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Variation and immunity to intestinal worms

  • D. WAKELIN (a1), S. E. FARIAS (a1) and J. E. BRADLEY (a1)

Genetically determined variation in host capacity to express resistance to a given parasite plays a major role in determining the outcome of infection. It can be assumed that the same is true of variation in parasites, but very much less is known of its influence on the host–parasite relationship. Phenotypic and genotypic variation within species of intestinal worms is now well documented, detailed studies having been made of parasites such as Ascaris in humans and trichostrongyles in domestic animals. However, the extent to which this variation affects the course of infection or the host immune response in these hosts is limited. Of the nematodes used as experimental models in laboratory rodents, detailed data on phenotypic or genotypic variation are limited to Strongyloides and Trichinella. Parasite variation is known to be subject to host-mediated selection, the emergence of anthelmintic resistance being a good example. Repeated passage has been used to select lines of parasite that survive in abnormal hosts or which show adaptation to host immunity. Experimental studies with Trichinella genotypes in mice have demonstrated the extent to which parasite variation influences the nature and degree of the host's immune and inflammatory responses, the complex interplay between immunogenicity and pathogenicity influencing both partners in the relationship. Recent studies with isolates of Trichuris muris have shown how parasite variation influences the capacity of mice to express the T helper cell responses necessary for resistance. Molecular differences between T. muris isolates have been shown in their excreted/secreted products as well as at the level of their DNA. Knowledge of the functional consequences of parasite variation will add to our understanding of host-parasite evolution as well as providing a rational basis for predicting the outcome of controls strategies that rest on the improvement of host resistance through vaccination or selective breeding.

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ALFORD, K., OBENDORF, D. L., FREDEKING, T. M., HAEHLING, E. & STEWART, G. L. (1998). Comparison of the inflammatory responses of mice infected with American and Australian Trichinella pseudospiralis or Trichinella spiralis. International Journal for Parasitology 28, 343348.

ANDERSON, T. J., BLOUIN, M. S. & BEECH, R. N. (1998). Population biology of parasitic nematodes: applications of genetic markers. Advances in Parasitology 41, 219282.

ANDERSON, T. J., ROMERO-ABAL, M. E. & JAENIKE, J. (1995). Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology 110, 221229.

BARRETT, F., JACKSON, F. & HUNTLEY, J. F. (1998). Pathogenicity and immunogenicity of different isolates of Teladorsagia circumcincta. Veterinary Parasitology 76, 95104.

BEHNKE, J. M., HANNAH, J. & PRITCHARD, D. I. (1983). Nematospiroides dubius in the mouse: evidence that adult worms depress the expression of homologous immunity. Parasite Immunology 5, 397408.

BEHNKE, J. M., PAUL, V. & RAJASEKARIAH, G. R. (1986). The growth and migration of Necator americanus following infection of neonatal hamsters. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 146149.

BELLABY, T., ROBINSON, K., WAKELIN, D. & BEHNKE, J. M. (1995). Isolates of Trichuris muris vary in their ability to elicit protective immune responses to infection in mice. Parasitology 111, 353357.

BLACKWELL, N. M. & ELSE, K. J. (2001). B cells and antibodies are required for resistance to the parasitic gastrointestinal nematode parasite Trichuris muris. Infection and Immunity 69, 38603868.

BLOUIN, M. S., DAME, J. B., TARRANT, C. A. & COURTNEY, C. H. (1992). Unusual population genetics of a parasitic nematode; mtDNA variation within and among populations. Evolution 46, 470476.

BOLAS-FERNANDEZ, F. & WAKELIN, D. (1989). Infectivity of Trichinella isolates in mice is determined by host immune responsiveness. Parasitology 99, 8388.

BOLAS-FERNANDEZ, F., ALBARRAN-GOMEZ, E., NAVARRETE, I. & MARTINEZ-FERNANDEZ, A. R. (1993). Dynamics of porcine humoral responses to experimental infections by Spanish Trichinella isolates: comparison of three larval antigens in ELISA. Journal of Veterinary Medicine Series B 40, 223229.

CHEHRESA, A., BEECH, R. N. & SCOTT, M. E. (1997). Life-history variation among lines isolated from a laboratory population of Heligmosomoides polygyrus bakeri. International Journal for Parasitology 27, 541551.

CURRIE, R. M., NEEDHAM, C. S., DRAKE, L. J., COOPER, E. S. & BUNDY, D. A. (1998). Antigenic variability in Trichuris trichiura populations. Parasitology 117, 347353.

DOBSON, C. & OWEN, M. E. (1977). Influence of serial passage on the infectivity and immunogenicity of Nematospiroides dubius in mice. International Journal for Parasitology 7, 463466.

DOBSON, C. & TANG, J. M. (1991). Genetic variation and host-parasite relations: Nematospiroides dubius in mice. Journal of Parasitology 77, 884889.

EDWARDS, A. J., BURT, J. S. & OGILVIE, B. M. (1971). The effect of immunity upon some enzymes of the parasitic nematode Nippostrongylus brasiliensis. Parasitology 62, 339347.

