Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-19T16:38:25.207Z Has data issue: false hasContentIssue false
  • English
  • Français

Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules

Published online by Cambridge University Press:  06 April 2009

A. Dessein ,
J. C. Samuelson ,
A. E. Butterworth ,
Maureen Hogan ,
Barbara A. Sherry ,
M. A. Vadas  and
J. R. David
A. Dessein
Affiliation:
Department of Medicine, Harvard Medical School and the Department of Rheumatology and Immunology, Robert B. Brigham Division, Brigham and Women's Hospital, Boston, Massachusetts 02115
J. C. Samuelson
Affiliation:
Department of Medicine, Harvard Medical School and the Department of Rheumatology and Immunology, Robert B. Brigham Division, Brigham and Women's Hospital, Boston, Massachusetts 02115
A. E. Butterworth
Affiliation:
Department of Medicine, Harvard Medical School and the Department of Rheumatology and Immunology, Robert B. Brigham Division, Brigham and Women's Hospital, Boston, Massachusetts 02115
Maureen Hogan
Affiliation:
Department of Medicine, Harvard Medical School and the Department of Rheumatology and Immunology, Robert B. Brigham Division, Brigham and Women's Hospital, Boston, Massachusetts 02115
Barbara A. Sherry
Affiliation:
Department of Medicine, Harvard Medical School and the Department of Rheumatology and Immunology, Robert B. Brigham Division, Brigham and Women's Hospital, Boston, Massachusetts 02115
M. A. Vadas
Affiliation:
Department of Medicine, Harvard Medical School and the Department of Rheumatology and Immunology, Robert B. Brigham Division, Brigham and Women's Hospital, Boston, Massachusetts 02115
J. R. David
Affiliation:
Department of Medicine, Harvard Medical School and the Department of Rheumatology and Immunology, Robert B. Brigham Division, Brigham and Women's Hospital, Boston, Massachusetts 02115
Get access Rights & Permissions [Opens in a new window]

Summary

Schistosomula of Schistosoma mansoni, recovered either after penetration of cercariae through isolated rat skin or by mechanical transformation of cercariae, become fully resistant after 24–48 h of culture to damage by human blood eosinophils in the presence of human anti-schistosomular sera. Cultured schistosomula are also shown to lose their susceptibility to attack by human eosinophils in the presence of human complement. This resistance is related to the simultaneous reduction of the ability of human anti-schistosomular antibodies and human complement component C3 to bind to the surface of the cultured larvae. The development of insusceptibility to antibody, complement and eosinophil-mediated attack does not require the acquisition by the schistosomula of a protective coat of host or other macromolecules, since it is achieved in chemically defined culture medium free of serum and macromolecules. This supports the hypothesis that schistosomula undergo intrinsic changes which render them insusceptible to immune attack.

Type
Research Article
Information
Parasitology , Volume 82 , Issue 3 , June 1981 , pp. 357 - 374
Copyright
Copyright © Cambridge University Press 1981

