Hostname: page-component-77c89778f8-m8s7h Total loading time: 0 Render date: 2024-07-24T10:05:00.275Z Has data issue: false hasContentIssue false

Disguise as an evasive stratagem of parasitic organisms

Published online by Cambridge University Press:  23 August 2011

Diane J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA

Extract

It is now well established that animal parasites elicit vigorous immune responses in their hosts and that the resistance to reinfection thus acquired is mediated through conventional humoral and/or cellular effector mechanisms. It is also recognized, however, that some parasites exhibit extreme longevity in the face of a potentially hostile or lethal environment, and it may be assumed therefore that such organisms possess a repertoire of highly sophisticated and successful evasive strategies. Of all the survival mechanisms thus far proposed, the concept of antigen sharing, or disguise, is probably the most contentious. Arguments have arisen over the nature and origin of the shared determinants and over the validity of their role in ensuring parasite survival within the fully immunocompetent host. This presentation reviews published data concerning the existence of a disguise stratagem amongst medically important parasites and evaluates experiments designed to investigate the functional importance of disguise in immune evasion.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1984

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bout, D., Capron, A., Dupas, H. & Capron, M. (1974). Characterisation of Schistosoma mansoni antigens. Proceedings of the Third International Congress of Parasitology, Munich 2, 1146–8.Google Scholar
Boyer, M. H., Kalfayan, L. J. & Ketchum, D. G. (1977). The host antigen phenomenon in experimental murine schistosomiasis. III. Destruction of parasites transferred from mice to hamsters. American Journal of Tropical Medicine and Hygiene 26, 254–7.CrossRefGoogle ScholarPubMed
Boyer, M. H., Ketchum, D. G. & Palmer, P. D. (1976). The host antigen phenomenon in experimental murine schistosomiasis: the transfer of 3-week-old Schistosoma mansoni between two inbred strains of mice. International Journal for Parasitology 6, 235–8.CrossRefGoogle Scholar
Brown, A. P., Burakoff, S. J. & Sher, A. (1980). Specificity of alloreactive T lymphocytes that adhere to lung stage schistosomula of Schistosoma mansoni. Journal of Immunology 124, 2516–18.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Vadas, M. A., Martz, E. & Sher, A. (1979). Cytolytic T lymphocytes recognise alloantigens on schistosomula of Schistosoma mansoni but fail to induce damage. Journal of Immunology 122, 1314–21.CrossRefGoogle ScholarPubMed
Cameron, G. L. & Stavely, J. M. (1957). Blood group P substance in hydatid cyst fluids. Nature, London 179, 147.CrossRefGoogle ScholarPubMed
Capron, A., Biguet, J., Vernes, A. & Afchain, D. (1968). Structure antigenique des helminthes. Aspects immunologiques des relations hôte—parasite. Pathologie-Biologie 16, 121–38.Google Scholar
Chernin, J. (1982). The nature of antigens common to both the metacestodes of Taenia crassiceps and its laboratory host. Journal of Helminthology 56, 339–44.CrossRefGoogle ScholarPubMed
Cioli, D. & Neis, R. (1972). Antigeni dell'ospite in Schistosoma mansoni. Parassitologia 14, 73–9.Google Scholar
Clegg, J. A. (1972). The schistosome surface in relation to parasitism. In Functional Aspects of Parasite Surfaces. Symposia of the British Society for Parasitology vol. 10 (ed. Taylor, A. E. R. and Muller, R.), pp. 2340. Oxford: Blackwell Scientific Publications.Google Scholar
