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Refractoriness of host haemocytes to parasite immunosuppressive factors as a putative resistance mechanism in the Biomphalaria glabrataEchinostoma caproni system

Published online by Cambridge University Press:  12 July 2001

E. HUMBERT
Affiliation:
Centre de Biologie et d'Ecologie, UMR 5555 du CNRS, 52 Ave de Villeneuve, Université de Perpignan, 66860 Perpignan cedex, France
C. COUSTAU
Affiliation:
Centre de Biologie et d'Ecologie, UMR 5555 du CNRS, 52 Ave de Villeneuve, Université de Perpignan, 66860 Perpignan cedex, France

Abstract

In contrast to the growing knowledge accumulated on plant resistance to pathogens, mechanisms of parasite resistance largely remain to be elucidated in animal species. In the present study we investigated mechanisms underlying resistance/susceptibility in the snail–trematode system Biomphalaria glabrataEchinostoma caproni. In particular, we compared the effect of the parasite excretory–secretory (E–S) products on the defence functions of haemocytes from 2 susceptible and 2 resistant snail strains. In vitro experiments showed that E. caproni E–S products inhibit adhesion and phagocytosis of haemocytes from susceptible snails. A partial biochemical characterization also suggested that the interfering factor(s) is (are) heat-labile glycosylated polypeptides of molecular mass between 10 and 30 kDa. Interestingly, haemocytes from resistant snails remained unaffected by the parasite E–S products, suggesting that a constitutive difference results in their refractoriness to the parasite's immunosuppressive factor(s).

