Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T08:21:36.321Z Has data issue: false hasContentIssue false
  • English
  • Français

Evidence that radio-sensitive cells are central to skin-phase protective immunity in CBA/Ca mice vaccinated with radiation-attenuated cercariae of Schistosoma mansoni as well as in naive mice protected with vaccine serum

Published online by Cambridge University Press:  06 April 2009

V. S. Delgado  and
D. J. McLaren
V. S. Delgado
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
D. J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
Get access Rights & Permissions [Opens in a new window]

Summary

Naive CBA/Ca mice and CBA/Ca mice vaccinated 4 weeks previously with radiation-attenuated cercariae of Schistosoma mansoni were subjected to 550 rad of whole body (gamma) irradiation and then challenged 3 days laterwith normal cercariae. The perfusion recovery data showed that this procedure reduced theprimary worm burden in naive mice by 22% and the challenge worm burden in vaccinated mice by 82%. Irradiation also ablated the peripheral blood leucocytes of both mouse groups by 90%–100% at the time of challenge. Histological data revealed that such treatment caused a dramatic change in number, size and leucocyte composition of cutaneous inflammatory skin reactions that characterize challenged vaccinated mice and are known to entrap invading larvae; cutaneous eosinophils were preferentially abolished by this treatment. Polyvaccine mouse serum that conferred protection passively upon naive recipient mice, failed to protect naive/irradiated mice when administered by the same protocol. Distraction of macrophages by treatment of mice with silica did not affect the establishment of a primary worm burden and reduced the protection exhibited by vaccinated mice by only 16%. These data indicate that radio-sensitive cells are important to both innate and specific acquired resistance in this mouse model and that macrophages contribute only marginally to the expression of vaccine immunity.

Keywords

Schistosoma mansoniimmunityradio-sensitive cellsresistancevaccination
Type
Research Article
Information
Parasitology , Volume 100 , Issue 1 , February 1990 , pp. 45 - 56
Copyright
Copyright © Cambridge University Press 1990

