Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-25T15:51:24.276Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro proliferative response to living schistosomula by T lymphocytes from mice infected with Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

S. L. James
S. L. James
Affiliation:
Department of Medicine, Harvard Medical School, Brigham and Women's Hospital, Boston, Massachusetts 02115
Get access Rights & Permissions [Opens in a new window]

Summary

The development of T cell reactivity toward schistosomula during murine Schistosoma mansoni infection has been studied using an adaptation of the in vitro lymphocyte proliferation assay in which the response is elicited by exposure to living schistosomula. The reactivity measured in this system was shown to be a T lymphocyte function and to require the presence of adherent cells. This assay may therefore provide a new method for analysis of basic interactions between host cells and schistosomula. Lymph node cell responses were observed in two phases, the first of which appeared during the second week after infection, reflecting the immunogenicity of schistosome larval forms. A later, more pronounced response appeared during the chronic stage of infection, where sensitization appeared to be stimulated primarily by ongoing exposure to adult worms, rather than eggs. Lung-stage and skin-stage larvae elicited a similar degree of thymidine uptake by cells from chronically infected mice. Intact skin-stage larvae and particulate fractions provoked greater proliferation than soluble larval constituents, indicating that the lymphocyte response is directed in large part toward determinants which remain associated with the schistosomula during culture. However, the presence of major histocompatibility complex products on the membrane of lung-stage schistosomula did not influence the presentation of larval antigens to sensitized lymphocytes. The implications of these findings in immunity to schistosomiasis are discussed.

Type
Research Article
Information
Parasitology , Volume 83 , Issue 1 , August 1981 , pp. 147 - 162
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

