Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-26T10:38:55.386Z Has data issue: false hasContentIssue false

Studies on immunity to Schistosoma mansoni in vivo: whole-body irradiation has no effect on vaccine-induced resistance in mice

Published online by Cambridge University Press:  06 April 2009

D. A. A. Vignali
Affiliation:
Department of Medical Helminthology, Winches Farm Laboratories, London School of Hygiene and Tropical Medicine, 395 Hatfield Road, St Albans, Herts., AL4 0XQ
Q. D. Bickle
Affiliation:
Department of Medical Helminthology, Winches Farm Laboratories, London School of Hygiene and Tropical Medicine, 395 Hatfield Road, St Albans, Herts., AL4 0XQ
M. G. Taylor
Affiliation:
Department of Medical Helminthology, Winches Farm Laboratories, London School of Hygiene and Tropical Medicine, 395 Hatfield Road, St Albans, Herts., AL4 0XQ

Summary

Actively immunized mice, whole-body irradiated with 650 or 525 rad., manifested comparable levels of resistance to Schistosoma mansoni compared with unirradiated, immunized mice in spite of a marked reduction in circulating leucocytes (>90%) and platelets (>85%), and despite an abrogation of delayed-type hypersensitivity (DTH) (Type IV) response to schistosomular antigens (as determined by footpad swelling, 24 h after injection of antigen). However, limited histopathological comparison of lung sections from irradiated and unirradiated mice 7 days post-challenge showed that cellular reactions (‘foci’) around parasites were essentially similar in size and cellular composition except that in irradiated mice, eosinophils were poorly represented both in the foci and in lung tissue in general. Neither presumed immune complex-mediated (Type III, Arthus reaction) hypersensitivity (as determined by footpad swelling, 5 h after injection of antigen) nor serum anti-schistosomulum extract antibody levels (as determined by ELISA) were affected. In addition, the pattern of 125I-labelled schistosomular surface antigens immunoprecipitated with serum from irradiated and unirradiated mice was essentially similar. These results are consistent with antibody playing an important role in vaccine-induced immunity in mice but suggest that radiosensitive T cell function and radiosensitive cells, such as platelets and polymorphonuclear cells, including eosinophils, may not be essential.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

