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The effect of infection history on the fitness of the gastrointestinal nematode Strongyloides ratti

Published online by Cambridge University Press:  05 March 2009

C. BLEAY
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
C. P. WILKES
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
S. PATERSON
Affiliation:
School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, UK
M. E. VINEY*
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
*
*Corresponding author: School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK. Tel: +44 (0)117 928 7469. Fax: +44 (0)117 331 7985. E-mail: Mark.Viney@bristol.ac.uk

Summary

Hosts in nature will often acquire infections by different helminth species over their lifetime. This presents the potential for new infections to be affected (particularly via the host immune response) by a host's history of previous con- or hetero-specific infection. Here we have used an experimental rat model to investigate the consequences of a history of primary infection with either Nippostrongylus brasiliensis, Strongyloides venezuelensis or S. ratti on the fitness of, and immunological response to, secondary infections of S. ratti. We found that a history of con-specific, but not hetero-specific, infection reduced the survivorship of S. ratti; the fecundity of S. ratti was not affected by a history of either con- or hetero-specific infections. We also found that a history of con-specific infection promoted Th2-type responses, as shown by increased concentrations of total IgE, S. ratti-specific IgG1, rat mast cell protease II (RMCPII), IL4 (but decreased concentrations of IFNγ) produced by mesenteric lymph node cells in response to S. ratti antigen. Additionally, S. ratti-specific IgG1 was positively related to the intensity of both primary and secondary infections of S. ratti. Hetero-specific primary infections were only observed to affect the concentration of total IgE and RMCPII. The overall conclusion of these experiments is that the major immunological effect acting against an infection is induced by the infection itself and that there is little effect of prior infections of the host.

Type
Research Article
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Bancroft, A. J., Else, K. J. and Grencis, R. K. (1994). Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. European Journal of Immunology 24, 31133118.CrossRefGoogle ScholarPubMed
Behnke, J. M. (2008). Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions.... or pure randomness? Parasitology 135, 751766.CrossRefGoogle ScholarPubMed
Bleay, C., Wilkes, C. P., Paterson, S. and Viney, M. E. (2007). Density-dependent immune responses against the gastrointestinal nematode Strongyloides ratti. International Journal for Parasitology 37, 15011509.CrossRefGoogle ScholarPubMed
Crawley, M. J. (2002). Statistical Computing: an Introduction to Data Analysis Using S-plus. Wiley, Chichester, UK.Google Scholar
Finkelman, F. D., Shea-Donohue, T., Goldhill, J., Sullivan, C. A., Morris, S. C., Madden, K. B., Gause, W. C. and Urban, J. F. J. (1997). Cytokine regulation of host defense against parasitic gastrointestinal nematodes: Lessons from studies with rodent models. Annual Review of Immunology 15, 505533.CrossRefGoogle ScholarPubMed
Finkelman, F. D., Wynn, T. A., Donaldson, D. D. and Urban, J. F. J. (1999). The role of IL-13 in helminth-induced inflammation and protective immunity against nematode infections. Current Opinion in Immunology 11, 420426.CrossRefGoogle ScholarPubMed
Gemmill, A. W., Viney, M. E. and Read, A. F. (1997). Host immune status determines sexuality in a parasitic nematode. Evolution 51, 393401.CrossRefGoogle Scholar
Harvey, S. C., Gemmill, A. W., Read, A. F. and Viney, M. E. (2000). The control of morph development in the parasitic nematode Strongyloides ratti. Proceedings of the Royal Society of London, B 267, 20572063.Google Scholar
Keymer, A. E. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573587.Google Scholar
Kimura, E., Shintoku, Y., Kadosaka, T., Fujiwaram, M., Kondom, S. and Itoh, M. (1999). A second peak of egg excretion in Strongyloides ratti-infected rats: its origin and biological meaning. Parasitology 119, 221226.CrossRefGoogle ScholarPubMed
Moqbel, R. and Wakelin, D. (1979). Trichinella spiralis and Strongyloides ratti: Immune interaction in adult rats. Experimental Parasitology 47, 6572.Google Scholar
Nawa, Y., Mimori, T., Korenaga, M. and Tada, I. (1982). Stage-specific cross-resistance between Nippostrongylus brasiliensis and Strongyloides ratti (Nematoda) in rats. Journal of Parasitology 68, 804808.CrossRefGoogle ScholarPubMed
Paterson, S. and Viney, M. E. (2002). Host immune responses are necessary for density-dependence in nematode infections. Parasitology 125, 283292.CrossRefGoogle ScholarPubMed
Paterson, S., Wilkes, C. P., Bleay, C. and Viney, M. E. (2008). Immunological responses elicited by different infection regimes with Strongyloides ratti. PLoS One 3, e2509.CrossRefGoogle ScholarPubMed
Turner, J. D., Faulkner, H., Kamgno, J., Cormont, F., van Snick, J., Else, K. J., Grencis, R. K., Behnke, J. M., Boussinesq, M. and Bradley, J. E. (2003). Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. Journal of Infectious Diseases 188, 17681775.CrossRefGoogle Scholar
Viney, M. E. (1996). Developmental switching in the parasitic nematode Strongyloides ratti. Proceedings of the Royal Society of London, B 263, 201208.Google ScholarPubMed
West, S. A., Gemmill, A. W., Graham, A., Viney, M. E. and Read, A. F. (2001). Immune stress and facultative sex in a parasitic nematode. Journal of Evolutionary Biology 14, 333337.Google Scholar
Wilkes, C. P., Bleay, C., Paterson, S. and Viney, M. E. (2007). The immune response during a Strongyloides ratti infection of rats. Parasite Immunology 29, 339346.CrossRefGoogle ScholarPubMed
Wilkes, C. P., Thompson, F. J., Gardner, M. P., Paterson, S. and Viney, M. E. (2004). The effect of the host immune response on the parasitic nematode Strongyloides ratti. Parasitology 128, 661669.CrossRefGoogle ScholarPubMed
Wilson, K. and Grenfell, B. T. (1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 3338.Google Scholar