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Mice infected with the larvae of Taenia crassiceps exhibit a Th2-like immune response with concomitant anergy and downregulation of Th1-associated phenomena

Published online by Cambridge University Press:  06 April 2009

O. F. Villa  and
R. E. Kuhn
O. F. Villa
Affiliation:
Department of Internal Medicine, Saint Agnes Hospital of Baltimore, 900 Caton Avenue, Baltimore, MD 21229-5299, USA
R. E. Kuhn*
Affiliation:
Wake Forest University, Department of Biology, P.O. Box 7325, Winston-Salem, N.C. 27109, USA
*
* Corresponding author.
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Summary

Infection of intermediate hosts with eggs of taeniid parasites results in a larval infestation known as cysticercosis. A number of studies have indicated that cysticercosis is associated with immunosuppression, although little is known about the mechanisms involved. In the present study, mice infected with the larvae of Taenia crassiceps were found to exhibit a pronounced anergy, which preferentially affected T-cells located anatomically close to the parasite. This anergy was linked to late events in the T cell activation pathway; that is, stimulation through the T cell receptor(TCR)/CD complex by Concanavalin-A, or plate-bound monoclonal antibodies (mAb) to TCRαβ or CD3ε, or combinations of phorbol ester and ionomycin (all of which can bypass early membrane-related events), failed to fully activate T lymphocytes. The relative proximity of T cells to the parasite was directly related to upregulation of IL-4 and downregulation of IL-2 production. In addition, the profiles of parasite-specific Abs showed an exclusive increase of serum IgG1 during infection. Taken together, the data suggest that infection of mice with larvae of T. crassiceps alters the balance of CD4+ Th cells by upregulating Th2 and downregulating Th1 cells located in close proximity to the parasite.

Keywords

experimental cysticercosisTaenia crassicepsimmunosuppressionTh cells
Type
Research Article
Information
Parasitology , Volume 112 , Issue 6 , June 1996 , pp. 561 - 570
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Abraham, K. M. & Teale, J. M. (1987). Isotype restriction during infection of mice with the cestode Mesocestoides corti, role of immune suppression. Journal of Immunology 138, 1699–704.Google Scholar
Altman, A., Coggeshall, K. M. & Mustelin, T. (1990).Molecular events mediating T-cell activation. In Advances in Immunology, Vol. 48 (ed. Dickson, F. J.), pp. 227–360. San Diego, CA: Academic Press.Google Scholar
Ben-Sasson, S. Z., Legros, G., Conrad, D. H., Finkelman, F. D. & Paul, W. E. (1990). IL-4 production by T cells from naive donors. IL-2 is required for IL-4 production. Journal of Immunology 145, 1127–36.Google Scholar
Bogdan, C., Vodovotz, Y. & Nathan, C. (1991). Macrophage deactivation by interleukin 10. Journal of Experimental Medicine 174, 1549–55.Google Scholar
Botero, D. & Castaño, S. (1982). Treatment of cysticercosis with praziquantel in Colombia. American Journal of Tropical Medicine and Hygiene 31, 810–21.Google Scholar
Burger, C. J., Rikihisa, Y. & Lin, Y. C. (1986). Taenia taeniaeformis: inhibition of mitogen induced proliferation and interleukin-2 production in rat splenocytes by larval in vitro product. Experimental Parasitology 62, 216–22.Google Scholar
Chilson, O. P. & Kelly-Chilson, A. E. (1989). Mitogenic lectins bind to the antigen receptor on human lymphocytes. European Journal of Immunology 19, 389–96.Google Scholar
Culbreth, K. L., Esch, G. W. & Kuhn, R. E. (1972). Growth and development of larval Taenia crassiceps (Cestoda) III. The relationship between larval biomass and the uptake and incorporation of 14C-leucine. Experimental Parasitology 32, 272–81.Google Scholar
De Aluja, A. S. & Vargas, G. (1988). The histopathology of porcine cysticercosis. Veterinary Parasitology 28, 65–77.Google Scholar
