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Immunity-mediated regulation of fecundity in the nematode Heligmosomoides polygyrus – the potential role of mast cells

Published online by Cambridge University Press:  22 December 2009

K. HASHIMOTO ,
R. UCHIKAWA ,
T. TEGOSHI ,
K. TAKEDA ,
M. YAMADA  and
N. ARIZONO
K. HASHIMOTO*
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kyoto 602-8566, Japan
R. UCHIKAWA
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kyoto 602-8566, Japan
T. TEGOSHI
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kyoto 602-8566, Japan
K. TAKEDA
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kyoto 602-8566, Japan
M. YAMADA
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kyoto 602-8566, Japan
N. ARIZONO
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kyoto 602-8566, Japan
*
*Corresponding author: Tel: +81 75 2515326. Fax: +81 75 2515328. E-mail: [email protected]
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Summary

Previous studies have shown that host immunity regulates the fecundity of nematodes. The present study was aimed at clarifying the reversible nature of fecundity in response to changes of immunological status and to determine which effector cells are responsible for compromising fecundity in Heligmosomoides polygyrus. Enhanced fecundity was observed in immunocompromised SCID and nu/nu mice compared to those in the corresponding wild-type mice, with significantly fewer numbers of intrauterine eggs produced in the wild-type than in the immunodeficient mice. When 14-day-old adult worms from BALB/c mice were transplanted into naïve BALB/c mice, their fecundity increased significantly as early as 24 h post-transplantation, but not when they were transferred into immune mice, suggesting the plastic and reversible nature of fecundity in response to changes in host immunological status. In mast cell-deficient W/Wv mice, nematode fecundity was significantly higher than in mast cell-reconstituted W/Wv or +/+ mice. The serum levels of the mast-cell protease mMCP1 were markedly increased in the wild-type as well as the mast cell-reconstituted W/Wv, but not in the W/Wv, SCID, or nu/nu mice during infection. These findings raise the interesting possibility that certain activities of mast cells, either directly or indirectly, regulate parasite fecundity during infection.

Keywords

Heligmosomoides polygyrusfecunditymast cellW/Wv mouse
Type
Research Article
Information
Parasitology , Volume 137 , Issue 5 , April 2010 , pp. 881 - 887
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Arizono, N., Kasugai, T., Yamada, M., Okada, M., Morimoto, M., Tei, H., Newlands, G. F., Miller, H. R. and Kitamura, Y. (1993). Infection of Nippostrongylus brasiliensis induces development of mucosal-type but not connective tissue-type mast cells in genetically mast cell-deficient Ws/Ws rats. Blood 81, 2572–2578.CrossRefGoogle Scholar
Artis, D. and Grencis, R. K. (2008). The intestinal epithelium: sensors to effectors in nematode infection. Mucosal Immunology 1, 252–264.CrossRefGoogle ScholarPubMed
Bleay, C., Wilkes, C. P., Paterson, S. and Viney, M. E. (2009). The effect of infection history on the fitness of the gastrointestinal nematode Strongyloides ratti. Parasitology 136, 567–577. doi:10.1017/S0031182009005617CrossRefGoogle ScholarPubMed
Finkelman, F. D., Shea-Donohue, T., Morris, S. C., Gildea, L., Strait, R., Madden, K. B., Schopf, L. and Urban, J. F. Jr. (2004). Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunological Reviews 201, 139–155. doi:10.1111/j.0105-2896.2004.00192.xCrossRefGoogle Scholar
Galli, S. J. and Tsai, M. (2008). Mast cells: versatile regulators of inflammation, tissue remodeling, host defense and homeostasis. Journal of Dermatological Science 49, 7–19. doi:10.1016/j.jdermsci.2007.09.009CrossRefGoogle Scholar
Hashimoto, K., Uchikawa, R., Tegoshi, T., Takeda, K., Yamada, M. and Arizono, N. (2009). Depleted intestinal goblet cells and severe pathological changes in SCID mice infected with Heligmosomoides polygyrus. Parasite Immunology 31, 457–465. doi:10.1111/j.1365-3024.2009.01123.xCrossRefGoogle ScholarPubMed
Khan, W. I. and Collins, S. M. (2004). Immune-mediated alteration in gut physiology and its role in host defence in nematode infection. Parasite Immunology 26, 319–326.CrossRefGoogle ScholarPubMed
Kitamura, Y., Go, S. and Hatanaka, K. (1978). Decrease of mast cells in W/W v mice and their increase by bone marrow transplantation. Blood 52, 447–452.CrossRefGoogle Scholar
Lawrence, C. E. and Pritchard, D. I. (1994). Immune response profiles in responsive and non-responsive mouse strains infected with Heligmosomoides polygyrus. International Journal for Parasitology 24, 487–494. doi:10.1016/0020-7519(94)90139-2CrossRefGoogle ScholarPubMed
Miller, H. R. P. (1987). Gastrointestinal mucus, a medium for survival and for elimination of parasitic nematodes and protozoa. Parasitology 94 (Suppl), S77–S100.CrossRefGoogle ScholarPubMed
Monroy, F. G. and Enriquez, F. J. (1992). Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitology Today 8, 49–54. doi:10.1016/0169-4758(92)90084-FCrossRefGoogle Scholar
Newlands, G. F., Miller, H. R., MacKellar, A. and Galli, S. J. (1995). Stem cell factor contributes to intestinal mucosal mast cell hyperplasia in rats infected with Nippostrongylus brasiliensis or Trichinella spiralis, but anti-stem cell factor treatment decreases parasite egg production during N. brasiliensis infection. Blood 86, 1968–1976.CrossRefGoogle ScholarPubMed
Nowell, M. A., De Pomerai, D. I. and Pritchard, D. I. (1999). Caenorhabditis elegans as a biomonitor for immunological stress in nematodes. Parasite Immunology 21, 495–505. 10.1046/j.1365-3024/1999/00249.xCrossRefGoogle ScholarPubMed
Paterson, S. and Viney, M. E. (2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283–292. doi:10.1017/S0031182002002056CrossRefGoogle ScholarPubMed
Pritchard, D. I., Quinnell, R. J. and Walsh, E. A. (1995). Immunity in humans to Necator americanus: IgE, parasite weight and fecundity. Parasite Immunology 17, 71–75. doi:10.1111/j.1365-3024.1995.tb00968.xCrossRefGoogle Scholar
Rothwell, T. L. (1989). Immune expulsion of parasitic nematodes from the alimentary tract. International Journal for Parasitology 9, 139–168.CrossRefGoogle Scholar
Urban, J. F. Jr., Katona, I. M. and Finkelman, F. D. (1991). Heligmosomoides polygyrus: CD4+ but not CD8+ T cells regulate the IgE response and protective immunity in mice. Experimental Parasitology 73, 500–511. doi:10.1016/0014-4894(91)90074-7CrossRefGoogle Scholar
Urban, J. F. Jr., Maliszewski, C. R., Madden, K. B., Katona, I. M. and Finkelman, F. D. (1995). IL-4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice. The Journal of Immunology 15, 4675–4684.CrossRefGoogle Scholar
Viney, M. E., Steer, M. D. and Wilkes, C. P. (2006). The reversibility of constraints on size and fecundity in the parasitic nematode Strongyloides ratti. Parasitology 133, 477–483. doi:10.1017/S003118200600062X CrossRefGoogle ScholarPubMed