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Responses to larval Taenia taeniaeformis in mice with severe combined immunodeficiency (scid)

Published online by Cambridge University Press:  06 April 2009

K. Ishiwata
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Hokkaido University, Sapporo 060, Japan
Y. Oku
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Hokkaido University, Sapporo 060, Japan
M. Ito
Affiliation:
Central Institute for Experimental Animals, 1430 Nogawa, Miyamae-ku, Kawasaki-shi, Kanagawa 216, Japan
M. Kamiya
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Hokkaido University, Sapporo 060, Japan

Summary

Responses to Taenia taeniaeformis infection were studied in mice with severe combined immunodeficiency (scid), which lack functional T and B lymphocytes. In the early phase of infection, accumulation of polymorphonuclear leucocytes (PML) occurred around the larvae in the liver of scid mice and their immunocompetent counterparts, C.B-17, (a BALB/c strain, genetically resistant to this parasite). PML accumulation continued until encapsulation of developing larvae by fibroblasts (14 days p.i.), and subsequent fibrosis resulted in granuloma formation. No infiltration of eosinophils or macrophages around larvae was observed in scid mice prior to granuloma formation, while in C.B-17 mice infiltration was observed as early as 5 days p.i., when specific antibodies could not be detected in the circulation. Most larvae were destroyed by 14 days p.i. in C.B-17 mice. In scid mice the larvae survived but the host capsules (cysts) were thin and most contained blood at 42 days p.i. In these cysts, inflammatory cells were observed on the larval surface and in invaded parasite tissue. Hepatocyte coagulation necrosis adjacent to larvae was commonly found in C.B-17 mice by 5 days p.i., while it did not occur in scid mice throughout these experiments. These results suggest that in host responses to larval T. taeniaeformis, PML accumulation and encapsulation by fibrosis are T and B cell independent, while eosinophil and macrophage infiltration, as well as resistance to infection, are T and/or B cell dependent. Additionally, there may be an association between host cell necrosis around larvae and T and/or B cell responses.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Boros, D. L. (1978). Granulomatous inflammations. Progress in Allergy 24, 183267.Google ScholarPubMed
Bortoletti, G. & Ferretti, G. (1985). Morphological studies on the early development of Taenia taeniaeformis larvae in susceptible mice. International Journal for Parasitology 15, 365–75.Google Scholar
Bortoletti, G., Conchedda, M. & Ferretti, G. (1985). Damage and early destruction of Taenia taeniaeformis larvae in resistant hosts, and anomalous development in susceptible hosts: a light microscopic and ultrastructural study. International Journal for Parasitology 15, 377–84.CrossRefGoogle ScholarPubMed
Bosma, G. C., Custer, R. P. & Bosma, M. J. (1983). A severe combined immunodeficiency mutation in the mouse. Nature, London 301, 527–30.Google Scholar
Bøgh, H. O., Lightowlers, M. W., Sullivan, N. D., Mitchell, G. F. & Rickard, M. D. (1990). Stage–specific immunity to Taenia taeniaeformis infection in mice. A histological study of the course of infection in mice vaccinated with either oncosphere or metacestode antigens. Parasite Immunology 12, 153–62.Google Scholar
Byram, J. E. & Von Lichtenberg, F. (1977). Altered schistosome granuloma formation in nude mice. American Journal of Tropical Medicine and Hygiene 26, 944–56.Google Scholar
Cheever, A. W., Byram, J. E. & Von Lichtenberg, F. (1985). Immunopathology of Schistosoma japonicum infection in athymic mice. Parasite Immunology 7, 387–98.Google Scholar
Conder, G. A., Marchiondo, A. A., Williams, J. F. & Andersen, F. L. (1983). Ultrastructural characterization of serum-induced changes in the tegument of Taenia taeniaeformis. Journal of Parasitology 69, 838–45.Google Scholar
Cook, R. W., Trapp, A. L. & Williams, J. F. (1981). Pathology of Taenia taeniaeformis infection in the rat: hepatic, lymph node and thymic changes. Journal of Comparative Pathology 91, 219–26.CrossRefGoogle ScholarPubMed
Custer, R. P., Bosma, G. C. & Bosma, M. J. (1985). Severe combined immunodeficiency (SCID) in the mouse pathology, reconstitution, neoplasms. American Journal of Pathology 120, 464–77.Google Scholar
Czitrom, A. A., Edwards, S., Phillips, R. A., Bosma, M. J., Marrack, P. & Kappler, J. W. (1985). The function of antigen-presenting cells in mice with severe combined immunodeficiency. Journal of Immunology 134, 2276–80.CrossRefGoogle ScholarPubMed
Davis, S. W. & Hammerberg, B. (1988). Activation of the alternative pathway of complement by larval Taenia taeniaeformis in resistant and susceptible strains of mice. International Journal for Parasitology 18, 591–7.CrossRefGoogle ScholarPubMed
Davis, S. W. & Hammerberg, B. (1990). Effect of depletion of L3T4+ cells on resistance to early primary infection of mice with Taenia taeniaeformis. International Journal for Parasitology 20, 595601.Google Scholar