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

Aitken, R., Coulson, P. S., Dixon, B. & Wilson, A. (1987). Radiation-resistant acquired immunity of vaccinated mice to Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 37, 570–7.CrossRefGoogle ScholarPubMed
Allison, A. C. (1976). Fluorescence microscopy of lymphocytes and mononuclear phagocytes and the use of silica to eliminate the latter. In In Vitro Methods in Cell-Mediated and Tumor Immunity (ed. Bloom, B. & David, J.), pp. 395–404. New York: Academic Press.Google Scholar
Allison, A. C. & Hart, D'A. P. (1968). Potentiation by silica of growth of Mycobacterium tuberculosis in macrophage cultures. British Journal of Experimental Pathology 49, 465–76.Google ScholarPubMed
Bickle, Q. D., Dobinson, T. & James, E. R. (1979). The effect of gamma-irradiation on migration and survival of Schistosoma mansoni schistosomula in mice. Parasitology 79, 223–30.CrossRefGoogle ScholarPubMed
Butterworth, E. A. (1984). Cell-mediated damage to helminths. Advances in Parasitology 23, 144–207.Google ScholarPubMed
Capron, A., Dessaint, J. P., Capron, M., Joseph, M. & Torpier, G. (1982). Effector mechanisms of immunity to schistosomes and their regulation. Immunological Reviews 61, 41–66.CrossRefGoogle ScholarPubMed
Cawley, S., Findon, G. & Miller, T. E. (1988). Peripheral blood leukocyte count as an index of defense status in the leukopenic host. Journal of Laboratory and Clinical Medicine 112, 52–7.Google ScholarPubMed
Crabtree, J. E. & Wilson, R. A. (1986). The role of pulmonary cellular reactions in the resistance of vaccinated mice to Schistosoma mansoni. Parasite Immunology 8, 265–85.CrossRefGoogle ScholarPubMed
Dean, D. A., Bukowski, M. A. & Cheever, A. W. (1981). Relationship between acquired resistance, portal hypertension and lung granulomas in ten strains of mice infected with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 30, 806–14.CrossRefGoogle ScholarPubMed
Dean, D. A., Mangold, B. L., Georgi, J. R. & Jacobson, R. H. (1984). Comparison of Schistosoma mansoni migration patterns in normal and irradiated cercariae-immunized mice by means of autoradiographic analysis. Evidence that worm elimination occurs after the skin phase in immunized mice. American Journal of Tropical Medicine and Hygiene 33, 89–96.CrossRefGoogle Scholar
Delgado, V. S. & McLaren, D. J. (1989). Contribution of IgG1 and radio-resistant cells to immune expression in guinea-pigs vaccinated with radiation-attenuated cercariae of Schistoma mansoni. International Journal for Parasitology (in the Press).Google Scholar
Ford, M. J., Bickle, Q. D. & Taylor, M. G. (1987). Immunity to Schistosoma mansoni in congenitally athymic irradiated and mast cell-depleted rats. Parasitology 89, 313–26.CrossRefGoogle Scholar
Harriott-Smith, S. T. & Halliday, J. (1988). Suppression of contact hypersensitivity by short-term ultraviolet irradiation. I. Immunosuppression by serum from irradiated mice. Clinical and Experimental Immunology 71, 144–8.Google ScholarPubMed
Harrison, R. A., Bickle, Q. & Doenhoff, M. J. (1982). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. Evidence that the mechanisms which mediate resistance during early patent infections may lack immunological specificity. Parasitology 84, 93–110.CrossRefGoogle ScholarPubMed
Howard, J. G., Hale, C. & Liew, F. Y. (1981). Immunological regulation of experimental cutaneous leishmaniasis. IV. Prophylactic effect of sublethal irradiation as a result of abrogation of suppressor T cell generation in mice genetically susceptible to Leishmania tropica. Journal of Experimental Medicine 153, 557–68.CrossRefGoogle ScholarPubMed
Incani, R. N & McLaren, D. J. (1984). Histopathological and ultrastructural studies of cutaneous reactions elicited in naive and chronically infected mice by invading schistosomula of Schistosoma mansoni. International Journal for Parasitology 14, 250–76.CrossRefGoogle ScholarPubMed
James, S. L., Correa-Oliveira, R. & Leonard, E. J. (1984). Defective vaccine-induced immunity to Schistosoma mansoni in P strain mice. II. Analysis of cellular responses. Journal of Immunology 133, 1587–93.CrossRefGoogle Scholar
James, S. L., Leonard, E. J. & Meltzer, M. S. (1982). Macrophages as effector cells of protective immunity in murine schistosomiasis. IV. Coincident induction of macrophage activation for extracellular killing of schistosomula and tumor cells. Cellular Immunology 74, 74–86.CrossRefGoogle ScholarPubMed
James, S. L. & Sher, A. (1983). Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. III. Identification of a mouse strain, P/N, that fails to respond to vaccination. Parasite Immunology 5, 567–75.CrossRefGoogle Scholar
Kamiya, H., Smithers, S. R. … McLaren, D. J. (1987). Schistosoma mansoni: autoradiographic tracking studies of isotopically-labelled challenge parasites in naive and vaccinated CBA/Ca mice. Parasite Immunology 9, 515–29.CrossRefGoogle ScholarPubMed
Keller, R. (1973). Cytostatic elimination of syngeneic rat tumor cells in vitro by nonspecifically activated macrophages. Journal of Experimental Medicine 138, 625–44.CrossRefGoogle ScholarPubMed
Lendrum, A. C. (1944). The staining of eosinophil polymorphs and enterochromaffin cells in histological sections. Journal of Pathology and Bacteriology 56, 441.CrossRefGoogle Scholar
Levy, M. H. & Wheelock, E. F. (1975). Effect of intravenous silica on immune and non-immune function of the murine host. Journal of Immunology 115, 41–8.CrossRefGoogle ScholarPubMed
Lichtenberg, F. Von, Sher, A., Gibbons, N. & Doughty, B. (1976). Eosinophil-enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 84, 479–99.Google ScholarPubMed
Liew, F. Y., Hale, C. & Howard, J. G. (1982). Immunological regulation of experimental cutaneous leishmaniasis. V. Characterisation of effector and specific suppressor T cells. Journal of Immunology 128, 1917–22.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.). Chichester: John Wiley/Research Studies Press.Google Scholar