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

Anderson, R. E., Sprent, J. & Miller, J. F. A. P. (1974). Radiosensitivity of T and B lymphocytes. I. Effect of irradiation on cell migration. European Journal of Immunology 4, 199203.CrossRefGoogle Scholar
Anderson, R. E. & Warner, N. L. (1970). Ionizing radiation and the immune response. In Advances in Immunology, vol. 24 (ed. Dixon, F. J. and Kunkel, H. G.), pp. 215335. London: Academic Press.Google Scholar
Bickle, Q. D., Andrews, B. J., Doenhoff, M. J., Ford, M. J. & Taylor, M. G. (1985). Resistance against Schistosoma mansoni induced by highly irradiated infections: studies on the species specificity of immunization and attempts to transfer resistance. Parasitology 90, 301–12.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Andrews, B. J. & Taylor, M. G. (1986). Schistosoma mansoni: characterization of two protective monoclonal antibodies. Parasite Immunology 8, 95107.CrossRefGoogle ScholarPubMed
Bickle, Q. D. & Ford, M. J. (1982). Studies on the surface antigenicity and susceptibility to antibody-dependent killing of developing schistosomula using sera from chronically infected mice and mice vaccinated with irradiated cercariae. Journal of Immunology 128, 2101–6.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Taylor, M. G., Doenhoff, M. J. & Nelson, G. S. (1979). Immunization of mice with gamma-irradiated, intramuscularly injected schistosomula of Schistosoma mansoni. Parasitology 79, 209–22.CrossRefGoogle ScholarPubMed
Booman, M. J. J. T., Cornelissen, I. M. H. A., Berden, J. H. M., De Jong, J. & Koene, R. A. P. (1984). A comparative study of total body irradiation as a method of inducing granulocyte depletion in mice. Journal of Immunological Methods 70, 31–8.Google Scholar
Boraschi, D. & Meltzer, M. S. (1980 a). Defective tumoricidal capacity of macrophages from P/J mice: characterization of the macrophage cytotoxic defect after in vivo and in vitro activation stimuli. Journal of Immunology 125, 771–6.CrossRefGoogle Scholar
Boraschi, D. & Meltzer, M. S. (1980 b). 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
Bout, D., Joseph, M., David, J. R. & Capron, A. (1981). In vitro killing of S. mansoni schistosomula by lymphokine activated mouse macrophages. Journal of Immunology 127, 15.CrossRefGoogle ScholarPubMed
Bout, D., Joseph, M., Pontet, M., Vorng, H., Deslée, D. & Capron, A. (1986). Rat resistance to schistosomiasis: platelet-mediated cytotoxicity induced by C-reactive protein. Science 231, 153–6.CrossRefGoogle ScholarPubMed
Brecher, G. & Cronkite, E. P. (1950). Morphology and enumeration of human blood platelets. Journal of Applied Physiology 3, 365–77.CrossRefGoogle ScholarPubMed
Butterworth, A. E. (1984). Cell-mediated immunity to helminths. Advances in Parasitology 23, 143235.CrossRefGoogle 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. & Clark, S. S. (1981). Attempts to transfer the resistance of Schistosoma monsoni-infected and irradiated cercaria-immunized mice by means of parabiosis. American Journal of Tropical Medicine and Hygiene 30, 113–20.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 cercaria-immunized mice by means of autoradiographic analysis. American Journal of Tropical Medicine and Hygiene 33, 8996.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D. & Taylor, M. G. (1987). Immunity to Schistosoma mansoni in congenitally athymic, irradiated and mast cell-depleted rats. Parasitology 94, 313–26.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D., Taylor, M. G. & Andrews, B. J. (1984). Passive transfer of resistance and the site of immune-dependent elimination of the challenge infection in rats vaccinated with highly irradiated cercariae of Schistosoma mansoni. Parasitology 89, 461–82.CrossRefGoogle ScholarPubMed
James, S. L. (1986). Induction of protective immunity against Schistosoma mansoni by a nonliving vaccine. III. Correlation of resistance with induction of activated larvacidal macrophages. Journal of Immunology 136, 3872–7.CrossRefGoogle ScholarPubMed
James, S. L. & Cheever, A. W. (1985). Comparison of immune responses between high and low responder strains of mice in the concomitant immunity and vaccine models of resistance to Schistosoma mansoni. Parasitology 91, 301–15.CrossRefGoogle ScholarPubMed
James, S. L., Correa-Oliveira, R. & Leonard, E. J. (1984 a). 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., Correa-Oliveira, R., McCall, D. & Sher, A. (1985). Genetic control of host resistance to schistosomes. In Genetic Control of Host Resistance to Injection and Malignancy, pp. 523–30. New York: Alan R. Liss.Google Scholar
James, S. L., Leonard, E. J. & Meltzer, M. S. (1982 b). Macrophages as effector cells of protective immunity in murine schistosomiasis. IV. Coincidental induction of macrophage activation for extracellular killing of schistosomula and tumor cells. Cellular Immunology 74, 8696.CrossRefGoogle Scholar
James, S. L., Natovitz, P. C., Farrar, W. L. & Leonard, E. J. (1984 b). Macrophages as effector cells of protective immunity in murine schistosomiasis: macrophage activation in mice vaccinated with radiation-attenuated cercariae. Infection and Immunity 44, 569–75.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
James, S. L., Sher, A., Lazdins, J. K. & Meltzer, M. S. (1982 a). Macrophages as effector cells of protective immunity in murine schistosomiasis. II. Killing of newly transformed schistosomula in vitro by macrophages activated as a consequence of Schistosoma mansoni infection. Journal of Immunology 128, 1535–40.CrossRefGoogle ScholarPubMed
Kettman, J. & Mathews, M. C. (1975). Radioresistance of cells responsible for delayed hypersensitivity reactions in the mouse. Journal of Immunology 115, 606–8.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1986). Passive transfer with serum and IgG antibodies of irradiated cercaria induced resistance against Schistosoma mansoni in mice. Journal of Immunology 7, 2644–8.CrossRefGoogle Scholar
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, 87102.CrossRefGoogle ScholarPubMed
Miller, K. L. & 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
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
Wilson, R. A., Coulson, P. S. & Dixon, B. (1986). Migration of the 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