Clegg, J. A. (1974). Host antigens and the immune response in schistosomiasis. In Parasites in the Immunized Host: Mechanisms of Survival. Ciba Foundation Symposium 25, 161176. Amsterdam: Elsevier.Google Scholar
Clegg, J. A., Smithers, S. R. & Terry, R. J. (1971). Acquisition of human antigens by Schistosoma mansoni during cultivation in vitro. Nature, London 232, 653–4.CrossRefGoogle ScholarPubMed
Coelho, P. M. Z., Gazzinelli, G. & Pellegrino, J. (1980). Schistosoma mansoni: host antigen occurrence on worms recovered from laboratory vertebrate animals. Parasitology 81, 349–54.CrossRefGoogle ScholarPubMed
Court, J. P. & Storey, D. M. (1981). Shared antigens between Litomosoides carinii and its hosts Sigmodon hispidus and Mastomys natalensis. Tropenmedezin und Parasitologie 32, 161–4.Google ScholarPubMed
Dahl, J. S., Dahl, C. E. & Levine, R. P. (1979). The role of fatty acid composition and membrane fluidity in the resistance of Acholeplasma laidlawii to complement-mediated killing. Journal of Immunology 123, 104–8.CrossRefGoogle ScholarPubMed
Damian, R. T. (1964). Molecular mimicry: antigen sharing by parasite and host and its consequences. American Naturalist 98, 129–49.CrossRefGoogle Scholar
Damian, R. T. (1967). Common antigens between Schistosoma mansoni and the laboratory mouse. Journal of Parasitology 53, 60–4.CrossRefGoogle ScholarPubMed
Damian, R. T. (1979). Molecular mimicry in biological adaptation. In Host Parasite Interfaces at Population, Individual and Molecular Levels (ed. Nickol, B. B.), pp. 103–26. London: Academic Press.Google Scholar
Damian, R. T., Greene, N. D. & Hubbard, W. J. (1973). Occurrence of mouse α2-macroglobulin antigenic determinants on Schistosoma mansoni adults, with evidence on their nature. Journal of Parasitology 59, 6473.CrossRefGoogle Scholar
Dean, D. A. (1977). Decreased binding of cytotoxic antibody by developing Schistosoma mansoni. Evidence for a surface change independent of host antigen adsorption and membrane turnover. Journal of Parasitology 63, 418–26.CrossRefGoogle ScholarPubMed
Diffley, P. (1978). Comparative immunological analysis of host plasma proteins bound to blood stream forms of Trypanosoma brucei subspecies. Infection and Immunity 21, 605–12.CrossRefGoogle Scholar
Diffley, P. & Honigberg, B. M. (1977). Fluorescent antibody analysis of host plasma components on bloodstream forms of African pathogenic trypanosomes. I. Host specificity and time of accretion in Trypanosoma congolense. Journal of Parasitology 63, 599606.CrossRefGoogle ScholarPubMed
Diffley, P. & Honigberg, B. M. (1978). Immunologic analysis of host plasma proteins on bloodstream forms of African pathogenic trypanosomes. II. Identification and quantitation of surface-bound albumin, nonspecific IgG and complement on Trypanosoma congolense. Journal of Parasitology 64, 674–81.CrossRefGoogle ScholarPubMed
Emerson, S. G. & Cone, R. E. (1981). I-Kk and H-2k antigens are shed as supramolecular particles in association with membrane lipids. Journal of Immunology 127, 482–6.CrossRefGoogle Scholar
Erickson, D. G., Beattie, R. J., Yamaguchi, S., Miyasaka, E. & Williams, J. E. (1973). Host parasite relationship in schistosomiasis mansoni and japonica in rhesus monkeys: interhost worm transfers. Japanese Journal of Parasitology 22, 307–14.Google Scholar
Gitter, B. D., Mccormick, S. L. & Damian, R. T. (1982). Murine alloantigen acquisition by Schistosoma mansoni: presence of H-2K determinants on adult worms and failure of allogeneic lymphocytes to recognise acquired MHC gene products on schistosomula. Journal of Parasitology 68, 513–18.CrossRefGoogle ScholarPubMed