ELSE, K. J. & WAKELIN, D. (1988). The effect of H-2 and non-H-2 genes on the expulsion of the nematode Trichuris muris from inbred and congenic mice. Parasitology 96, 543550.

FISHER, M. C. & VINEY, M. E. (1998). The population genetic structure of the facultatively sexual parasitic nematode Strongyloides ratti in wild rats. Proceedings of the Royal Society of London B 265, 703709.

FRASER, E. M. & KENNEDY, M. W. (1991). Heterogeneity in the expression of surface-exposed epitopes among larvae of Ascaris lumbricoides. Parasite Immunology 13, 219225.

GASSER, R. B. & NEWTON, S. E. (2000). Genomic and genetic research on bursate nematodes: significance, implications and prospects. International Journal for Parasitology 30, 509534.

GEMMILL, A. W., VINEY, M. E. & READ, A. F. (2000). The evolutionary ecology of host-specificity: experimental studies with Strongyloides ratti. Parasitology 120, 429437.

GIBBS, H. C. (1986). Hypobiosis in parasitic nematodes – an update. Advances in Parasitology 25, 129174.

GOYAL, P. K. & WAKELIN, D. (1993a). Influence of variation in host strain and parasite isolate on inflammatory and antibody responses to Trichinella spiralis in mice. Parasitology 106, 371378.

GOYAL, P. K. & WAKELIN, D. (1993b). Vaccination against Trichinella spiralis in mice using antigens from different isolates. Parasitology 107, 311317.

GOYAL, P. K., HERMANEK, J. & WAKELIN, D. (1994). Lymphocyte proliferation and cytokine production in mice infected with different geographical isolates of Trichinella spiralis. Parasite Immunology 16, 105110.

GRANT, W. N. & MASCORD, L. J. (1996). Beta-tubulin gene polymorphism and benzimidazole resistance in Trichostrongylus colubriformis. International Journal for Parasitology 26, 7177.

GRANT, W. N. & WHITTINGTON, G. E. (1994). Extensive DNA polymorphism within and between two strains of Trichostrongylus colubriformis. International Journal for Parasitology 24, 719725.

GRENCIS, R. K. & ENTWISTLE, G. M. (1997). Production of an interferon-gamma homologue by an intestinal nematode: functionally significant or interesting artefact? Parasitology 115, S101S106.

HALEY, J. A. (1966). Biology of the rat nematode Nippostrongylus brasiliensis (Travassos, 1914). III. Characteristics of N. brasiliensis after 30–120 serial passages in the Syrian hamster. Journal of Parasitology 52, 98108.

HALL, A. & HOLLAND, C. (2000). Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitology Today 16, 540544.

HARNETT, W., DEEHAN, M. R., HOUSTON, K. M. & HARNETT, M. M. (1999). Immunomodulatory properties of a phosphorylcholine-containing secreted filarial glycoprotein. Parasite Immunology 21, 601608.

HAWDON, J. M., LI, T., ZHAN, B. & BLOUIN, M. S. (2001). Genetic structure of populations of the human hookworm, Necator americanus, in China. Molecular Ecology 10, 14331437.

HOEKSTRA, R., CRIADO FORNELIO, A., FAKKELDIJ, J., BERGMAN, J. & ROOS, M. H. (1997). Microsatellites of the parasitic nematode Haemonchus contortus: polymorphism and linkage with a direct repeat. Molecular and Biochemical Parasitology 89, 9871007.

JENKINS, D. C. & PHILLIPSON, R. F. (1972). Evidence that the nematode Nippostrongylus brasiliensis can adapt to and overcome the effects of host immunity. International Journal for Parasitology 2, 353359.

KAPEL, C. M. O. (2000). Host diversity and biological characteristics of the Trichinella genotypes and their effect on transmission. Veterinary Parasitology 93, 263278.

KAPEL, C. M. O. & GAMBLE, H. R. (2000). Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. International Journal for Parasitology 30, 215221.

KAPEL, C. M. O. (2001). Sylvatic and domestic Trichinella spp. in wild boars; infectivity, muscle larvae distribution, and antibody response. Journal of Parasitology 87, 309314.

KOYAMA, K. & ITO, Y. (1996). Comparative studies on immune responses to infection in susceptible B10.BR mice infected with different strains of the murine nematode parasite Trichuris muris. Parasite Immunology 18, 257263.

KOYAMA, K. & ITO, Y. (2001). Comparative studies on the levels of serum IgG1 and IgG2a in susceptible B10.BR mice infected with different strains of the intestinal nematode parasite Trichuris muris. Parasitology Research 87, 570572.

LA ROSA, G., MARUCCI, G., ZARLENGA, D. S. & POZIO, E. (2001). Trichinella pseudospiralis populations of the Palearctic region and their relationship with populations of the Nearctic and Australian regions. International Journal for Parasitology 31, 297305.