Type
Research Article
Copyright
© 2001 Cambridge University Press

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References

ADEMA, C. M., ARGUELLO, D. F. II, STRICKER, S. A. & LOKER, E. S. (1994). A time-lapse study of interactions between Echinostoma paraensei intramolluscan larval stages and adherent haemocytes from Biomphalaria glabrata and Helix aspersa. Journal of Parasitology 80, 719727.CrossRefGoogle Scholar
ADEMA, C. M., HERTEL, L. A., MILLER, R. D. & LOKER, E. S. (1997). A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proceedings of the National Academy of Sciences, USA 94, 86918696.CrossRefGoogle Scholar
ADEMA, C. M. & LOKER, E. S. (1997). Specificity and immunobiology of larval digenean-snail associations. In Advances in Trematode Biology (ed. FRIED, B. & GRACZYK, T. K.), pp. 229263. CRC Press, Boca Raton.
ANTONOVICS, J. & THRALL, P. (1994). The cost of resistance and the maintenance of genetic polymorphism in host–pathogen systems. Proceedings of the Royal Society of London, B 257, 105110.CrossRefGoogle Scholar
ATAEV, G. L. & COUSTAU, C. (1999). Cellular response to Echinostoma caproni infection in Biomphalaria glabrata strains selected for susceptibility/resistance. Developmental and Comparative Immunology 23, 187198.CrossRefGoogle Scholar
CHERNIN, E. (1963). Observations on hearts explanted in vitro from the snail Australobis glabratus. Journal of Parasitology 49, 353364.CrossRefGoogle Scholar
COOPER, E. L., RINKEVICH, B., UHLENBRUCK, G. & VALEMBOIS, P. (1992). Invertebrate immunity: another viewpoint. Scandinavian Journal of Immunology 35, 247266.CrossRefGoogle Scholar
COUSTAU, C. & YOSHINO, T. P. (1994a). Schistosoma mansoni: modulation of hemocyte surface polypeptides detected in individual snails, Biomphalaria glabrata, following larval exposure. Experimental Parasitology 79, 110.Google Scholar
COUSTAU, C. & YOSHINO, T. P. (1994b). Surface membrane polypeptides associated with hemocytes from Schistosoma mansoni-susceptible and -resistant strains of Biomphalaria glabrata (Gastropoda). Journal of Invertebrate Pathology 63, 8289.Google Scholar
COUSTAU, C., CHEVILLON, C. & FFRENCH-CONSTANT, R. (2000). Resistance to xenobiotics and parasites: can we count the cost? Trends in Ecology and Evolution 15, 378383.Google Scholar
DAVIDS, B. J. & YOSHINO, T. P. (1998). Integrin-like RGD-dependent binding mechanism involved in the spreading response of circulating molluscan phagocytes. Developmental and Comparative Immunology 22, 3953.CrossRefGoogle Scholar
DAVIDS, B. J., WU, X.-J. & YOSHINO, T. P. (1999). Cloning of a β integrin subunit cDNA from an embryonic cell line derived from the freshwater mollusc, Biomphalaria glabrata. Gene 228, 213223.CrossRefGoogle Scholar
DEGAFFE, G. & LOKER, E. S. (1998). Susceptibility of Biomphalaria glabrata to infection with Echinostoma paraensei: Correlation with the effect of parasite secretory-excretory products on host hemocyte spreading. Journal of Invertebrate Pathology 71, 6472.CrossRefGoogle Scholar
DEMPSEY, M. A., SILVA, H. & KLESSIG, D. F. (1998). Engineering disease and pest resistance in plants. Trends in Microbiology 6, 5461.CrossRefGoogle Scholar
DUCLERMORTIER, P., LARDANS, V., SERRA, E., TROTTEIN, F. & DISSOUS, C. (1999). Biomphalaria glabrata embryonic (Bge) cells express a protein with a domain homologous to the lectin domain of mammalian selectins. Parasitology Research 85, 481486.CrossRefGoogle Scholar
ELLIS, S. & MELLOR, H. (2000). Regulation of endocytic traffic by rho family GTPases. Trends in Cell Biology 10, 8588.CrossRefGoogle Scholar
FRANK, S. A. (1996). Statistical properties of polymorphism in host-parasite genetics. Evolutionary Ecology 10, 307317.CrossRefGoogle Scholar
GRANATH, W. O. JR, CONNORS, V. A. & TARLETON, R. L. (1994). Interleukin 1 activity in haemolymph from strains of the snail Biomphalaria glabrata varying in susceptibility to the human blood fluke, Schistosoma mansoni: presence, differential expression, and biological function. Cytokine 6, 2127.CrossRefGoogle Scholar
HALTERMAN, D. A. & MARTIN, G. B. (1997). Signal recognition and transduction involved in plant disease resistance. Essays in Biochemistry 32, 8789.Google Scholar
JEYARASASINGAM, U., HEYNEMAN, D., LIM, H. K. & MANSOUR, N. (1972). Life cycle of a new echinostome from Egypt, Echinostoma liei sp. nov. (Trematoda: Echinostomatidae). Parasitology 65, 203222.Google Scholar
