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Histological examination of the cellular reactions around schistosomula of Schistosoma mansoni in the lungs of sublethally irradiated and unirradiated, immune and control rats

Published online by Cambridge University Press:  06 April 2009

Dario A. A. Vignali ,
S. N. Klaus ,
Q. D. Bickle  and
M. G. Taylor
Dario A. A. Vignali
Affiliation:
Department of Medical Helminthology and 1Wolfson Tropical Pathology Unit, London School of Hygiene and Tropical Medicine, Keppel St, London WC1E 7HT
S. N. Klaus*
Affiliation:
Department of Medical Helminthology and 1Wolfson Tropical Pathology Unit, London School of Hygiene and Tropical Medicine, Keppel St, London WC1E 7HT
Q. D. Bickle
Affiliation:
Department of Medical Helminthology and 1Wolfson Tropical Pathology Unit, London School of Hygiene and Tropical Medicine, Keppel St, London WC1E 7HT
M. G. Taylor*
Affiliation:
Department of Medical Helminthology and 1Wolfson Tropical Pathology Unit, London School of Hygiene and Tropical Medicine, Keppel St, London WC1E 7HT
*
*Previous address: Department of Dermatology, Yale University Medical School, 333 Cedar St, New Haven, CT 06510, USA. Current address: Department of Dermatology, Hadassah Hospital, P.O. Box 12000, Jerusalem, Israel.
†Reprint requests: Dr M. G. Taylor.
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Summary

Histopathological data on the cellular reactions (foci) around Schistosoma mansoni schistosomula in the lungs of both irradiated (750 rad) and unirradiated, passively immunized and normal rats were consistent with the idea that a significant proportion of immune-mediated attrition in passively immunized rats occurs in the lungs. In unirradiated rats, immune serum elicited an enhanced (i.e. larger) and accelerated (i.e. more rapidly developing) inflammatory cellular infiltration around lung-stage parasites when administered 5 days post-infection, when the parasites were already in the lungs. This demonstrated the antigenicity of lung-stage schistosomula and their potential as targets for immune attack. In irradiated rats, innate immunity was decreased as judged by an increase in the number of worms recovered by portal perfusion, and was accompanied by an overall decreased percentage of trapped parasites compared with unirradiated controls, suggesting that trapping in the lungs is involved in innate, as well as acquired immunity. In contrast to the results in unirradiated rats, passive transfer of immune serum into irradiated recipients did not result in larger lung foci than in the NRS-recipients. However, there was evidence of an accelerated response resulting in an essentially similar ratio of trapped parasites (VRS- compared with NRS-recipients) in irradiated rats, as compared with unirradiated rats, reflecting the similar levels of resistance manifested in both groups of rats. This also lent credence to the notion that it was the speed of immune recognition of the migrating schistosomula and the establishment of trapping foci that were of greater importance rather than the size of the enveloping granulomata. Investigations into the cellular composition of the foci surrounding trapped parasites in unirradiated rats revealed a predominance of mononuclear cells, with equal proportions of lymphocytes and macrophages. Eosinophils represented less than 3% of the cellular composition of the foci and were typically distant from the parasites themselves, arguing against their role in specific immunity in this model. Irradiation of recipient rats resulted in a corresponding increase in the percentage of macrophages in lung foci.

Keywords

Schistosoma mansoniirradiationcellular reactionshistopathology.
Type
Research Article
Information
Parasitology , Volume 98 , Issue 1 , February 1989 , pp. 57 - 65
Copyright
Copyright © Cambridge University Press 1989

