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Immune modulation by a high molecular weight fraction from the rat tapeworm Hymenolepis diminuta

Published online by Cambridge University Press:  22 December 2004

A. WANG  and
D. M. McKAY
A. WANG
Affiliation:
Intestinal Disease Research Programme, McMaster University, 1200 Main Street West, Hamilton, Ontario, Canada L8N 3Z5
D. M. McKAY
Affiliation:
Intestinal Disease Research Programme, McMaster University, 1200 Main Street West, Hamilton, Ontario, Canada L8N 3Z5
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Abstract

The host-parasite relationship is exquisitely specific. In exploiting the host niche, a variety of helminth parasites have been shown to directly manipulate their hosts' immune responses. We assessed the ability of a whole-worm extract of Hymenolepis diminuta to modulate immune cell activation. Immune cells isolated from human blood or rodent spleens were activated with the T cell mitogen, concanavalin A (Con A)±H. diminuta extract and cytokine production (i.e. IL-2, -4, -10, -12) and proliferation assessed by ELISA and [3H]thymidine incorporation 24 and 72 h post-treatment, respectively. Co-treatment with the H. diminuta extract (100 μg protein/ml) virtually abolished Con A-induced immune cell proliferation, which was not due to increased apoptosis. Boiling of the worm extract reduced its anti-proliferative effect and fractionation indicated that a >50 kDa component was predominantly responsible for the inhibition of Con A-induced immune cell proliferation. Cytokine determinations revealed that the H. diminuta extract significantly reduced Con A-stimulated IL-2 and IL-4, but enhanced the production of IFNγ, IL-12 and IL-10. The increased IL-12 was due to an LPS contaminant in the extract and a helminth-derived ‘IL-12’-like peptide that bound in the ELISA and Western blots. In contrast, a H. diminuta–derived factor directly stimulated IL-10 production by murine splenocytes, and contaminating LPS synergistically enhanced the production of IL-10. Thus, H. diminuta has the potential to block stimulated T cell proliferation and, by inhibiting IL-4 and promoting IL-10 production, may bias the immune environment towards one of immunoregulation and away from IL-4 dominated T helper 2 type events.

Keywords

cestodecytokineshost-parasite interaction
Type
Research Article
Information
Parasitology , Volume 130 , Issue 5 , May 2005 , pp. 575 - 585
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

