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Elevated agglutination titres in plasma of Biomphalaria glabrata exposed to Echinostoma paraensei: characterization and functional relevance of a trematode-induced response

Published online by Cambridge University Press:  06 April 2009

E. S. Loker ,
L. Couch  and
L. A. Hertel
E. S. Loker
Affiliation:
Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA
L. Couch
Affiliation:
Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA
L. A. Hertel
Affiliation:
Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA
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Summary

Production of elevated haemolymph agglutination titres by Biomphalaria glabrata following exposure to Echinostoma paraensei miracidia was investigated, to characterize this parasite-induced response and to understand its functional relevance. Both the dose of infection (1, 10 or 100 miracidia per snail) or the number of separate exposures to infection (between one and three, over a 4 or 8 day interval) were varied, and assuming a threshold dosage (10 miracidia per snail or higher) was exceeded, titres of juvenile snails peaked at 8–16 times the values for unexposed control snails, regardless of the exposure regimen. Adult snails, which are relatively refractory to infection, have slightly higher resting titres than juveniles, but exhibit only a 2- to 4-fold increase in titre following exposure. Juveniles exposed to infection but lacking demonstrable infection had lower titres than snails with confirmed infections. