Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T11:02:09.410Z Has data issue: false hasContentIssue false

High transmission rates restore expression of genetically determined susceptibility of mice to nematode infections

Published online by Cambridge University Press:  05 January 2006

M. E. SCOTT
Affiliation:
Institute of Parasitology, Macdonald Campus of McGill University, 21 111 Lakeshore Road, Ste-Anne de Bellevue, Quebec, Canada H9X 3V9

Abstract

This study investigated why the susceptible or resistance phenotype to the nematode Heligmosomoides polygyrus was lost when susceptible (C57BL/6) and resistant (Balb/c) strains of mice were housed together in indoor arenas with continuous transmission of the parasite larvae present in peat trays (Scott, 1991). First, both strains expressed their normal phenotype when given a controlled challenge while living in arenas, and when experimentally infected with only 5 parasite larvae. To test whether chronic exposure to peat altered the resistance phenotype, mice were given a challenge infection while living on peat. C57BL/6 mice living on peat had higher egg production and higher worm numbers than Balb/c mice, except at 2 months post-challenge. Finally, natural transmission rates were increased in arena experiments through either regular replacement of arena mice with naïve mice or direct introduction of additional larvae. A transient difference in infection levels between strains was detected in response to a modest increase in transmission whereas a 10-fold increase in transmission allowed C57BL/6 mice to exhibit the typical profile of high egg production and elevated worm numbers. These data indicate that C57BL/6 mice are less able to regulate parasite numbers at high transmission rates compared with lower transmission rates.

Type
Research Article
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. ( 1986). The population dynamics and epidemiology of intestinal nematode infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 686696.CrossRefGoogle Scholar
Bansemir, A. D. and Sukhdeo, M. V. K. ( 1994). The food resource of adult Heligmosomoides polygyrus in the small intestine. Journal of Parasitology 80, 2428.CrossRefGoogle Scholar
Behnke, J. M., Cabaj, W. and Wakelin, D. ( 1992). Susceptibility of adult Heligmosomoides polygyrus to intestinal inflammatory responses induced by heterologous infection. International Journal for Parasitology 22, 7586.CrossRefGoogle Scholar
Behnke, J. M., Iraqui, F., Menge, D., Baker, R. L., Gibson, J. and Wakelin, D. ( 2003). Chasing the genes that control resistance to gastrointestinal nematodes. Journal of Helminthology 77, 99110.CrossRefGoogle Scholar
Behnke, J. M. and Robinson, M. ( 1985). Genetic control of immunity to Nematospiroides dubius: a 9-day anthelmintic abbreviated immunizing regime which separates weak and strong responder strains of mice. Parasite Immunology 7, 235253.CrossRefGoogle Scholar
Bisset, S. A., Morris, C. A., Squire, D. R., Hickey, S. M. and Wheeler, M. ( 1994). Genetics of resilience to nematode parasites in sheep. New Zealand Journal of Agricultural Research 37, 521534.CrossRefGoogle Scholar
Brailsford, T. J. and Behnke, J. M. ( 1992). The dynamics of trickle infections with Heligmosomoides polygyrus in syngeneic strains of mice. International Journal for Parasitology 22, 351359.CrossRefGoogle Scholar
Brindley, P. J., He, S., Sitepu, P., Pattie, W. A. and Dobson, C. ( 1986). Inheritance of immunity in mice to challenge infection with Nematospiroides dubius. Heredity 57, 5358.CrossRefGoogle Scholar
CANADIAN COUNCIL ON ANIMAL CARE ( 1984). Guide to the Care and Use of Experimental Animals, Vol. 1 and II. National Library of Canada, Ottawa, ON, Canada.
Chapman, J. C., Christian, J. J., Pawlikowski, M. A. and Michael, S. D. ( 1998). Analysis of steroid hormone levels in female mice at high population density. Physiology and Behavior 64, 529533.CrossRefGoogle Scholar
Cypess, H. R. and Zidian, J. L. ( 1975). Heligmosomoides polygyrus (=Nematospiroides dubius): the development of self-cure and/or protection in several strains of mice. Journal of Parasitology 61, 819824.CrossRefGoogle Scholar
Dirks, P. and Freeman, H. J. ( 1987). Effects of differing purified cellulose, pectin and hemicellulose fiber diets on mucosal morphology in the rat small and large intestine. Clinical Investigations in Medicine 10, 3238.Google Scholar
Eady, S. J. ( 2003). Breeding for gastrointestinal nematode resistance in sheep: panacea or patch? Journal of Parasitology (Suppl.) 89, S215S225.Google Scholar
Enriquez, F. J., Zidian, J. L. and Cypess, R. H. ( 1988). Nematospiroides dubius: genetic control of immunity to infections in mice. Experimental Parasitology 67, 1219.CrossRefGoogle Scholar
Fakae, B. B., Harrison, L. J. and Sewell, M. M. ( 2000). The intensity and duration of primary Heligmosomoides polygyrus infection in TO mice modify acquired immunity to secondary challenge. Journal of Helminthology 74, 225231.Google Scholar
Gause, W. C., Urban, J. F., Jr. and Stadecker, M. J. ( 2003). The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269277.CrossRefGoogle Scholar
Heitman, T. L., Koski, K. G. and Scott, M. E. ( 2003). Energy deficiency alters behaviours involved in transmission of Heligmosomoides polygyrus (Nematoda) in mice. Canadian Journal of Zoology 81, 17671773.CrossRefGoogle Scholar
Keymer, A. E. and Tarlton, A. B. ( 1991). The population dynamics of acquired immunity to Heligmosomoides polygyrus in the laboratory mouse: strain, diet and exposure. Parasitology 103, 121126.CrossRefGoogle Scholar
Keymer, A. E., Tarlton, A. B., Hiorns, R. W., Lawrence, C. E. and Pritchard, D. I. ( 1990). Immunogenetic correlates of susceptibility to infection with Heligmosomoides polygyrus in outbred mice. Parasitology 101, 6973.CrossRefGoogle Scholar
Khan, L. P., Knox, M. R., Gray, G. D., Lea, J. M. and Walkden-Brown, S. W. ( 2003). Enhancing immunity to nematode parasites in single-bearing Merino ewes through nutrition and genetic selection. Veterinary Parasitology 112, 211225.CrossRefGoogle Scholar
Menge, D. M., Behnke, J. M., Lowe, A., Gibson, J. P., Iraqui, F. A., Baker, R. L. and Wakelin, D. ( 2003). Mapping of chromosomal regions influencing immunological responses to gastrointestinal nematode infections in mice. Parasite Immunology 25, 341349.CrossRefGoogle Scholar
Moulia, C., Le Brun, N. and Renaud, F. ( 1996). Mouse-parasite interactions: from gene to population. Advances in Parasitology 38, 119167.CrossRefGoogle Scholar
Peng, X., Lang, C. M., Drozdowicz, C. K. and Ohlsson-Wilhelm, B. M. ( 1989). Effect of cage population density on plasma corticosterone and peripheral lymphocyte populations of laboratory mice. Laboratory Animals 23, 302306.CrossRefGoogle Scholar
Prowse, S. J., Mitchell, G. F., Ey, P. L. and Jenkin, C. R. ( 1979). The development of resistance in different inbred strains of mice to infection with Nematospiroides dubius. Parasite Immunology 1, 277288.CrossRefGoogle Scholar
Quinnell, R. J. ( 2003). Genetics of susceptibility to human helminth infections. International Journal for Parasitology 33, 12191231.CrossRefGoogle Scholar
Scott, M. E. ( 1988). Predisposition of mice to Heligmosomoides polygyrus and Aspiculuris tetraptera (Nematoda). Parasitology 97, 101114.CrossRefGoogle Scholar
Scott, M. E. ( 1991). Heligmosomoides polygyrus (Nematoda): susceptible and resistant strains of mice are indistinguishable following natural infection. Parasitology 103, 429438.CrossRefGoogle Scholar
Scott, M. E., Dare, O. K., Tu, T. and Koski, K. G. ( 2005). Mild energy restriction alters mouse-nematode population dynamics in semi-natural indoor arenas. Canadian Journal of Zoology 83, 610619.CrossRefGoogle Scholar
Sigleo, S., Jackson, M. J. and Vahouny, G. V. ( 1984). Effects of dietary fiber constituents on intestinal morphology and nutrient transport. American Journal of Physiology 264, G34G39.CrossRefGoogle Scholar
Slater, A. F. and Keymer, A. E. ( 1986). Heligmosomoides polygyrus (Nematoda): the influence of dietary protein on the dynamics of repeated infection. Proceedings of the Royal Society of London, B 229, 6983.CrossRefGoogle Scholar
Stear, M. J. and Murray, M. ( 1994). Genetic resistance to parasitic disease: particularly of resistance in ruminants to gastrointestinal nematodes. Veterinary Parasitology 54, 161176.CrossRefGoogle Scholar
Su, Z. and Dobson, C. ( 1997). H-2 genes and resistance to infection with Heligmosomoides polygyrus in selectively bred mice. International Journal for Parasitology 27, 595600.CrossRefGoogle Scholar
Sun, Y., Koski, K. G., Wykes, L. J. and Scott, M. E. ( 2002). Dietary pectin, but not cellulose, influences Heligmosomoides polygyrus (Nematoda) reproduction and intestinal morphology in the mouse. Parasitology 124, 447455.CrossRefGoogle Scholar
Tanguay, G. and Scott, M. E. ( 1992). Factors generating aggregation of Heligmosomoides polygyrus (Nematoda) in laboratory mice. Parasitology 104, 519529.CrossRefGoogle Scholar
Villarroel, M., Acevedo, C., Yanez, E. and Biolley, E. ( 2003). Functional properties of Sphagnum magellanicum fiber and its direct use in formulation of bakery products. [In Spanish]. Archivos Latinoamericanos de Nutrición 53, 4007.Google Scholar
Wahid, F. N. and Behnke, J. M. ( 1991). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): H-2 linked genes determine worm survival. Parasitology 103, 157164.Google Scholar
Wahid, F. N. and Behnke, J. M. ( 1996). Genetic control of acquired resistance to Heligmosomoides polygyrus: overcoming genetically determined weak responder status by strategic immunization with ivermectin-abbreviated infections. Journal of Helminthology 70, 159168.CrossRefGoogle Scholar
Wahid, F. N., Behnke, J. M., Grencis, R. K., Else, K. J. and Ben-Smith, A. W. ( 1994). Immunological relationships during primary infection with Heligmosomoides polygyrus: Th2 cytokines and primary response phenotype. Parasitology 108, 461471.CrossRefGoogle Scholar
Wakelin, D. ( 1988). Genetic control of susceptibility and resistance to parasitic infection. Advances in Parasitology 16, 219308.Google Scholar
Wassom, D. L., Dick, T. A., Arnason, N., Strickland, D. and Grundmann, A. W. ( 1986). Host genetics: a key factor in regulating the distribution of parasites in natural host populations. Journal of Parasitology 72, 334337.CrossRefGoogle Scholar