LA ROSA, G. & POZIO, E. (2000). Molecular investigation of African isolates of Trichinella reveals genetic polymorphism in Trichinella nelsoni. International Journal for Parasitology 30, 663667.

MACLEAN, J. M., LEWIS, D. & HOLMES, P. H. (1987). The pathogenesis of benzimidazole-resistant and benzimidazole-susceptible strains of Trichostrongylus colubriformis in the Mongolian gerbil (Meriones unguiculatus). Journal of Helminthology 61, 179189.

MAINGI, N., SCOTT, M. E. & PRICHARD, R. K. (1990). Effect of selection pressure for thiabendazole resistance on fitness of Haemonchus contortus in sheep. Parasitology 100, 327335.

MAIZELS, R. M., BUNDY, D. A. P., SELKIRK, M. E., SMITH, D. F. & ANDERSON, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature 365, 797805.

MALLET, S. & HOSTE, H. (1995). Physiology of two strains of Trichostrongylus colubriformis resistant and susceptible to thiabendazole and mucosal response of experimentally infected rabbits. International Journal for Parasitology 25, 2327.

MURRELL, K. D., LICHTENFELS, R. J., ZARLENGA, D. S. & POZIO, E. (2000). The systematics of the genus Trichinella with a key of species. Veterinary Parasitology 93, 293307.

NAGANO, I., WU, Z., MATSUO, A., POZIO, E. & TAKAHASHI, Y. (1999). Identification of Trichinella isolates by polymerase chain reaction–restriction fragment length polymorphism of the mitochondrial cytochrome c-oxidase submit I gene. International Journal for Parasitology 29, 11131120.

NEWTON, S. E., MORRISH, L. E., MARTIN, P. J., MONTAGUE, P. E. & ROLPH, T. P. (1995). Protection against multiply drug-resistant and geographically distant strains of Haemonchus contortus by vaccination with H11, a gut membrane-derived protective antigen. International Journal for Parasitology 25, 511521.

PRICHARD, R. K. (2001). Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends in Parasitology 17, 445453.

QUINNELL, R. J., BEHNKE, J. M. & KEYMER, A. E. (1991). Host specificity of and cross-immunity between two strains of Heligmosomoides polygyrus. Parasitology 102, 419427.

SEN, H. G. & SETH, D. (1967). Complete development of the human hookworm, Necator americanus in golden hamsters, Mesocricetus auratus. Nature, London 214, 609610.

SOLOMON, M. S. & HALEY, J. A. (1966). Biology of the rat nematode Nippostrongylus brasiliensus (Travassos, 1914). V. Characteristics of N. brasiliensis after serial passage in the laboratory mouse. Journal of Parasitology 52, 237241.

SOLTYS, J., GOYAL, P. K. & WAKELIN, D. (1999). Cellular immune responses in mice infected with the intestinal nematode Trichuris muris. Experimental Parasitology 92, 4047.

STEWART, G. L. (1989). Biological and immunological characteristics of Trichinella pseudospiralis. Parasitology Today 5, 344349.

STEWART, G. L., MANN, M. A., UBELAKER, J. E., MCCARTHY, J. L. & WOOD, B. G. (1988). A role for elevated plasma corticosterone in modulation of host response during infection with Trichinella pseudospiralis. Parasite Immunology 10, 139150.

SU, Z. & DOBSON, C. (1997). Genetic and immunological adaptation of Heligmosomoides polygyrus in mice. International Journal for Parasitology 27, 653663.

TANG, J., DOBSON, C. & MCMANUS, D. P. (1995). Antigens in phenotypes of Heligmosomoides polygyrus raised selectively from different strains of mice. International Journal for Parasitology 25, 847852.

TELFORD, G., WHEELER, D. J., APPLEBY, P., BOWEN, J. G. & PRITCHARD, D. I. (1998). Heligmosomoides polygyrus immunomodulatory factor (IMF), targets T-lymphocytes. Parasite Immunology 20, 601611.

VINEY, M. E. (2001). Diversity in populations of parasitic nematodes and its significance. In Parasitic Nematodes: Molecular Biochemistry and Immunology (ed. KENNEDY, M. W. & HARNETT, W.), pp. 83102. Wallingford, UK, CABI Publishing.

WAKELIN, D. (1973). The stimulation of immunity to Trichuris muris in mice exposed to low-level infections. Parasitology 66, 181189.

WAKELIN, D. & GOYAL, P. K. (1996). Trichinella isolates: parasite variability and host responses. International Journal for Parasitology 26, 471481.

WU, Z., NAGANO, I., POZIO, E. & TAKAHASHI, Y. (1999). Polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) for the identification of Trichinella isolates. Parasitology 118, 211218.

ZARLENGA, D. S., CHUTE, M. B., MARTIN, A. & KAPEL, C. M. O. (1999). A multiplex PCR for unequivocal differentiation of all encapsulated and non-encapsulated genotypes of Trichinella. International Journal for Parasitology 29, 18591867.

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