De Aluja, A. S., Gonzáles, D., Rodríguez-Carbajal, J. & Flisser, A. (1989). Histological description of tomographic images of Taenia solium cysticerci in pig brains. Clinical Imaging 13, 292–8.Google Scholar
De Waal, Malefyt R., Hannen, J., Spits, H., Roncarolo, M. G., Te-Velde, A., Figdor, C. G., Johnson, K., Kastelein, R., Yssel, H. & De Vries, J. E. (1992).Interleukin 10 (IL–10) and viral IL-10 strongly reduce antigen-specific human T-cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. Journal of Experimental Medicine 174, 915–24.Google Scholar
Dison, H. & Lipscomb, F. (1961). Cysticercosis: An analysis and follow up of 450 cases. Medical Research Council Special Report 299, 1–58.Google Scholar
Estrada, J. J. & Kuhn, R. E. (1985). Immunochemical detection of antigens of Taenia solium and anti-larval antibodies in the cerebrospinal fluid of patients with neurocysticercosis. Journal of Neurological Sciences 71, 39–48.Google Scholar
Finkelman, F. D., Holmes, J., Katona, I. M., Urban, J. F., Beckman, M. P., Park, L. S., Schooley, K. A., Coffman, R. L., Mosmann, T. R. & Paul, W. E. (1990).Lymphokine control of in vivo immunoglobulin isotype selection. Annual Reviews of Immunology 8, 303–33.Google Scholar
Fiorentino, D. F., Bond, M. W. & Mosmann, T. R. (1989).Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. Journal of Experimental Medicine 170, 2081–95.Google Scholar
Fiorentino, D. F., Zlotnik, A., Mosmann, T. R., Howard, M. & O'Garra, A. (1991). IL-10 inhibits cytokine production by activated macrophages. Journal of Immunology 147, 3815–22.Google Scholar
Flisser, A., Woodhouse, E. & Larralde, C. (1980). Human cysticercosis: antigens, antibodies, and non-responders. Clinical and Experimental Immunology 39, 27–37.Google Scholar
Flisser, A. I., Madrazo, I., Gonzalez, D., Sandoval, M., Rodriguez-Carbajal, J. & De-Dios, J. (1988). Comparative analysis of human and porcine neurocysticercosis by computed tomography. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 739–42.Google Scholar
Freeman, R. (1962). Studies on the biology of Taenia crassiceps (Zender 1980) Rudolphi, 1810 (Cestoda). Canada Journal of Zoology 40, 969–90.Google Scholar
Gazzinelli, R. T., Oswald, I. P., James, S. L. & Sher, A. (1992). IL-10 inhibits parasite killing and nitrogen oxide production by INF-γ activated macrophages. Journal of Immunology 148, 1792–6.CrossRefGoogle Scholar
Gillis, S., Ferm, M. M., Ou, W. & Smith, K. A. (1978). T-cell growth factor: Parameters of production and a quantitative microassay for activity. Journal of Immunology 120, 2027–32.Google Scholar
Good, A. H. & Miller, K. L. (1976). Depression of immune responses to sheep erythrocytes in mice infected with Taenia crassiceps larvae. Infection and Immunity 14, 449–56.CrossRefGoogle ScholarPubMed
Hammerberg, B. & Williams, J. F. (1978 a). Interaction between Taenia taeniaeformis and the complement system. Journal of Immunology 120, 1033–7.Google Scholar
Hammerberg, B. & Williams, J. F. (1978 b). Physicochemical characterization of complement-interacting factors from Taenia taeniaeformis. Journal of Immunology 120, 1039–45.Google Scholar
Harlow, E. & Lane, D. (1988). Immunoaffinity purification. In Antibodies: a Laboratory Manual (ed. Harlow, E. & Lane, D.), p. 51. NY: Cold Spring Harbor Laboratory.Google Scholar
Hashimoto, S., Takahashi, Y., Tomita, Y., Hayama, T., Sawada, S., Horie, T., McCombs, C. C. & Michalski, J. P. (1991). Mechanism of calcium ionophore and phorbol ester-induced T-cell activation. Scandinavian Journal of Immunology 33, 393–403.Google Scholar
Hustead, S. T. & Williams, J. F. (1977). Permeability studies on taeniid metacestodes: I. Uptake of proteins by larval stages of Taenia taeniformis, T. crassiceps and Echinococcus granulosos. Journal of Parasitology 63, 314–21.Google Scholar