Goldring, O. L., Clegg, J. A., Smithers, S. R. & Terry, R. J. (1976). Acquisition of human blood group antigens by Schistosoma mansoni. Clinical and Experimental Immunology 26. 181–7.Google ScholarPubMed
Goldring, O. L., Kusel, J. R. & Smithers, S. R. (1977). Schistosoma mansoni: origin in vitro of host-like surface antigens. Experimental Parasitology 43, 8293.CrossRefGoogle ScholarPubMed
Goldring, O. L., Sher, A., Smithers, S. R. & Mclaren, D. J. (1977). Host antigens and parasite antigens of murine Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 144–8.CrossRefGoogle ScholarPubMed
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
Hogarth-Scott, R. S. (1968). Naturally occurring antibodies to the cuticle of nematodes. Parasitology 58, 221–6.CrossRefGoogle Scholar
Hughes, D. L. & Harness, E. (1973a). Attempts to demonstrate a ‘host antigen’ effect by the experimental transfer of adult Fasciola hepatica into recipient animals, immunised against the donor. Research in Veterinary Science 14, 151–4.CrossRefGoogle ScholarPubMed
Hughes, D. L. & Harness, E. (1973b). The experimental transfer of immature Fasciola hepatica from donor mice and hamsters to rats immunised against the donors. Research in Veterinary Science 14, 220–2.CrossRefGoogle ScholarPubMed
Hustead, S. T. & Williams, J. F. (1977). Permeability studies on taeniid metacestodes. I. Uptake of proteins by larval stages of Taenia taeniaeformis, T. crassiceps and Echinococcus granulosus. Journal of Parasitology 63, 314–21.CrossRefGoogle ScholarPubMed
Kemp, W. M., Brown, P. R., Merritt, S. C. & Miller, R. E. (1980). Tegument-associated antigen modulation by adult male Schistosoma mansoni. Journal of Immunology 124, 806–11.CrossRefGoogle ScholarPubMed
Kemp, W. M., Damian, R. T. & Greene, N. D. (1976). Immunocytochemical localisation of IgG on adult Schistosoma mansoni tegumental surfaces. Journal of Parasitology 62, 830–2.CrossRefGoogle ScholarPubMed
Kemp, W. M., Damian, R. T., Greene, N. D. & Lushbaugh, W. B. (1976). Immunocytochemical localisation of mouse α2-macroglobulinlike antigenic determinants on Schistosoma mansoni adults. Journal of Parasitology 62, 413–19.CrossRefGoogle ScholarPubMed
Kemp, W. M., Merritt, S. C., Bogucki, M. S., Rosier, J. G. & Seed, J. R. (1977). Evidence for adsorption of heterospecific host immunoglobulin on the tegument of Schistosoma mansoni. Journal of Parasitology 119, 1849–54.Google ScholarPubMed
Kemp, W. M., Merritt, S. C. & Rosier, J. G. (1979). Schistosoma mansoni: identification of immunoglobulins associated with the tegument of adult parasites from mice. Experimental Parasitology 45, 81–7.CrossRefGoogle Scholar
Le Ray, D. (1975). Structures antigéniques de Trypanosoma brucei (Protozoa, Kinetoplastida). Analyse immuno-électrophorétique et étude comparative. Annales de la Société Belge de Médecine Tropicale 55, 129311.Google Scholar
Lewert, R. M., Yogore, M. G., Para, J. M. & Ozeel, M. A. (1977). Rejection of mouse-derived Schistosoma japonicum and serum lethality of hosts immunised with mouse globulin or mouse erythrocytes. Journal of Parasitology 63, 825–30.CrossRefGoogle ScholarPubMed
Maizels, R. M., Philipp, M. & Dasgupta, A. (1982). Host serum albumin on the surface of microfilariae. Molecular and Biochemical Parasitology, Suppl., pp. 93–4.Google Scholar
Marcus, D. M. & Cass, L.E. (1969). Glycosphingolipids with Lewis blood group activity; uptake by human erythrocytes. Science 164, 553–5.CrossRefGoogle ScholarPubMed
Mcgreevy, P. B., Ismail, M. M., Phillips, T. M. & Denham, D. A. (1975). Studies with Brugia pahangi. 10. An attempt to demonstrate the sharing of antigenic determinants between the worm and its hosts. Journal of Helminthology 49, 107–13.CrossRefGoogle ScholarPubMed