McLaren, D. J. (1982). Role of granulocytes in immune defense against parasites. Zentralblatt für Bakteriologie und Parasitenkunde 12, 57–73.Google Scholar
McLaren, D. J., Pearce, E. J. & Smithers, S. R. (1985). Site potential for challenge attrition in mice, rats and guinea-pigs vaccinated with irradiated cercariae of Schistosoma mansoni. Parasite Immunology 7, 29–44.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Smithers, S. R. (1987). The immune response to schistosomes in experimental hosts. In The Biology of Schistosomes (ed. Rollinson, D. & Simpson, A. J. G.), pp. 233–63. London: Academic Press.Google Scholar
McLaren, D. J. & Smithers, S. R. (1988). Serum from CBA/Ca mice vaccinated with irradiated cercariae of Schistosoma mansoni protects naive recipients through the recruitment of cutaneous effector cells. Parasitology 97, 287–302.Google ScholarPubMed
McLaren, D. J., Strath, M. & Smithers, S. R., (1987). Schistosoma mansoni: evidence that immunity in vaccinated and chronically infected CBA/Ca mice is sensitive to treatment with a monoclonal antibody that depletes cutaneous effector cells. Parasite Immunology 9, 667–82.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1983). Autoradiographic analysis of Schistosoma mansoni migration from skin to lungs in naive mice. Evidence that most attrition occurs after the skin phase. American Journal of Tropical Medicine and Hygiene 32, 785–9.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1986). Passive transfer with serum and IgG antibodies of irradiated cercariae-induced resistance against Schistosoma mansoni in mice. Journal of Immunology 136, 2644–8.CrossRefGoogle Scholar
Mangold, B. L., Dean, D. A., Coulson, P. S. & Wilson, R. A. (1986). Site requirements and kinetics of immune-dependent elimination of intravascularly administered lung stage schistosomula in mice immunized with highly irradiated cercariae of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 35, 332–40.CrossRefGoogle ScholarPubMed
Mastin, A. J., Bickle, Q. D. & Wilson, R. A. (1983). Schistosoma mansoni: migration and attrition of irradiated and challenge schistosomula in the mouse. Parasitology 87, 87–102.CrossRefGoogle ScholarPubMed
Miller, K. L., Smithers, S. R. & Sher, A. (1981). The response of mice immune to Schistosoma mansoni to a challenge infection which bypasses the skin: evidence for two mechanisms of immunity. Parasite Immunology 3, 25–31.CrossRefGoogle ScholarPubMed
Minard, P., Dean, D. A., Jacobson, R. H., Vannier, W. E. & Murrell, K. D. (1978). Immunization of mice with cobalt-60 irradiated Schistosoma mansoni cercariae. American Journal of Tropical Medicine and Hygiene 27, 76–93.CrossRefGoogle ScholarPubMed
Nelson, E. L. & Backer, J. R. (1959). The effect of whole-body X-irradiation on the bactericidal activity of phagocytic cells. II. Survival of Pseudomonas aeruginosa within livers and spleens of mice. Journal of Infectious Diseases 104, 20–3.CrossRefGoogle Scholar
O'Brien, A. D., Scher, I. & Formal, S. B. (1979). Effect of silica on the innate resistance of inbred mice to Salmonella typhimurium infection. Infection and Immunity 25, 513–20.CrossRefGoogle ScholarPubMed
Pearsall, N. N. & Weiser, R. S. (1968). The macrophage in allograft immunity. Effect of silica as a specific macrophage toxin. Journal of the Reticuloendothial Society 5, 107–20.Google ScholarPubMed
Pomeroy, C. & Filice, G. A. (1988). Effect of intravenous silica on the course of Nocardia asteroides pneumonia. Infection and Immunity 56, 2507–11.CrossRefGoogle ScholarPubMed
Rios, A. & Simmons, R. L. (1972). Poly-2-vinylpyridine- N-oxide reverses the immunosuppressive effects of silica and carrageenan. Transplantation 13, 343–5.CrossRefGoogle ScholarPubMed
Sher, A., Hieny, S., James, S. L. & Asofsky, R. (1982). Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. II. Analysis of immunity in hosts deficient in T lymphocytes, B lymphocytes or complement. Journal of Immunology 128, 1880–4.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Doenhoff, M. J. (1982). Schistosomiasis. In Immunology of Parasitic Infections (ed. Cohen, S. & Warren, K. S.), pp. 527–607. Oxford: Blackwell Scientific Publications.Google Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Thompson, J. C. & Johnstone, A. C. (1987). The effects of gamma-irradiation on haemopoiesis and red blood cell destruction in hamsters infected with Leptospira interrogans serovar ballum. British Journal of Experimental Pathology 68, 389–98.Google ScholarPubMed
Vignali, D. A. A., Bickle, Q. D. & Taylor, M. G. (1988). Studies on immunity to Schistosoma mansoni in vivo: whole-body irradiation has no effect on vaccine-induced resistance in mice. Parasitology 96, 49–61.CrossRefGoogle ScholarPubMed
Ward, R. M. & McLaren, D. J. (1988). Schistosoma mansoni: evidence that eosinophils and/or macrophages contribute to skin-phase challenge attrition in vaccinated CBA/Ca mice. Parasitology 96, 63–84.CrossRefGoogle ScholarPubMed
Wilson, R. A. (1987). Cercariae to liver worms: development and migration in the mammalian host. In The Biology of Schistosomes (ed. Rollinson, D. & Simpson, A. J. G.), pp. 115–46. London: Academic Press.Google Scholar
Wilson, R. A., Coulson, P. S. & Dixon, B. (1986). Migration of schistosomula of Schistosoma mansoni in mice vaccinated with radiation-attenuated cercariae, and normal mice: an attempt to identify the timing and site of parasite death. Parasitology 92, 101–16.CrossRefGoogle ScholarPubMed
Wilson, R. A., Coulson, P. S. & Mchugh, S. M. (1983). A significant part of the concomitant immunity of mice to Schistosoma mansoni is a consequence of a leaky hepatic portal system, not immune killing. Parasite Immunology 5, 595–601.CrossRefGoogle Scholar