Anwar, A. R. E., Smithers, S. R. & Kay, A. B. (1979). Killing of schistosomula of Schistosoma mansoni coated with antibody and/or complement by human leukocytes in vitro: requirement for complement in preferential killing by eosinophils. Journal of Immunology 122, 628–37.Google Scholar
Butterworth, A. E., Vadas, M. A., Martz, E. & Sher, A. (1979 a). Cytolytic T lymphocytes recognize alloantigens on schistosomula of Schistosoma mansoni but fail to induce damage. Journal of Immunology 122, 1314–21.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Vadas, M. A., Wassom, D. L., Dessein, A., Hogan, M., Sherry, B., Gleich, G. J. & David, J. R. (1979 b). Interactions between human eosinophils and schistosomula of Schistosoma mansoni. II. The mechanism of irreversible eosinophil adherence. Journal of Experimental Medicine 150, 1456–71.CrossRefGoogle ScholarPubMed
Capron, A., Dessaint, J. P. & Capron, M. (1975). Specific IgE antibodies in immune adherence of normal macrophages to Schistosoma mansoni schistosomules. Nature, London 253, 474–5.CrossRefGoogle ScholarPubMed
Capron, M., Torpier, G. & Capron, A. (1979). In vitro killing of S. mansoni schistosomula by eosinophils from infected rats: role of cytophilic antibodies. Journal of Immunology 123, 2220–30.CrossRefGoogle ScholarPubMed
Clegg, 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, 79–98.Google Scholar
Colley, D. G. (1972). Schistosoma mansoni: eosinophilia and the development of lymphocyte blastogenesis in response to soluble egg antigen in inbred mice. Experimental Parasitology 32, 520–6.CrossRefGoogle ScholarPubMed
Colley, D. G., Cook, J. A., Freeman, G. L., Bartholomew, R. K. & Jordan, P. (1977). Immune responses during human Schistosomoniasis mansoni. I. In vitro lymphocyte blastogenic responses to heterogeneous antigenic preparations from schistosome eggs, worms and cercariae. International Archives of Allergy and Applied Immunology 53, 420–33.CrossRefGoogle ScholarPubMed
Dean, D. A., Minard, P., Murrell, K. D. & Vannier, W. E. (1978). Resistance of mice to secondary infection with Schistosoma mansoni. II. Evidence for a correlation between egg deposition and worm elimination. American Journal of Tropical Medicine and Hygiene 27, 957–65.CrossRefGoogle Scholar
Doenhoff, M. & Long, E. (1979). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. IV. The inability of T cell-deprived mice to resist re-infection, and other in vivo studies on the mechanisms of resistance. Parasitology 78, 171–83.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.Google Scholar
James, S. L. & Sher, A. (1980). Immune mechanisms that stimulate mouse leukocyte migration in response to schistosomula of Schistosoma mansoni. Journal of Immunology 124, 1837–44.CrossRefGoogle ScholarPubMed
Julius, M. H., Simpson, E. & Herzenberg, L. A. (1973). A rapid method for the isolation of functional thymus-derived murine lymphocytes. European Journal of Immunology 3, 645–9.Google Scholar
Katz, S. P. & Colley, D. G. (1976). Induction of cellular and humoral immunological responsiveness to a soluble cercarial antigen preparation from Schistosoma mansoni. Infecand Immunity 14, 502–8.CrossRefGoogle ScholarPubMed
Khoury, P. B., Reid, W. A., Weiner, D. J., Soulsby, E. J. L. & Phillips, S. M. (1980). Kinetics and characterization of antigen-binding and antibody producing cells in the draining lymph nodes and spleen during initial murine schistosomiasis. I. Cellular responses against antigens. Cellular Immunology (in the Press).Google Scholar
Lazdins, J., Stein, M., David, J. R. & Sher, A. (1981). Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation on discontinuous density gradients of percoll. Experimental Parasitology (in the Press).Google Scholar
Lowry, O. H., Rosebrough, A. L., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265–75.Google Scholar
Maddison, S. E. & Kagan, I. G. (1979). Adoptive transfer of protective immunity in experimental schistosomiasis in the mouse. Journal of Parasitology 65, 515–19.Google Scholar
Mahmoud, A. A. F., Warren, K. S. & Graham, R. C. (1975). Antieosinophil serum and the kinetics of eosinophilia in Schistosoma mansoni. Journal of Experimental Medicine 142, 560–74.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
Ottesen, E. A., Hiatt, R. A., Cheever, A. W., Sotomayer, Z. R. & Neva, F. A. (1978). The acquisition and loss of antigen-specific cellular immune responsiveness in acute and chronic schistosomiasis in man. Clinical and Experimental Immunology 33, 38–47.Google ScholarPubMed
Phillips, S. M., Reid, W. A., Bruce, J. I., Hedlund, K., Colvin, R. C., Campbell, B., Diggs, C. L. & Sadun, E. H. (1976). The cellular and humoral immune response to Schistosoma mansoni infections in inbred rats. I. Mechanisms during initial exposure. Cellular Immunology 19, 99–116.Google 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
Ramalro-Pinto, F. J., Smithers, S. R. & Playfair, J. H. L. (1979). Carrier effect during the course of experimental schistosomiasis: suppression of the response to TNP-schistosomula in rats and inbred mice. Journal of Immunology 123, 507–14.CrossRefGoogle Scholar
Sher, A. (1977). Immunity against Schistosomiasis mansoni in the mouse. American Journal of Tropical Medicine and Hygiene 26, 20–8.Google Scholar
Sher, A. & Moser, G. (1980). Schistosomiasis: immunological properties of developing schistosomula. American Journal of Pathology 102, 121–6.Google Scholar
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.Google Scholar
Sher, 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 mouse. Journal of Infectious Diseases 130, 626–33.CrossRefGoogle ScholarPubMed
Sher, A., Smithers, S. R. & Mackenzie, P. (1975). Passive transfer of acquired resistance to Schistosoma mansoni in laboratory mice. Parasitology 70, 347–57.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Gammage, K. (1980). The recovery of schistosomula of Schistosoma mansoni 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.CrossRefGoogle Scholar
Stirewalt, M. A., Minnick, D. R. & Fregeau, W. A. (1966). Definition and collection in quantity of schistosomula of Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 352–60.CrossRefGoogle Scholar