Hostname: page-component-77c89778f8-gq7q9 Total loading time: 0 Render date: 2024-07-25T02:34:51.907Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of immune responses between high and low responder strains of mice in the concomitant immunity and vaccine models of resistance to Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

Stephanie L. James  and
A. W. Cheever
Stephanie L. James
Affiliation:
Departments of Medicine and Microbiology, The George Washington University Medical Center, Washington, D.C. 20037
A. W. Cheever
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20205
Get access Rights & Permissions [Opens in a new window]

Extract

Mice of the inbred P strain fail to develop significant resistance to challenge Schistosoma mansoni infection at 6 weeks after either low-grade primary infection or vaccination with attenuated homologous parasites, in contrast to other strains such as C57B1/6, and thus provide a model for comparison of potential immune resistance mechanisms in low versus high responder animals. In this study, the antigen-specific cellular responses found to correlate with resistance in these strains were delayed cutaneous hypersensitivity, production of macrophage activating lymphokine and macrophage larvicidal activity, all of which were greater in infected or vaccinated C57B1/6 mice than in similarly immunized but non-resistant P mice. Humoral responses correlating with resistance were IgM reactivity to schistosomula surface antigens in both infected and vaccinated animals, as well as both IgM and IgG reactivity to soluble schistosome antigens in infected mice. Immune responses that showed no relationship with resistance included IgG reactivity to larval surface antigens and immediate hypersensitivity to soluble worm antigens. In infected mice, neither granuloma size nor extent of hepatic fibrosis correlated positively with resistance to challenge infection. Thus, similarities exist between patterns of resistance and immune response at this early time after immunization with either viable or attenuated parasites. These observations suggest that common immune effector mechanisms could be involved, with activated macrophages playing a central role in resistance.

Type
Research Article
Information
Parasitology , Volume 91 , Issue 2 , October 1985 , pp. 301 - 315
Copyright
Copyright © Cambridge University Press 1985