Jenkins, M. K., Chen, C., Jung, G., Mueller, D. L. & Schwartz, R. H. (1990). Inhibition of antigen specific proliferation of type 1 murine T cell clones after stimulation with immobilized anti-CD3 monoclonal antibody. Journal of Immunology 144, 16–22.Google Scholar
Kanellopoulos, J. M., De Petris, S., Leca, G. & Crumpton, M. J. (1985). The mitogenic lectin from Paseolus vulgaris does not recognize the T3 antigen of human T lymphocytes. European Journal of Immunology 15, 479–86.Google Scholar
Kelly, E. A., Cruz, E. S., Hauda, K. M. & Wassom, D. L. (1991). INF-γ and IL-5 producing cells compartmentalize to different lymphoid organs in Trichinella spiralis-infected mice. Journal of Immunology 147, 306–11.Google Scholar
Kubo, R. T., Born, W., Kappler, J. M., Marrack, P. & Pigeon, M. (1989). Characterization of a monoclonal antibody which detects all murine αβ T-cell receptors. Journal of Immunology 142, 2736.CrossRefGoogle Scholar
Kumar, D. & Gaur, S. N. S. (1994). Taenia solium cysticercosis in pigs. Helminthological Abstracts 63, 365–83.Google Scholar
Kunz, J., Kalinna, B., Watschke, V. & Geyer, E. (1989). Taenia crassiceps metacestode vesicular fluid antigens shared with the Taenia solium larval stage and reactive with serum antibodies from patients with neurocysticercosis. International Journal of Medical Microbiology 271, 510–20.Google Scholar
Kupper, T., Horowitz, M., Lee, F., Robb, R. & Flood, P. M. (1987). Autocrine growth of T-cells independent of interleukin 2: Identification of interleukin 4 (IL-4, BSF-1) as a autocrine growth factor for cloned antigen-specific helper T-cell. Journal of Immunology 138, 4280–7.CrossRefGoogle ScholarPubMed
Larralde, C., Sotelo, J., Montoya, R. M., Palencia, G., Padilla, A., Govezensky, T., Diaz, M. L. & Sciutto, E. (1990). Immunodiagnosis of human cysticercosis in cerebrospinal fluid. Antigens from the murine Taenia crassiceps cysticerci effectively substitute those from porcine Taenia solium. Archives of Pathology and Laboratory Medicine 114, 926–8.Google Scholar
Leid, R. W., Suquet, C. M. & Perryman, L. E. (1984). Inhibition of antigen and lectin-induced proliferation of rat spleen cells by a Taenia taeniaeformis proteinase inhibitor. Clinical and Experimental Immunology 57, 187–91.Google ScholarPubMed
Leo, O., Foo, M., Sachs, D. H., Samuelson, L. E. & Bluestone, J. A. (1987). Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proceedings of the National Academy of Sciences, USA 84, 1374–8.Google Scholar
Mage, M. (1991). Fractionation of T-cells and B cells using panning techniques. In Current Protocols in Immunology, Vol. 1 (ed. Coligan, J. E., Kruisbeek, A. M., Margulies, D. H., Shevach, E. M. & Strober, W.), p. 3.5.1. New York: John Wiley and Sons.Google Scholar
Mitchell, G. F., Marchalonis, J. J., Smith, P. M., Nicholas, W. L. & Warner, N. L. (1977). Studies on immune responses to larval cestodes in mice. Immunoglobulins associated with the larvae of Mesocestoides corti. Australian Journal of Experimental Biology and Medical Science 55, 187–211.Google Scholar
Molinari, J. L., Tato, P. & Valles, Y. (1987). Immunodepresión de linfocitos T en cerdos, modulada por Cysticercus cellulosae. Revista Latino Americana de Microbiologia 29, 293–300.Google Scholar
Nabors, G. S., Afonso, L. C. C., Farrell, J. P. & Scott, P. (1995). Switch from a type 2 to a type 1 helper cells response and cure of established Leishmania major infection in mice is induced by combined therapy with interleukin 12 and Pentostam. Proceedings of the National Academy of Sciences, USA 92, 3142–6.Google Scholar
Nishizuka, Y. (1992). Intracellular signaling by hydrolisis of phospholipids and activation of protein kinase C. Science 258, 607–14.Google Scholar