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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, 199–203.CrossRefGoogle Scholar
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 gammairradiated, intramuscularly injected schistosomula of Schistosoma mansoni. Parasitology 79, 209–22.CrossRefGoogle 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
Capron, M., Nogueira-Queiroz, J. A., Papin, J. P. & Capron, A. (1984). Interactions between eosinophils and antibodies: in vivo protective role against rat schistosomiasis. Cellular Immunology 83, 60–72.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
Ford, M. J. (1985). Studies on the mechanisms of induction and expression of acquired resistance to Schistosoma mansoni. Ph.D. thesis, London School of Hygiene and Tropical Medicine, University of London.Google Scholar
Ford, M. J., Bickle, Q. D., Taylor, M. G. & Andrews, B. J. (1984 a). 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
Ford, M. J., Bickle, Q. D. & Taylor, M. G. (1984 b). Immunization of rats against Schistosoma mansoni using irradiated cercariae, lung schistosomula and liver-stage worms. Parasitology 89, 327–44.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D. & Taylor, M. G. (1987 a). Immunity to Schistosoma mansoni in congenitally athymic, irradiated and mast cell depleted rats. Parasitology 94, 313–26.CrossRefGoogle ScholarPubMed
Ford, M. J., Dissous, C., Pierce, R. J., Taylor, M. G., Bickle, Q. D. & Capron, A. (1987 b). The isotypes of antibody responsible for the ‘late’ passive transfer of immunity in rats vaccinated with highly irradiated cercariae. Parasitology 94, 509–22.CrossRefGoogle ScholarPubMed
Knopf, P. M., Cioli, D., Mangold, B. L. & Dean, D. A. (1986). Migration of Schistosoma mansoni in normal and passively immunized laboratory rats. American Journal of Tropical Medicine and Hygiene 35, 1173–84.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Knopf, P. M. (1981). Host protective immune responses to Schistosoma mansoni infections in the rat: kinetics of hyperimmune serum-dependent elimination of schistosomes in passive transfer assay. Parasitology 83, 559–74.CrossRefGoogle Scholar
McLaren, D. J. (1980). Schistosoma mansoni: the parasite surface in relation to immunity. In Tropical Medicine Research Studies, vol. 1 (ed. Brown, K. N.), pp. 1–299. Chichester: Research Studies Press.Google Scholar
McLaren, D. J. & Smithers, S. R. (1985). Schistosoma mansoni: challenge attrition during the lung phase of migration in vaccinated and serum-protected rats. Experimental Parasitology 60, 1–9.CrossRefGoogle ScholarPubMed
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
Moser, G., Wassom, D. L. & Sher, A. (1980). Studies of the antibody-dependent killing of schistosomula of Schistosoma mansoni employing haptenic target antigens. I. Evidence that the loss of susceptibility to immune damage undergone by developing schistosomula involves a change unrelated to the masking of parasite antigens by host molecules. Journal of Experimental Medicine 152, 41–53.CrossRefGoogle Scholar
Oshman, R., Knopf, P. M., Von Lichtenberg, F. & Byram, J. E. (1986). Effects of protective immune serum on the yields of parasites and pulmonary cell reactions in schistosome-infected rats. American Journal of Tropical Medicine and Hygiene 35, 523–30.CrossRefGoogle ScholarPubMed
Phillips, S. M., Reid, W. A., Bruce, J. I., Hedlund, K., Colvin, R. C., Campbell, R., Diggs, C. L. & Sadun, E. H. (1975). The cellular and humoral immune response to Schistosoma mansoni infections in inbred rats. I. Mechanisms after initial exposure. Cellular Immunology 19, 99–116.CrossRefGoogle Scholar
Sher, A., James, S. J., Simpson, L., Lazdins, J. K. & Meltzer, M. S. (1982). Macrophages as effector cells of protective immunity in murine schistosomiasis. III. Loss of susceptibility to macrophage-mediated killing during maturation of S. mansoni schistosomula from the skin to the lung stage. Journal of Immunology 128, 1876–9.CrossRefGoogle Scholar
Vignali, D. A. A., Bickle, Q. D., Taylor, M. G., Tennent, G. & Pepys, M. B. (1988 a). Comparison of the role of complement in immunity to Schistosoma mansoni in rats and mice. Immunology 63, 55–61.Google ScholarPubMed
Vignali, D. A. A., Bickle, Q. D. & Taylor, M. G. (1988 b). 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