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

Anwar, A. R. E., Smithers, S. R. & Kay, A. B. (1979). Killing of schistosomula of Schistosoma mansoni coated with antibody or complement by human leukocytes in vitro. Requirement for complement in preferential killing by eosinophils. Journal of Immunology 122, 628–37.CrossRefGoogle ScholarPubMed
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, 73–86.CrossRefGoogle ScholarPubMed
Butterworth, A. E., David, J. R., Franks, D., Mahmoud, A. A. F., David, R. H., Sturrock, R. F. & Houba, V.(1977 a). Antibody-dependent eosinophil-mediated damage to 51Cr-labelled schistosomula of Schistosoma mansoni. Damage by purified eosinophils. Journal of Experimental Medicine 145, 136–50.Google Scholar
Butterworth, A. E., Remold, H. G., Houba, V., David, J. R., Peters, D. R., David, R. H. & Sturrock, R. F.(1977 b). Antibody-dependent eosinophil-mediated damage to 51Cr-labelled schistosomula of Schistosoma mansoni: mediation by IgG and inhibition by antigen-antibody complexes. Journal of Immunology 118, 2230–6.CrossRefGoogle Scholar
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–47.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1971). Acquisition of human antigens by Schistosoma mansoni during cultivation in vitro. Nature, London 232, 653–4.Google Scholar
Clegg, J. A. & Smithers, S. R. (1972). The effect of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 79–98.Google Scholar
Clegg, J. A., Smithers, S. R. & Terry, R. J. (1970). Concomitant immunity and host antigens associated with schistosomiasis. International Journal for Parasitology 1, 43–9.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.Google Scholar
Eisen, H. & Tallan, I. (1978). Tetrahymena pyriformis recovers from antibody immobiliation by producing antibody fragments. Nature, London 270, 514–15.CrossRefGoogle Scholar
Fearon, D. T. (1978). Regulation by membrane sialic acid of βlH-dependent decay- dissociation of amplification C3 convertase of the alternative complement pathway. Proceedings of the National Academy of Sciences, USA 75, 1971–5.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 Scholar
Goldring, O. L., Sher, A., Smithers, S. R. & McLaren, D. J. (1977). Host antigens and parasite antigens in murine Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 144–8.Google Scholar
Hockley, D. J. & McLaren, D. J. (1973). Schistosoma mansoni: changes in outer membrane of the tegument during the development from cercariae to adult worm. International Journal for Parasitology 3, 133–47.Google Scholar
Hsü, S. Y. G., Lust, G. L. & Hsü, H. F. (1971). The fate of challenge schistosome cercariae in a monkey immunized by cercariae exposed to high doses of X-irradiation. Proceedings of the Society for Experimental Biology and Medicine 136, 727–31.Google Scholar
Iscove, N. N. & Melchers, F. (1978). Complete replacement of serum by albumin, transferrin and soybean lipid in cultures of lipopolysaccharide-reactive B lymphocytes. Journal of Experimental Medicine 147, 923–33.Google Scholar
Imohiosen, E. A. E., Sher, A. & Von Lichtenberg, F. (1978). Early developmental changes of the schistosomula of Schistosoma mansoni in vitro and in mouse lung. Parasitology 76, 317–26.Google Scholar
Karnovsky, M. J. (1975). A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. Journal of Cell Biology 27, 137 a (Abstract).Google Scholar
Mahmoud, A. A. F., Warren, K. S. & Peters, P. A. (1975). A role for the eosinophil in acquired resistance to Schistosoma mansoni infection as determined by antieosinophil serum. Journal of Experimental Medicine 142, 805–13.Google Scholar
McLaren, D. G., 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, 67–75.Google Scholar
Perez, H., Clegg, J. A. & Smithers, S. R. (1974). Acquired immunity to S. mansoni in the rat: measurement of immunity by the lung recovery technique. Parasitology 69, 349–59.CrossRefGoogle Scholar
Phillips, S. M. & Colley, D. G. (1978). Immunologic aspects of host responses to schistosomiasis: resistance, immunopathology and eosinophil involvement. Progress in Allergy 24, 49–182.Google Scholar
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E., Mota-Santos, T. A., Figueiredo, E. A. & Pellegrino, J. (1974). Schistosoma mansoni: defined system for a stepwise trans. formation of cercariae to schistosomula in vitro. Experimental Parasitology 36, 360–72.CrossRefGoogle Scholar
Ramalho-Pinto, F. J., McLaren, D. J. & Smithers, S. R. (1978). Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. Journal of Experimental Medicine 147, 147–56.CrossRefGoogle ScholarPubMed
Samuelson, J. C., Sher, A. & Caulfield, J. P. (1980). Newly transformed schistosomula spontaneously lose their surface antigens and C3 receptor sites during cultures. Journal of Immunology 124, 2055–7.CrossRefGoogle Scholar
Santoro, F., Lachmann, P. J., Capron, A. & Capron, M. (1979). Activation of complement by Schistosoma mansoni schistosomula: killing of parasites by the alternative pathway and requirement of IgG for classical pathway activation. Journal of Immunology 123, 1551–7.Google Scholar
Sher, A. (1977). Immunity against Schistosoma mansoni in the mouse. American Journal of Tropical Medicine and Hygiene 26, 20–8.CrossRefGoogle ScholarPubMed
Sher, A., Hall, B. F. & Vadas, M. A. (1978). Acquisition of murine major histocompatibility complex gene products by schistosomula of Schistosoma mansoni. Journal of Experimental Medicine 148, 46–57.CrossRefGoogle ScholarPubMed
Sher, F. A., MacKenzie, P. & Smithers, S. R. (1974). Decreased recovery of invading parasites from the lungs as a parameter of acquired immunity to schistosomiasis in the laboratory mouse. Journal of Infectious Diseases 130, 626–33.CrossRefGoogle Scholar
Smith, M. V. & Kusel, J. R. (1979). The acquisition of antigens in the intercellular substance of mouse skin by schistosomula of Schistosoma mansoni. Clinical and Experimental Immunology 36, 430–5.Google ScholarPubMed
Smithers, S. R. & Gamage, K. (1980). The recovery of schistosomula from the skin, lungs and hepatic portal system of non-infected and S. mansoni-infected mice: evidence for two phases of parasite attrition in immune mice. Parasitology 80, 289–300.Google Scholar
Smithers, S. R., McLaren, D. J. & Ramalho-Pinto, F. J. (1977). Immunity to schistosomes: the target. American Journal of Tropical Medicine and Hygiene 26, 11–19.Google Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosomiasis mansoni and the recovery of adult worms. Parasitolgy 55, 695–700.Google Scholar
Smithers, S. R. & Terry, R. J. (1969). Immunity in schistosomiasis. Annals of the New York Academy of Sciences 160, 826–40.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Terry, R. J. (1976). The immunology of schistosomiasis. Advances in Parasitology 14, 399–422.CrossRefGoogle ScholarPubMed
Smithers, S. R., Terry, R. J. & Hockley, D. J. (1969). Host antigens in schintosomiasis. Proceedings of the Royal Society of London, B 171, 483–94.Google Scholar
Stirewalt, M. A., Minnick, D. R. & Fregean, W. A. (1966). Definition and collection in quantity of schistosmula of Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 352–60.Google Scholar
Tavares, C. A. P., Cordeiro, M. N., Mota-Santos, T. A. & Gazzinelli, G. (1980). Artificially transformed schistosomula of Schistosoma mansoni: mechanism of acquisition of protection against antibody-mediated killing. Parasitology 80, 95–104.Google Scholar
Tavares, C. A. P., Soares, R. C., Coelho, M. Z. & Gazzinelli, G. (1978). Schistosoma mansoni: evidence for a role of serum factors in protecting artificially transformed schistosomula against antibody-mediated killing in vitro. Parasitology 77, 225–33.Google Scholar
Torpier, G., Capron, A. & Ouaissi, M. A. (1979). Receptor for IgG (Fc) and human ° microglobulin on S. mansoni schistosomula. Nature, London 278, 447–9.Google Scholar
Vadas, M. A., David, J. R., Butterworth, A. E., Pisani, N. T. & Siongok, T. A. (1979). A new method of purification of human eosinophils and neutrophils and a comparison of the ability of these cells to damage schistosomula of Schistosoma mansoni. Journal of Immunology 122, 1228–36.CrossRefGoogle Scholar