ALLEN, J. E. & MACDONALD, A. S. ( 1998). Profound suppression of cellular proliferation mediated by secretions of nematodes. Parasite Immunology 20, 241–247.CrossRefGoogle Scholar
ARECHAVALETA, F., MOLINARI, J. L. & TATO, P. ( 1998). A Taenia solium metacestode factor nonspecifically inhibits cytokine production. Parasitology Research 84, 117–122.Google Scholar
CASTRODEZA, C. ( 1979). Non-progressive evolution, the Red Queen hypothesis and the balance of nature. Acta Biotheories 28, 11–18.CrossRefGoogle Scholar
DEMATTEIS, S., PIROTTO, F., MARQUES, J., NIETO, A., ORN, A. & BAZ, A. ( 2001). Modulation of the cellular immune response by a carbohydrate rich fraction from Echinococcus granulosus protoscoleces in infected or immunized Balb/c mice. Parasite Immunology 23, 1–9.CrossRefGoogle Scholar
DESOWITZ, M. ( 1981). Harmonious parasites. In New Guinea Tapeworms and Jewish Grandmothers. Tales of People and Parasites pp. 179–205. N.W. Norton & Co., London.
DIAZ-GRANADOS, N., HOWE, K., LU, J. & McKAY, D. M. ( 2000). Dextran sulphate sodium-induced colonic histopathology, but not altered epithelial ion transport, is reduced by inhibition of phosphodiesterase activity. American Journal of Pathology 156, 2169–2177.CrossRefGoogle Scholar
DUVAUX-MIRET, O., STEFANO, G. B., SMITH, E. M., DISSOUS, C. & CAPRON, A. ( 1992). Immunosuppression in the definitive and intermediate hosts of the human parasite Schistosoma mansoni by the release of immunoreactive neuropeptides. Proceedings of the National Academy of Sciences, USA 89, 778–781.CrossRefGoogle Scholar
DWINELL, M. B., BASS, P., SCHAEFER, D. M. & OAKS, J. A. ( 1997). Tapeworm infection decreases intestinal transit and enteric aerobic bacterial populations. American Journal of Physiology (Gastrointestinal Liver Physiology) 273, G480–G485.CrossRefGoogle Scholar
FOSTER, N. & LEE, D. ( 1995). A vasoactive intestinal polypeptide like protein excreted/secreted by Nippostrongylus brasiliensis and its effect on contraction of uninfected rat intestine. Parasitology 110, 97–104.Google Scholar
GORDON, S. ( 2003). Alternative activation of macrophages. Nature Reviews Immunology 3, 23–35.CrossRefGoogle Scholar
GRENCIS, R. K. & ENTWISTLE, G. M. ( 1997). Production of an interferon-gamma homologue by an intestinal nematode: functionally significant or interesting artifact? Parasitology 115, S101–S105.Google Scholar
HUNTER, M. M. & McKAY, D. M. ( 2004). Helminths as therapeutic agents for inflammatory bowel disease. Alimentary Pharmacology and Therapeutics 19, 167–177.CrossRefGoogle Scholar
KHAN, W. I., BLENNERHASSETT, P. A., VARGHESE, A. K., CHOWDHURY, S. K., OMSTED, P., DENG, Y. & COLLINS, S. M. ( 2002). Intestinal nematode infection ameliorates experimental colitis in mice. Infection and Immunity 71, 5931–5937.CrossRefGoogle Scholar
KROENING, K. D., ZIMMERMAN, N. P., BASS, P. & OAKS, J. A. ( 2003). Guanosine 3′,5′-cyclic monophosphate: a tapeworm-secreted signal molecule communicating with the rat host's small intestine. Journal of Parasitology 89, 1136–1141.CrossRefGoogle Scholar
LEUNG, M. K., DISSOUS, C., CAPRON, A., WOLDEGABER, H., DUVAUX-MIRET, O., PRYOR, S. & STEFANO, G. B. ( 1995). Schistosoma mansoni: the presence and potential use of opiate-like substances. Experimental Parasitology 81, 208–215.CrossRefGoogle Scholar
LOPEZ-BRIONES, S., SCIUTTO, E., VENTURA, J. L., ZENTELLA, A. & FRAGOSO, G. ( 2003). CD4+ and CD19+ splenocytes undergo apoptosis during an experimental murine infection with Taenia crassiceps. Parasitology Research 90, 157–163.Google Scholar
MAIZELS, R. M. & HOLLAND, M. J. ( 1998). Parasite immunology: pathways for expelling intestinal helminths. Current Opinion in Biology 8, R711–R714.Google Scholar
MAIZELS, R. M. & YAZDANBAKHSH, M. ( 2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733–744.CrossRefGoogle Scholar
McKAY, D. M., BENJAMIN, M. & LU, J. ( 1998). CD4+ T cells mediate superantigen-induced abnormalities in murine jejunal ion transport. American Journal of Physiology (Gastrointestinal Liver Physiology) 275, G29–G38.CrossRefGoogle Scholar
McKAY, D. M., HALTON, D. W., McCAIGUE, M. D., JOHNSTON, C. F., FAIRWEATHER, I. & SHAW, C. ( 1990). Hymenolepis diminuta: Intestinal goblet cell response in male C57 mice. Experimental Parasitology 71, 9–20.CrossRefGoogle Scholar
McKAY, D. M. & SINGH, P. K. ( 1997). Superantigen-activation of immune cells evokes epithelial (T84) transport and barrier abnormalities via interferon-γ and tumour necrosis factor-α. Inhibition of increased permeability, but not diminished secretory responses by transforming growth factor β2. Journal of Immunology 159, 2382–2390.Google Scholar
MOCELLIN, S., PANELLI, M. C., WANG, E., NAGORSEN, D. & MARINCOLA, F. M. ( 2003). The dual role of IL-10. Trends in Immunology 24, 36–43.CrossRefGoogle Scholar
PERSAT, F., VINCENT, C., SCHMITT, D. & MOJON, M. ( 1996). Inhibition of human peripheral blood mononuclear cell proliferative response by glycosphingolipids from metacestodes of Echinococcus multilocularis. Infection and Immunity 64, 3682–3687.Google Scholar
PODESTA, R. B. & METTRICK, D. F. ( 1974). Pathophysiology of cestode infections: effect of Hymenolepis diminuta on oxygen tensions, pH and gastrointestinal function. International Journal for Parasitology 4, 277–292.CrossRefGoogle Scholar
RAKHA, N. K., DIXON, J. B., CARTER, S. D., CRAIG, P. S., JENKINS, P. & FOLKARD, S. ( 1991). Echinococcus multilocularis antigens modify accessory cell function of macrophages. Immunology 74, 652–656.Google Scholar
REARDON, C., SANCHEZ, A., HOGABOAM, C. M. & McKAY, D. M. ( 2001). Tapeworm infection reduces the ion transport abnormalities induced by dextran sulphate sodium (DSS) colitis. Infection and Immunity 69, 4417–4423.CrossRefGoogle Scholar
SATOGUINA, J., MEMPEL, M., LARBI, J., BADUSCHE, M., LOLIGER, C., ADJEI, O., GACHELIN, G., FLEISCHER, B. & HOERAUF, A. ( 2002). Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes and Infection 4, 1291–1300.CrossRefGoogle Scholar
SPOLSKI, R. J., THOMAS, P. G., SEE, E. J., MOONEY, K. A. & KUHN, R. E. ( 2002). Larval Taenia crassiceps secretes a protein with characteristics of murine interferon-gamma. Parasitology Research 88, 431–438.Google Scholar
SUMMERS, R. W., ELLIOT, D. E., QADIR, K., URBAN, J. F., Jr., THOMPSON, R. & WEINSTOCK, J. V. ( 2003). Trichuris suis seems to be same and possibly effective in the treatment of inflammatory bowel disease. American Journal of Gastroenterology 98, 2034–2041.CrossRefGoogle Scholar
VAN DER KLEIJ, D., LATZ, E., BROUWERS, J. F. H. M., KRUIZE, Y. C. M., SCHMITZ, M., KURT-JONES, E. A., ESPEVIK, T., DE JONG, E. C., KAPSENBERG, M. L., GOLENBOCK, D. T., TIELENS, A. G. M. & YAZDANBAKHSH, M. ( 2002). A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. Journal of Biological Chemistry 277, 48122–48129.CrossRefGoogle Scholar
WALKER, M., BAZ, A., DEMATTEIS, S., STETTLER, M., GOTTSTEIN, B., SCHALLER, J. & HEMPILL, A. ( 2004). Isolation and characterization of a secretory component of Echinococcus multiocularis metacestodes potentially involved in modulating the host-parasite interface. Infection and Immunity 72, 527–536.CrossRefGoogle Scholar
YONGE, K. A. & WEBB, R. A. ( 1989). Distribution of histamine in the lumen contents of the small intestine of uninfected and Hymenolepis diminuta-infected rats. Parasitology Research 76, 162–165.CrossRefGoogle Scholar