KRAAIJEVELD, A. R., VAN ALPHEN, J. J. & GODFRAY, H. C. (1998). The coevolution of host resistance and parasitoid virulence. Parasitology 116 (Suppl.), S29S45.CrossRefGoogle Scholar
LANGAND, J., JOURDANE, J., COUSTAU, C., DELAY, B. & MORAND, S. (1998). Cost of resistance, expressed as a delayed maturity, detected in the host-parasite system Biomphalaria glabrata/Echinostoma caproni. Heredity 80, 320325.CrossRefGoogle Scholar
LIE, K. J. (1982). Survival of Schistosoma mansoni and other trematode larvae in the snail Biomphalaria glabrata. A discussion of the interference theory. Tropical and Geographical Medicine 34, 111122.Google Scholar
LIE, K. J. & HEINEMAN, D. (1977). Studies on resistance in snails: Interference by nonirradiated echinostome larvae with natural resistance to Schistosoma mansoni in Biomphalaria glabrata. Journal of Invertebrate Pathology 29, 118125.CrossRefGoogle Scholar
LIGHTOWLERS, M. W. & RICKARD, M. D. (1988). Excretory–secretory products of helminth parasites: effects on host immune responses. Parasitology 96 (Suppl.), S123S166.CrossRefGoogle Scholar
LODES, M. J. & YOSHINO, T. P. (1989). Characterization of excretory-secretory proteins synthesized in vitro by Schistosoma mansoni primary sporocysts. Journal of Parasitology 75, 853862.CrossRefGoogle Scholar
LOKER, E. S., CIMINO, D. F. & HERTEL, L. A. (1992). Excretory–secretory products of Echinostoma paraensei sporocysts mediate interference with Biomphalaria glabrata hemocyte functions. Journal of Parasitology 78, 104115.CrossRefGoogle Scholar
MOORE, D. V., THILLET, G. J., CARNEY, D. M. & MELENEY, H. E. (1953). Experimental infection of Bulinus truncatus with Schistosoma haematobium. Journal of Parasitology 39, 215221.CrossRefGoogle Scholar
OWE-MISSI-OUKEM-BOYER, O., PORCHET, E., CAPRON, A. & DISSOUS, C. (1994). Characterization of immunoreactive TNFα molecules in the gastropod Biomphalaria glabrata. Developmental and Comparative Immunology 18, 211218.CrossRefGoogle Scholar
PASTRANA, D. V., RAGHAVAN, N., FITZGERALD, P., EISINGER, S. W., METZ, C., BUCALA, R., SCHLEIMER, R. P., BICKEL, C. & SCOTT, A. L. (1998). Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor. Infection and Immunity 66, 59555963.Google Scholar
REDDY, A. & FRIED, B. (1996). Egg laying in vitro of Echinostoma caproni (Trematoda) in nutritive and nonnutritive media. Parasitology Research 82, 475476.CrossRefGoogle Scholar
RIBEIRO, C., DUVIC, B., OLIVEIRA, P., GIVAUDAN, A., PALHA, F., SIMOES, N. & BREHÉLIN, M. (1999). Insect immunity-effects of factors produced by a nematobacterial complex on immunocompetent cells. Journal of Insect Physiology 45, 677685.CrossRefGoogle Scholar
RICHARDS, C. S., KNIGHT, M. & LEWIS, F. A. (1992). Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitology Today 8, 171174.CrossRefGoogle Scholar
SIMMS, E. L. & FRITZ, R. S. (1990). The ecology and evolution of host-plant resistance to insects. Trends in Ecology and Evolution 5, 356360.CrossRefGoogle Scholar
SMINIA, T. & BARENDSEN, L. (1980). A comparative morphological and enzyme histochemical study on blood cells of the freshwater snails Lymnaea stagnicola, Biomphalaria glabrata, and Bulinus truncatus. Journal of Morphology 165, 3139.CrossRefGoogle Scholar
SORCI, G., MOLLER, A. P. & BOULINIER, T. (1997). Genetics of host-parasite interactions. Trends in Ecology and Evolution 12, 196200.CrossRefGoogle Scholar
STEAR, M. J. & WAKELIN, D. (1998). Genetic resistance to parasitic infection. Revue Scientifique et Technique O. I. E. (Office International des Epizooties) 17, 143153.CrossRefGoogle Scholar
TROUVÉ, S., RENAUD, F., DURAND, P. & JOURDANE, J. (1996). Selfing and outcrossing in a parasitic hermaphrodite helminth (Trematoda, Echinostomatidae). Heredity 77, 18.CrossRefGoogle Scholar
UCHIKAWA, R. & LOKER, E. S. (1992). Echinostoma paraensei and Schistosoma mansoni: Adherence of unaltered or modified latex beads to hemocytes of the host snail Biomphalaria glabrata. Experimental Parasitology 75, 223232.CrossRefGoogle Scholar
VAN DER KNAAP, W. P. W. & LOKER, E. S. (1990). Immune mechanisms in trematode–snail interactions. Parasitology Today 6, 175190.CrossRefGoogle Scholar
VILCINSKAS, A. & GÖTZ, P. (1999). Parasitic fungi and their interactions with the insect immune system. Advances in Parasitology 43, 267313.CrossRefGoogle Scholar