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.), pp. 1220. Chichester: Research Studies Press/John Wiley.Google Scholar
Mclaren, D. J., Clegg, J. A. & Smithers, S. R. (1975). Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology 70, 6775.CrossRefGoogle ScholarPubMed
Mclaren, D. J. & Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature, London 269, 147–9.CrossRefGoogle ScholarPubMed
Mclaren, D. J., Hockley, D. J., Goldring, O. L. & Hammond, B. J. (1978). A freeze fracture study of the developing tegumental outer membrane of Schistosoma mansoni. Parasitology 76, 327–48.CrossRefGoogle ScholarPubMed
Mclaren, D. J. & Terry, R. J. (1982). The protective role of acquired host antigens during schistosome maturation. Parasite Immunology 4, 129–48.CrossRefGoogle ScholarPubMed
Michaeli, D., Senyk, G., Maoz, A. & Fuchs, S. (1972). Ascaris cuticle collagen and mammalian collagens: cell mediated and humoral immunity relationships. Journal of Immunology 109, 103–9.CrossRefGoogle ScholarPubMed
Smithers, S. R., Terry, R. J. & Hockley, D. J. (1969). Host antigens in schistosomiasis. Proceedings of the Royal Society of London B 171, 483–94.Google ScholarPubMed
Sogandares-Bernal, F. (1976). Immuno-globulins attached to and in the integument of adult Schistosoma mansoni Sambon 1907, from first infection CF1 mice. Journal of Parasitology 62, 222–6.CrossRefGoogle Scholar
Sogandares-Bernal, F. & Voge, M. (1978). Immunoglobulins on the surfaces of tetrathyridia of Mesocestoides corti Hoeppli 1925 (Cestoda) from laboratory infections of ICR mice. Journal of Parasitology 64, 620–4.CrossRefGoogle ScholarPubMed
Soulsby, E. J. L. (1970). Studies of the blood group and heterophile antigenic determinants of the cuticle of larvae of Ascaris suum. H. D. Srivastava Commemoration Volume, Prem, Lucknow, pp. 361–74.Google Scholar
Sprent, J. F. A. (1962). Parasitism, immunity and evolution. In The Evolution of Living Organisms (ed. Leeper, G. W.). Symposium of the Royal Society of Victoria, Melbourne, pp. 149165. Melbourne, Australia: University Press.Google Scholar
Torpier, G., Capron, A. & Ouassi, M. (1979). Receptor for IgG (Fe) and human β2-microglobulin on S. mansoni schistosomula. Nature, London 278, 447–9.CrossRefGoogle Scholar
Varela-Diaz, V. M. & Coltorti, E. A. (1972). Further evidence of the passage of host immunoglobulins into hydatid cysts. Journal of Parasitology 58, 1015–16.CrossRefGoogle ScholarPubMed
Varela-Diaz, V. M. & Coltorti, E. A. (1973). The presence of host immunoglobulins in hydatid cyst membranes. Journal of Parasitology 59, 484–8.CrossRefGoogle ScholarPubMed
Varela-Diaz, V. M., Williams, J. F., Coltorti, E. A. & Williams, C. S. F. (1974). Survival of cysts of Echinococcus granulosus after transplant into homologous and heterologous hosts. Journal of Parasitology 60, 608–12.CrossRefGoogle ScholarPubMed
Williams, J. F. (1982). Cestode infections. In Immunology of Parasitic Infections (ed. Cohen, S. and Warren, K.), pp. 676714. Oxford: Blackwell Scientific Publications.Google Scholar
Williams, J. F. & Soulsby, E. J. L. (1970). Antigenic analysis of the developmental stages of Ascaris suum. II. Host components. Experimental Parasitology 27, 362–7.CrossRefGoogle Scholar
Willms, K., Merchant, M. T., Arcos, L., Sealey, M., Diaz, S. & De Leon, L. D. (1980). Immunopathology of cysticercosis. In Molecules, Cells and Parasites in Immunology (ed. Flisser, A.Willms, K. and Larralde, C.), pp. 145–62. London: Academic Press.CrossRefGoogle Scholar