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Schistosoma mansoni: cellular reactions to challenge infections in the cheek pouch skin of chronically infected Chinese hamsters

Published online by Cambridge University Press:  06 April 2009

Jean E. Crabtree  and
R. A. Wilson
Jean E. Crabtree
Affiliation:
Department of Biology, University of York, York YO1 5DD
R. A. Wilson
Affiliation:
Department of Biology, University of York, York YO1 5DD
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Summary

The cellular reactions to the migration of challenge schistosomula of Schistosoma mansoni through the cheek pouch skin in Chinese hamsters immunized 20 weeks previously via the abdomen has been investigated at the ultrastructural level. The composition of the leucocytic infiltrate into the dermis and epidermis changed with time after infection. At 24 and 48 h the infiltrate was composed mainly of neutrophils and mononuclear cells. At 72 h fewer neutrophils but more eosinophils were present. The interaction of the leucocytes with the challenge schistosomula is described. Degranulation of eosinophils at the cell-parasite interface has been observed. Despite the fact that approximately 30% of 48 h schistosomula and 50% of 72 h schistosomula examined had adherent leucocytes only a few of the parasites exhibited signs of damage, consisting of tegumental vacuolation and changes in the electron opacity of the tegumental cytoplasm. There was no strong evidence of increased attrition of challenge schistosomula in the cheek pouch skin relative to the primary infection, although some dead challenge parasites were observed. It is concluded that a substantial proportion of the attrition of challenge infections in the Chinese hamster occurs at a post-dermal location.

Type
Research Article
Information
Parasitology , Volume 89 , Issue 1 , August 1984 , pp. 59 - 70
Copyright
Copyright © Cambridge University Press 1984

