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The effect of the host immune response on the parasitic nematode Strongyloides ratti

Published online by Cambridge University Press:  13 May 2004

C. P. WILKES
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
F. J. THOMPSON
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
M. P. GARDNER
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

Abstract

The host immune response has profound effects on parasitic nematode infections. Here we have investigated how a range of infection parameters are affected by host immune responses and by their suppression and enhancement. The infection parameters considered were the number of parasitic females, their size, per capita fecundity and intestinal position. We found that in immunosuppressive treatments worms persist in the gut, sometimes with a greater per capita fecundity, maintain their size and have a more anterior gut position, compared with worms from control animals. In immunization treatments there are fewer worms in the gut, sometimes with a lower per capita fecundity and they are shorter and have a more posterior gut position, compared with worms from control animals. Worms from animals immunosuppressed by corticosteroid treatment reverse their changes in size and gut position. This description of these phenomena pave the way for a molecular biological analysis of how these changes in infection parameters are brought about by the host immune response.

Type
Research Article
Copyright
2004 Cambridge University Press

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References

REFERENCES

ABE, T. & NAWA, Y. ( 1988). Worm expulsion and mucosal mast cell response induced by repetitive IL-3 administration in Strongyloides ratti-infected nude mice. Immunology 63, 181185.Google Scholar
BRAMBELL, M. R. ( 1965). The distribution of a primary infestation of Nippostrongylus brasiliensis in the small intestine of laboratory rats. Parasitology 55, 313324.CrossRefGoogle Scholar
GEMMILL, A. W., VINEY, M. E. & READ, A. F. ( 1997). Host immune status determines sexuality of a parasite nematode. Evolution 51, 393401.CrossRefGoogle Scholar
GEMMILL, A. W., SKORPING, A. & READ, A. F. ( 1999). Optimal timing of first reproduction in parasitic nematodes. Journal of Evolutionary Biology 12, 11481156.CrossRefGoogle Scholar
GUINNEE, M. A., GEMMILL, A. W., CHAN, B. H. K., VINEY, M. E. & READ, A. F. ( 2003). Host immune status affects maturation time in two nematode species – but not as predicted by a simple life history model. Parasitology 127, 507512.CrossRefGoogle Scholar
HARVEY, S. C., GEMMILL, A. W., READ, A. F. & VINEY, M. E. ( 2000). The control of morph development in the parasitic nematode Strongyloides ratti. Proceedings of the Royal Society of London, Series B 267, 20572063.CrossRefGoogle Scholar
KENNEDY, M. W. ( 1980). Effects of the host immune response on the longevity, fecundity and position in the intestine of Trichinella spiralis in mice. Parasitology 80, 4960.CrossRefGoogle Scholar
KENNEDY, M. W. & BRUCE, R. G. ( 1981). Reversibility of the effects of the host immune response on the intestinal phase of Trichinella spiralis in the mouse, following transplantation to a new host. Parasitology 82, 3948.CrossRefGoogle Scholar
KIMURA, E., SHINTOKU, Y., KADOSAKA, T., FUJIWARA, M., KONDO, S. & ITOH, M. ( 1999). A second peak of egg excretion in Strongyloides ratti-infected rats: its origin and biological meaning. Parasitology 119, 221226.CrossRefGoogle Scholar
KORENGA, M., HITOSHI, Y., YAMAGUCHI, N., SATO, Y., TAKATSU, K. & TADA, I. ( 1991). The role of interleukin-5 in protective immunity to Strongyloides venezuelensis infection in mice. Immunology 72, 502507.Google Scholar
MILLER, H. R. P. ( 1984). The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology 6, 167259.CrossRefGoogle Scholar
MOQBEL, R. & McLAREN, D. J. ( 1980). Strongyloides ratti: Structural and functional characteristics of normal and immune-damaged worms. Experimental Parasitology 49, 139152.CrossRefGoogle Scholar
MOQBEL, R., McLAREN, D. J. & WAKELIN, D. ( 1980). Strongyloides ratti: Reversibility of immune damage to adult worms. Experimental Parasitology 49, 153166.CrossRefGoogle Scholar
OVINGTON, K. S., MICKIE, K., MATTHAEI, K. I., YOUNG, I. G. & BEHM, C. A. ( 1998). Regulation of primary Strongyloides ratti infections in mice: a role for interleukin-5. Immunology 95, 488493.CrossRefGoogle Scholar
PATERSON, S. & VINEY, M. E. ( 2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283292.CrossRefGoogle Scholar
PATERSON, S. & VINEY, M. E. ( 2003). Functional consequences of genetic diversity in Strongyloides ratti infections. Parasitology 270, 10231032.CrossRefGoogle Scholar
READ, A. F. & SKORPING, A. ( 1995). The evolution of tissue migration by parasitic nematode larvae. Parasitology 111, 359371.CrossRefGoogle Scholar
SCHAD, G. A., THOMPSON, F., TALHAM, G., HOLT, D., NOLAN, T. J., ASHTON, F. T., LANGE, A. M. & BHOPALE, V. M. ( 1997). Barren female Strongyloides stercoralis from occult chronic infections are rejuvinated by transfer to parasite-naïve recipient hosts and give rise to an autoinfective burst. Journal of Parasitology 83, 785791.CrossRefGoogle Scholar
STEAR, M. J., PARK, M. & BISHOP, S. C. ( 1995 a). The key components of resistance to Ostertagia circumcincta in lambs. Parasitology Today 12, 438441.Google Scholar
STEAR, M. J., BISHOP, S. C., DOLIGALASKA, M., DUNCAN, J. L., HOLMES, P. H., IRVINE, J., McCRIRIE, L., McKELLAR, Q. A., SINSKI, E. & MURRAY, M. ( 1995 b). Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643652.Google Scholar
STEAR, M. J., BAIRDEN, K., DUNCAN, J. L., HOLMES, P. H., McKELLAR, Q. A., PARK, M., STRAIN, S., MURRAY, M., BISHOP, S. C. & GETTINBY, G. ( 1997). How hosts control worms. Nature, London 289, 27.CrossRefGoogle Scholar
SUKHDEO, M. V. K. & BANSEMIR, A. D. ( 1996). Critical resources that influence habitat selection decisions by gastrointestinal helminth parasites. International Journal for Parasitology 26, 483498.CrossRefGoogle Scholar
VINEY, M. E., ASHFORD, R. W. & BARNISH, G. ( 1991). A taxonomic study of Strongyloides Grassi, 1879 (Nematoda) with special reference to Strongyloides fuelleborni von Linstow, 1905 in man in Papua New Guinea and the description of a new subspecies. Systematic Parasitology 18, 95109.CrossRefGoogle Scholar
VINEY, M. E. ( 2002 a). How do host immune responses affect nematode infections? Trends in Parasitology 18, 6366.Google Scholar
VINEY, M. E. ( 2002 b). Environmental control of nematode life-cycles. In Behavioural Ecology of Parasites (ed. Lewis, E. E., Campbell, J. F. & Sukhdeo, M. V. K.) , pp. 111128. CABI Publishing, London.
ZAR, J. H. ( 1999). Biostatistical Analysis, 4th Edn. Prentice Hall, London.