Noelle, R. J., Daum, J., Bartlett, W. C., McCann, J. & Shepherd, D. M. (1991). Cognate interactions between helper T-cells and B-cells. V. Reconstitution of T helper cell function using purified membranes from activated Th1 and Th2 helper cells and lymphokines. Journal of Immunology 146, 1118–24.Google Scholar
Oswald, I. P., Gazzinelli, R. T., Sher, A. & James, S. L. (1992). IL-10 synergizes with IL-4 and transforming growth factor-beta to inhibit macrophage cytotoxic activity. Journal of Immunology 148, 3578–82.Google Scholar
Pearce, E. J., Caspar, P., Grzych, J. M., Lewis, F. A. & Sher, A. (1991). Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. Journal of Experimental Medicine 173, 159–66.Google Scholar
Plaut, M., Pierce, J. H., Watson, C. J., Hanley-Hyde, J., Nordan, R. P. & Paul, W. E. (1989). Mast cell lines produce lymphokines in response to cross-linkage of FceRI or to calcium ionophores. Nature, London 339, 64–7.Google Scholar
Rickard, M. D. & Williams, J. F. (1982). Hydatidosis/Cysticercosis: Immune Mechanisms and immunization against infection. Advances in Parasitology 21, 230.Google Scholar
Sally, C-Y., Chau, J. & Freeman, R. S. (1976).Intraperitoneal passage of Taenia crassiceps in rats. Journal of Parasitology 62, 837–9.Google Scholar
Schultz, C. L., Rothman, P., Kühn, R., Kenry, M., Müller, W., Rajewsky, K., Alt, F. & Coffman, R. L. (1992). T helper cell membranes promote IL-4-independent expression of germ-line C gamma 1 transcripts in B cells. Journal of Immunology 149, 60–4.Google Scholar
Scott, P., Natovitz, P., Coffman, R. L., Pearce, E. J. & Sher, A. (1988). Immunoregulation of cutaneous leishmaniasis. T-cell lines that transfer protective immunity of exacerbation belong to different T helper subsets and respond to different parasite antigens. Journal of Experimental Medicine 168, 1675–84.Google Scholar
Seder, R. A., Boulay, J. L., Finkelman, F., Barbier, S., Ben-Sasson, S. Z., Legros, C. L. & Paul, W. E. (1992). CD8+ cells can be primed in vitro to produce IL-4. Journal of Immunology 148, 1652–6.Google Scholar
Sher, A., Gazzinelli, R. T., Oswald, I. P., Clerici, M., Kullberg, M., Pearce, E. J., Berzofsky, J. A., Mosmann, T. R., James, S. L., Morse, H. C. & Shearer, G. M. (1992). Role of T-cell derived cytokines in the downregulation of immune responses in parasitic and retroviral infection. Immunological Reviews 127, 183–204.Google Scholar
Short, J. A., Heiner, D. C., Hsiao, R. L. & Andersen, F. L. (1990). Immunoglobulin E and G4 antibodies in cysticercosis. Journal of Clinical Microbiology 28, 1635–9.Google Scholar
Tanaka, T., Ben-Sasson, S. Z. & Paul, W. E. (1991). IL-4 increases IL-2 production by T-cells in response to accessory cell-independent stimuli. Journal of Immunology 146, 3831.Google Scholar
Te-Velde, A. A., Huijbens, R. J. F., Heije, K., De Vries, J. E. & Figdor, C. G. (1990). Interleukin-4 (IL-4) inhibits secretion of IL-1β, tumor necrosis factor α, and IL-6 by human monocytes. Blood 76, 1392–7.Google Scholar
Thompson-Snipes, L. A., Shar, V., Bond, M. W., Mosmann, T. R., Moore, K. W. & Rennick, D. M. (1991).Interleukin 10: a novel stimulatory factor for mast cells and their progenitors. Journal of Experimental Medicine 173, 507–10.Google Scholar
Vasquez, V. & Sotelo, J. (1992). The course of seizures after treatment for cerebral cysticercosis. New England Journal of Medicine 327, 696–701.Google Scholar
White, A. C., Tato, P. & Molinari, J. L. (1992). Host-parasite interactions in Taenia solium cysticercosis. Infectious Agents and Disease 1, 185–93.Google Scholar
Willms, K. & Merchant, M. T. (1980). The inflammatory reaction surrounding Taenia solium larvae in pig muscle: ultrastructural and light microscopic observations. Parasite Immunology 2, 261–7.Google Scholar
Yan, Y. W., Wu, L. R., Wang, X. N., Zhang, W. Y., Zhang, J. F. & Zhu, L. X. (1991). IgE and IgE-mediated immunoreaction in the pathogenesis of human cysticercosis. Chung Kuo Chi Sheng Hsueh Yu Chi Sheng Chung Ping Tsa Chih 9, 68–74.Google Scholar