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References

Barker, C. F. & Billingham, R. E. (1971). The lymphatic status of hamster cheek pouch tissue in relation to its properties as a graft and as a graft site. Journal of Experimental Medicine 133, 620–39.CrossRefGoogle ScholarPubMed
Bentley, A. G., Carlisle, S. & Phillips, S. M. (1981). Ultrastructural analysis of the cellular response to Schistosoma mansoni. II. Inflammatory responses in rodent skin. American Journal of Tropical Medicine and Hygiene 30, 815–24.CrossRefGoogle ScholarPubMed
Billingham, R. E. & Silvers, W. K. (1962). Studies on pouch skin homografts in Syrian hamsters. In Ciba Foundation Symposium on Transplantation, (ed. Wostenholme, G. E. and Cameron, M. P.), pp. 90–117. London: J. & A. Churchill Ltd.CrossRefGoogle Scholar
Blum, K. & Cioli, D. (1981). Schistosoma mansoni: age dependent susceptibility to immune elimination of schistsomula artificially induced into preinfected mice. Parasite Immunology 3, 13–24.CrossRefGoogle Scholar
Capron, A., Dessiant, J. P., Capron, M. & Bazin, H. (1975). Specific IgE antibodies in immune adherence of normal macrophages to Schistosoma mansoni schistosomules. Nature, London 253, 474–5.CrossRefGoogle ScholarPubMed
Caulfield, J. P., Korman, G., Butterworth, A. E., Hogan, M. & David, J. R. (1980). The adherence of human neutrophils and eosinophils to schistosomula: evidence for membrane fusion between cells and parasites. Journal of Cell Biology 86, 46–63.CrossRefGoogle ScholarPubMed
Colley, D. G., Magalhães-Filho, A. & Coelho, R. B. (1972). Immunopathology of dermal reactions induced by Schistosoma mansoni cercariae and cercarial extract. American Journal of Tropical Medicine and Hygiene 21, 558–68.CrossRefGoogle ScholarPubMed
Crabtree, J. E. (1982). An ultrastructural study of the migrating schistosomulum of Schistosoma mansoni. D.Phil thesis, University of York.Google Scholar
Davies, C. & Goose, J. (1981). Killing of newly excysted juveniles of Fasciola hepatica in sensitized rats. Parasite Immunology 3, 81–96.CrossRefGoogle ScholarPubMed
Davies, B. & Hughes, D. L. (1964). Fascioliasis: the invasive stages of Fasciola hepatica in mammalian hosts. In Advances in Parasitology, vol. 2 (ed. Dawes, B.), pp. 97–168. London: Academic Press.Google Scholar
Dean, D. A., Cioli, D. & Bukowski, M. A. (1981). Resistance induced by normal and irradiated Schistosoma mansoni: ability of various worm stages to serve as inducers and targets in mice. American Journal of Tropical Medicine and Hygiene 30, 1026–32.CrossRefGoogle ScholarPubMed
Dessein, A., Samuelson, J. C., Butterworth, A. E., Hogan, M., Sherry, B. A., Vadas, M. A. & David, J. R. (1981). Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent attack by schistosomula cultured in medium free of macromolecules. Parasitology 82, 357–74.CrossRefGoogle ScholarPubMed
Glauert, A. M., Butterworth, A. E., Sturrock, R. F. & Houba, V. (1978). The mechanism of antibody-dependent, eosinophil-mediated damage to schistosomula of Schistosoma mansoni in vitro: a study by phase contrast and electron microscopy. Journal of Cell Science 34, 173–92.CrossRefGoogle Scholar
Incani, R. N. (1981). Immunity to Schistosoma mansoni: in vitro and in vivo studies on the role of the neutrophil in schistosomula killing. Ph.D. thesis, University of Brunel.Google Scholar
Incani, R. N. & McLean, D. J. (1983). Ultrastructural observations on the in vitro interaction of rat neutrophils with schistosomula of Schistosoma mansoni in the presence of antibody and/or complement. Parasitology 86, 345–57.CrossRefGoogle ScholarPubMed
James, S. L. & Sher, A. (1980). Immune mechanisms that stimulate mouse leukocyte migration in response to schistosomula of Schistosoma mansoni. Journal of Immunology 124, 1837–44.CrossRefGoogle ScholarPubMed
Jensen, D. V., Stirewalt, M. A. & Walters, M. (1965). Growth of Schistosoma mansoni cercariae under dialysis membranes in Rose multipurpose chambers. Experimental Parasitology 17, 15–23.Google ScholarPubMed
Kassis, A. I., Aikawa, M. & Mahmoud, A. A. F. (1979). Mouse antibody-dependent eosinophil and macrophage adherence and damage to schistosomula of Schistosoma mansoni. Journal of Immunology 122, 398–405.CrossRefGoogle ScholarPubMed
Kay, A. B., Stechschulte, D. J. & Austen, K. F. (1971). An eosinophil leucocyte chemotactic factor of anaphylaxis. Journal of Experimental Medicine 133, 602–19.CrossRefGoogle ScholarPubMed
Lichtenberg, F. von, & Byram, J. E. (1980). Pulmonary cell reactions in resistance to Schistosoma mansoni. In The Host-Invader Interplay, vol. 2 (ed. van den Bossche, H.), pp. 405–416. Amsterdam: Elsevier/North Holland.Google Scholar
Lichtenberg, F. von & Ritchie, L. S. (1961). Cellular resistance against schistosomula of Schistosoma mansoni in Macaca mulatta monkeys following prolonged infections. American Journal of Tropical Medicine and Hygiene 10, 859–69.CrossRefGoogle Scholar
Lichtenberg, F. von, Sher, A., Gibbons, N. & Doughty, B. L. (1976). Eosinophil-enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni. American Journal of Pathology 84, 479–500.Google ScholarPubMed
Lin, S. S. & Sadun, E. H. (1959). Studies on the host-parasite relationships to Schistosoma japonicum. V. Reactions in the skin, lungs and liver of normal and immune animals following injection with S. japonicum. Journal of Parasitology 45, 549–56.CrossRefGoogle Scholar
McLaren, D. J. (1981). Schistosoma mansoni: the parasite surface in relation to host immunity. In Tropical Medicine Research Studies, vol. 1, (ed. Brown, K. N.), Chichester: Research Studies Press/John Wiley Press.Google Scholar
McLaren, D. J., Mackenzie, C. D. & Ramalho-Pinto, F. J. (1977). Ultrastructural observations on the in vitro interaction between rat eosinophils and some parasitic helminths (Schistosoma mansoni, Trichinella spiralis and Nippostrongylus brasiliensis). Clinical and Experimental Immunology 30, 105–18.Google ScholarPubMed
McLaren, D. J., McKean, J. R., Olsson, I., Venge, P. & Kay, A. B. (1981). Morphological studies in the killing of schistosomula of Schistosoma mansoni by human eosinophil and neutrophil cationic proteins in vitro. Parasite Immunology 3, 359–73.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Ramalho-Pinto, F. J. (1979). Eosinophil-mediated killing of schistosomula of Schistosoma mansoni in vitro: synergistic effect of antibody and complement. Journal of Immunology 123, 1431–8.CrossRefGoogle ScholarPubMed
McLaren, D. J., Ramalho-Pinto, F. J. & Smithers, S. R. (1978). Ultrastructural evidence for complement and antibody-dependent damage to schistosomula of Schistosoma mansoni by rat eosinophils in vitro. Parasitology 77, 313–24.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
Miller, P. & Wilson, R. A. (1978). Migration of the schistosomula of Schistosoma mansoni from skin to lungs. Parasitology 77, 281–302.CrossRefGoogle ScholarPubMed
Perez, H. A. & Smithers, S. R. (1977). Schistosoma mansoni in the rat: the adherence of macrophages to schistosomula in vitro after sensitization with immune serum. International Journal for Parasitology 7, 315–20.CrossRefGoogle ScholarPubMed
Ramalho-Pinto, F. J., McLaren, D. J. & Smithers, S. R. (1978). Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. Journal of Experimental Medicine 147, 147–56.CrossRefGoogle ScholarPubMed
Savage, A. M. & Colley, D. G. (1980). The eosinophil in the inflammatory response to cercarial challenge of sensitized and chronically infected CBA/J mice. American Journal of Tropical Medicine, and Hygiene, 29, 1268–78.CrossRefGoogle ScholarPubMed
Sher, A., Mackenzie, P. & Smithers, S. R. (1974). Decreased recovery of invading parasites from the lungs as a parameter of acquired immunity to schistosomiasis in the laboratory mouse. Journal of Infectious Diseases 130, 626–33.CrossRefGoogle Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adults. Parasitology 55, 695–700.CrossRefGoogle Scholar
Smithers, S. R. & Gammage, K. (1980). The recovery of schistosomula of Schistosoma mansoni 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
Wilson, R. A. & Lawson, J. R. (1980). An examination of the skin phase of schistosome migration using a hamster cheek pouch preparation. Parasitology 80, 257–66.CrossRefGoogle ScholarPubMed