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The role of mononuclear-cell recruitment to the lungs in the development and expression of immunity to Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

E. C. Ratcliffe
Affiliation:
Department of Biology, University of York, York Y01 5DD
R. A. Wilson
Affiliation:
Department of Biology, University of York, York Y01 5DD

Summary

The role of pulmonary cellular responses in the induction and expression of immunity to Schistosoma mansoni has been evaluated. From experiments in which mice were challenged at intervals after vaccination, we conclude that the resistance mechanism operating in the lungs develops between days 11 and 20. Injection of 51Cr-labelled splenocytes revealed that mononuclear cell recruitment to the lungs, stimulated by the arrival of attenuated schistosomula, intensified progressively between days 10 and 16 post-vaccination. The increased cellularity was reflected in a 19·5% augmentation in the wet-weight index (WW). The period of enhanced cell recruitment therefore coincided with the build-up of resistance. By day 22 post-vaccination infiltration had declined, whilst WW remained elevated. This indicates the persistence of recruited cells, which include schistosome-reactive T lymphocytes, in the lungs. We were unable to demonstrate augmented recruitment of 51Cr-labelled cells after challenge of vaccinated mice, but WW rose slightly, peaking on day 12. Although clearly of a lower order than the primary response, the secondary response was more rapid, implying the existence of immunological memory. These results accord with the concept that schistosome-reactive T lymphocytes recruited after vaccination ‘arm’ the lungs against the arrival of challenge parasites.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Aitken, R., Coulson, P. S., Dixon, B. & Wilson, R. A. (1987). Radiation-resistant acquired immunity of vaccinated mice to Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 37, 570–7.CrossRefGoogle ScholarPubMed
Aitken, R., Coulson, P. S. & Wilson, R. A. (1988). Pulmonary leucocytic responses in vaccinated mice are linked to acquired immunity against Schistosoma mansoni. Journal of Immunology 140, 3573–9.CrossRefGoogle ScholarPubMed
Blecha, F. & Topliff, D. (1984). Lung delayed type hypersensitivity in stressed mice. Canadian Journal of Comparative Medicine 48, 211–14.Google ScholarPubMed
Coulson, P. S. & Wilson, R. A. (1988). An examination of the mechanisms of pulmonary phase resistance to Schistosoma mansoni in vaccinated mice. American Journal of Tropical Medicine and Hygiene 38, 529–39.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
Fong, T. A. T. & Mosmann, T. R. (1989). The role of interferon-gamma in delayed-type hypersensitivity mediated by TH1 clones. Journal of Immunology 143, 2887–93.CrossRefGoogle ScholarPubMed
Hudson, L. & Hay, F. C. (1989). Practical Immunology, 3rd Edn.Oxford: Blackwell Scientific Publications.Google Scholar
James, S. L., Correa-Oliveira, R. & Leonard, E. (1984). Defective vaccine induced immunity to Schistosoma mansoni infection in P strain mice. II. Analysis of cellular responses. Journal of Immunology 133, 1587–93.CrossRefGoogle Scholar
James, S. L., De Blois, L. A., Al Zamel, F., Glaven, J. & Langhorne, J. (1986). Defective vaccine induced immunity to Schistosoma mansoni in P strain mice. III. Specificity of the associated defect in cell mediated immunity. Journal of Immunology 137, 3957–67.Google Scholar
Kambara, T. & Wilson, R. A. (1990). In situ pulmonary responses of T cell and macrophage sub-populations to a challenge infection in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Journal of Parasitology 76, 365–72.CrossRefGoogle Scholar
Liew, F. Y. (1984). Lymphocyte subsets involved in delayed-type hypersensitivity. Advances in Inflammation Research 7, 135–47.Google Scholar
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
Marchal, G. & Milon, G. (1984). Numeration of DTH mediating T lymphocytes in mice under optimal titration conditions. Annals of Immunology (Institut Pasteur) 135, 353–64.Google Scholar
Marchal, G., Milon, G. & Hurtrel, B. (1979). High radiosensitivity of induction in contrast to radioresistance of expression of cells mediating delayed-type hypersensitivity during response to sheep red blood cells in mice. Immunology 37, 273–8.Google 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, 87102.CrossRefGoogle ScholarPubMed
Mastin, A. J., Bickle, Q. D. & Wilson, R. A. (1985). An ultrastructural examination of irradiated schistosomula of Schistosoma mansoni during their extended stay in the lungs. Parasitology 91, 101–10.CrossRefGoogle ScholarPubMed
Menson, E. N., Coulson, P. S. & Wilson, R. A. (1989). Schistosoma mansoni: circulating and pulmonary leucocyte responses related to the induction of protective immunity in mice by irradiated parasites. Parasitology 98, 4355.CrossRefGoogle Scholar
Menson, E. N. & Wilson, R. A. (1989). Lung-phase immunity to Schistosoma mansoni: flow cytometric analysis of macrophage activation states in vaccinated mice. Journal of Immunology 143, 2342–8.CrossRefGoogle ScholarPubMed
Ratcliffe, E. C. & Wilson, R. A. (1991). The magnitude and kinetics of delayed-type hypersensitivity responses in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasitology 103, 6575.CrossRefGoogle ScholarPubMed
Schwartz, A., Askenase, P. A. & Gershon, R. K. (1977). The effect of locally injected vasoactive amines on the elicitation of delayed-type hypersensitivity. Journal of Immunology 118, 159–65.CrossRefGoogle 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 immunity in mice. Parasitology 96, 4962.CrossRefGoogle ScholarPubMed
Von Lichtenberg, F., Correa-Oliveira, R. & Sher, A. (1985). The fate of challenge schistosomula in the murine anti-schistosome vaccine model. American Journal of Tropical Medicine and Hygiene 34, 96106.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. 115146. London: Academic Press.Google Scholar
Wilson, R. A. & Coulson, P. S. (1989). Lung-phase immunity to schistosomes: a new perspective on an old problem. Parasitology Today 5, 274–8.CrossRefGoogle Scholar
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 site and timing of parasite death. Parasitology 92, 101–16.CrossRefGoogle ScholarPubMed
Zarkower, A., Scheuchenzuber, W. J. & Ferguson, F. G. (1981). Use of 51Cr-labelled mononuclear cells for measuring the cellular immune response in mouse lungs. Infection and Immunity 31, 712–15.CrossRefGoogle Scholar