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

Bergman, I. & Loxley, R. (1963). Two improved and simplified methods for the spectrophotometric determination of hydroxyproline. Analytical Biochemistry 35, 1961–5.Google Scholar
Bickle, Q., Long, E., James, E., Doenhoff, M. & Festing, M. (1980). Schistosoma mansoni: influence of the mouse host's sex, age and strain on resistance to reinfection. Experimental Parasitology 50, 222–32.CrossRefGoogle ScholarPubMed
Boraschi, D. & Meltzer, M. S. (1980). Defective tumoricidal capacity of macrophages from P/J mice: tumoricidal defect involves abnormalities in lymphokine-derived activation stimuli and in mononuclear phagocyte responsiveness. Journal of Immunology 125, 777–82.CrossRefGoogle Scholar
Bradley, D. J. & McCullough, F. S. (1973). Egg output and the epidemiology of Schistosoma haemotobium. II. An analysis of the epidemiology of endemic S. haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 491–500.CrossRefGoogle Scholar
Byram, J. E., von Lichtenberg, F., Lewis, F. A. & Stirewalt, M. A. (1983). Pathology of a live attenuated anti-schistosome vaccine in mice. American Journal of Tropical Medicine and Hygiene 32, 94–108.CrossRefGoogle ScholarPubMed
Cheever, A. W. (1970). Relative resistance of human schistosomes to digestion in potassium hydroxide. Bulletin of the World Health Organization 43, 601–3.Google ScholarPubMed
Cheever, A. W., Dunn, M. A., Dean, D. A. & Duvall, R. H. (1983). Differences in hepatic fibrosis in ICR, C3H and C57BL/6 mice infected with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 32, 1364–9.CrossRefGoogle ScholarPubMed
Correa-Oliveira, R., Sher, A. & James, S. L. (1984 a). Defective vaccine-induced immunity to S. mansoni in P strain mice. I. Analysis of antibody responses. Journal of Immunology 133, 1581–6.CrossRefGoogle Scholar
Correa-Oliveira, R., sher, A. & James, S. L. (1984 b). Mechanisms of protective immunity against S. mansoni infection in mice vaccinated with irradiated cercariae. V. Anamnestic cellular and humoral responses following challenge infection. American Journal of Tropical Medicine and Hygiene 33, 261–8.CrossRefGoogle ScholarPubMed
Dean, D., Minard, P., Murrell, K. D. & Vannier, W. (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
Deelder, A. M., Kornelis, D., Makbin, M., Noordpool, H. N., Codfried, R. M., Rotmans, J. P. & Oostburg, B. F. J. (1980). Applicability of different antigen preparations in the enzyme-linked immunosorbent assay for schistosomiasis mansoni. American Journal of Tropical Medicine and Hygiene 29, 401–10.CrossRefGoogle ScholarPubMed
Doenhoff, M. & Long, E. (1979). Factors affecting the acquisition of resistance against S. mansoni in the mouse. IV. The inability of T cell-deprived mice to resistant reinfection and other in vivo studies on the mechanisms of resistance. Parasitology 78, 171–83.CrossRefGoogle Scholar
James, S. L., Correa-Oliveira, R. & Leonard, E. J. (1984). Defective vaccine-induced immunity to S. mansoni in P nice. II. Analysis of cellular responses. Journal of Immunology 133, 1587–93.CrossRefGoogle Scholar
James, S., Labine, M. & Sher, A. (1981). Mechanisms of protective immunity against S. mansoni infection in mice vaccinated with irradiated cercariae. Cellular Immunology 65, 75–83.CrossRefGoogle ScholarPubMed
James, S. L., Lazdins, J. K., Hieny, S. & Natovitz, P. (1983). Macrophages as effector cells of protective immunity in murine schistosomiasis. Journal of Immunology 131, 1481–6.CrossRefGoogle ScholarPubMed
James, S. L. & Sher, A. (1983). Mechanisms of protective immunity against S. mansoni infection in mice vaccinated with irradiated cercariae. Parasite Immunology 5, 567–75.CrossRefGoogle ScholarPubMed
James, S. L., Skamene, E. & Meltzer, M. S. (1983 a). Macrophages as effector cells of protective immunity in murine schistosomiasis. Journal of Immunology 131, 984–53.Google ScholarPubMed
Lazdins, J. K., Stein, M. J., David, J. R. & Sher, A. (1982). Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation and discontinuous gradients of Percoll. Experimental Parasitology 53, 39–44.CrossRefGoogle ScholarPubMed
Long, E., Doenhoff, M. & Bain, J. (1978). Factors affecting the acquisition of resistance against S. mansoni in the mouse. II. The time at which resistance to reinfection develops. Journal of Helminthology 52, 187–91.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1984). The migration and survival of gamma-irradiated Schistosoma mansoni larvae and the duration of host-parasite contact in relation to the induction of resistance in mice. Parasitology 88, 249–66.CrossRefGoogle Scholar
Miller, K. & Smithers, S. R. (1980). Schistosoma mansoni: The attrition of a challenge infection in mice immunized with highly irradiated live cercariae. Experimental Parasitology 50, 212–21.CrossRefGoogle ScholarPubMed
Minard, P., Dean, D. A., Jacobson, R. A., Vannier, W. E. & Murrell, K. D. (1978). Immunization of mice with Cobalt-60 irradiated S. mansoni cercariae. American Journal of Tropical Medicine and Hygiene 27, 76–86.CrossRefGoogle Scholar
Murrell, K. D., Clark, S., Dean, D. A. & Vannier, W. E. (1979). Influence of mouse strain on induction of resistance with irradiated Schistosoma mansoni cercariae. Journal of Parasitology 65, 829–30.CrossRefGoogle ScholarPubMed
Olds, G. R. & Ellner, J. J. (1984). Modulation of macrophage activation and resistance by suppressor T lymphocytes in chronic murine S. mansoni infection. Journal of Immunology 133, 2720–4.CrossRefGoogle Scholar
Sher, A., Hieny, S., James, S. L. & Asofsky, R. (1982). Mechanisms of protective immunity against S. mansoni infection in mice vaccinated with irradiated cercariae. Journal of Immunology 128, 1880–4.CrossRefGoogle ScholarPubMed
Sher, A., Smithers, S. R. & Mackenzie, P. (1975). Passive transfer of acquired resistance to S. mansoni in laboratory mice. Parasitology 70, 347–57.CrossRefGoogle Scholar
Smithers, S. R. & Doenhoff, M. J. (1982). Schistosomiasis. In Immunology of Parasitic Infections (ed. Cohen, S. and Warren, K. S.), pp. 527–607.Google Scholar
Smithers, S. R. & Gammage, K. (1979). 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.CrossRefGoogle Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of S. mansoni and recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle Scholar
Smithers, S. R. & Terry, R. J. (1969). Immunity in schistosomiasis. Annals of the New York Academy of Science 160, 826–40.CrossRefGoogle ScholarPubMed
Stirewalt, M. A., Minnick, D. R. & Fregeau, W. A. (1966). Definition and collection in quantity of schistosomula S. mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 352–60.CrossRefGoogle Scholar
Taylor, M. G., James, E. R., Nelson, G. S., Bickle, Q., Dunne, D. W. & Webbe, G. (1976). Immunization of sheep against S.matthei using either irradiated cercariae or irradiated schistosomula. Journal of Helminthology 50, 1–9.CrossRefGoogle ScholarPubMed
Warren, K. S. (1973). Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology? Journal of Infectious Diseases 127, 595–609.CrossRefGoogle ScholarPubMed
Warren, K. S. & Peters, P. A. (1967). Comparison of penetration and maturation of S. mansoni in the hamster, mouse, guinea pig, rabbit and rat. American Journal of Tropical Medicine and Hygiene 16, 718–22.CrossRefGoogle Scholar
Wilson, R. A., Coulson, R. S. & McHugh, S. M. (1983). A significant part of the concomitant immunity of mice to S. mansoni is the consequence of a leaky hepatic portal system, not immune killing. Parasite Immunology 5, 595–601.CrossRefGoogle Scholar
Zodda, D. & Phillips, S. M. (1982). Monoclonal antibody-mediated protection against S. mansoni infection in mice. Journal of Immunology 129, 2326–8.CrossRefGoogle ScholarPubMed