Deschryver-Kecskemeti, K., Bancroft, G. J., Bosma, G. C., Bosma, M. J. & Unanue, E. R. (1988). Pathology of Listeria infection in murine severe combined immunodeficiency. A study by immunohistochemistry and electron microscopy. Laboratory Investigation 58, 698705.Google ScholarPubMed
Dorshkind, K., Keller, G. M., Phillips, R. A., Miller, R. G., Bosma, G. C., O'Toole, M. & Bosma, M. J. (1984). Functional status of cells from lymphoid and myeloid tissues in mice with severe combined immunodeficiency disease. Journal of Immunology 132, 1804–8.CrossRefGoogle ScholarPubMed
Dorshkind, K., Pollack, S. B., Bosma, M. J. & Phillips, R. A. (1985). Natural killer (NK) cells are present in mice with severe combined immunodeficiency (scid). Journal of Immunology 134, 3798–801.Google Scholar
Engelkirk, P. G. & Williams, J. F. (1982). Taenia taeniaeformis (Cestoda) in the rat: Ultrastructure of the host–parasite interface on days 1 to 7 post-infection. Journal of Parasitology 68, 620–33.CrossRefGoogle Scholar
Kamiya, H., Kamiya, M., Ohbayashi, M. & Nomura, T. (1980). Studies on the host resistance to infection with Echinococcus multilocularis. I. Difference of susceptibility of various rodents, especially of congenitally athymic nude mice. Japanese Journal of Parasitology 29, 87100. (In Japanese.)Google Scholar
Letonja, T. & Hammerberg, B. (1983). Third component of complement, immunoglobulin deposition, and leucocyte attachment related to surface sulfate on larval Taenia taeniaeformis. Journal of Parasitology 69, 637–44.Google Scholar
Letonja, T. & Hammerberg, C. (1987). Taenia taeniaeformis: early inflammatory response around developing metacestodes in the liver of resistant and susceptible mice II. Histochemistry and cytochemistry. Journal of Parasitology 73, 971–9.CrossRefGoogle ScholarPubMed
Letonja, T., Rikihisa, Y. & Hammerberg, C. (1984). Differential cellular response of resistant and susceptible rodents to the early stages of infection of Taenia taeniaeformis. International Journal for Parasitology 14, 551–8.CrossRefGoogle Scholar
Letonja, T., Hammerberg, C., Davis, S. & Hammerberg, B. (1988). Taenia taeniaeformis: cellular reconstruction of athymic mice and role of L3T4+ helper T lymphocytes in the early infection. Journal of Parasitology 74, 985–92.Google Scholar
Mahanty, S., Greenfield, R. A., Joyce, W. A. & Kincade, P. W. (1988). Inoculation candidiasis in a murine model of severe combined immunodeficiency syndrome. Infection and Immunity 56, 3162–6.Google Scholar
McCune, J. M., Namikawa, R., Kaneshima, H., Shultz, L. D., Lieberman, M. & Weissman, I. L. (1988). The SCID-hu mouse: murine model for the analysis of human hematolymphoid differentiation and function. Science 241, 1632–9.CrossRefGoogle ScholarPubMed
Mitchell, G. F. (1982). Genetic variation in resistance of mice to Taenia taeniaeformis: analysis of host-protective immunity and immune evasion. In Cysticercosis: Present State of Knowledge and Perspectives, (ed. Flisser, A., Willms, K., Laclette, J. P., Larralde, C., Ridaura, C. & Beltràn, F.), pp. 575584. London: Academic Press.Google Scholar
Mitchell, G. F. & Holmes, M. C. (1982). Nude mice in the study of susceptibility and responses to infection with metazoan and protozoan parasites. In Proceedings of the Third International Workshop on Nude Mice, Vol. 1 (ed. Reed, N. D.), pp. 19. New York: Gustav Fischer New York, Inc.Google Scholar
Mitchell, G. F., Goding, J. W. & Rickard, M. D. (1977). Studies on immune responses to larval cestodes in mice. Increased susceptibility of certain mouse strains and hypothymic mice to Taenia taeniaeformis and analysis of passive transfer of resistance with serum. Australian Journal of Experimental Biology and Medical Science 55, 165–86.CrossRefGoogle ScholarPubMed
Phillips, S. M., Diconza, J. J., Gold, J. A. & Reid, W. A. (1977). Schistosomiasis in the congenitally athymic (nude) mouse I. Thymic dependency of eosinophilia, granuloma formation, and host morbidity. Journal of Immunology 118, 594–9.Google Scholar
Pollaco, S., Nicholas, W. L., Mitchell, G. F. & Stewart, A. C. (1978). T-cell dependent collagenous encapsulating response in the mouse liver to Mesocestoides corti (Cestoda). International Journal for Parasitology 8, 457–62.Google Scholar
Rajasekariah, G. R., Rickard, M. D., Mitchell, G. F. & Anders, R. F. (1982). Immunization of mice against Taenia taeniaeformis using solubilized oncospheral antigens. International Journal for Parasitology 12, 111–16.Google Scholar
Rickard, M. D. (1983). Immunity. In Biology of the Eucestoda, Vol. 2 (ed. Arme, C. & Pappas, P. W.), pp. 539–79. London: Academic Press.Google Scholar
Rickard, M. D. & Williams, J. F. (1982). Hydatidosis/cysticercosis: immune mechanisms and immunization against infection. In Advances in Parasitology, Vol. 21 (ed. Baker, J. R. & Muller, R.), pp. 229–96. London: Academic Press.Google Scholar
Voller, A., Bidwell, D. E. & Bartlett, A. (1976). Enzyme immunoassays in diagnostic medicine. Theory and practice. Bulletin of the World Health Organization 53, 5565.Google Scholar
Warren, K. S. (1980). The cell biology of granulomas (aggregates of inflammatory cells) with a note on giant cells. In The Cell Biology of Inflammation, (ed. Weissmann, G.), pp. 543–57. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar