanosomes. In Immunology of Parasitic Infections (ed. Cohen, S. and Warren, K.), pp. 204260. Oxford: Blackwell Scientific Publications.Google Scholar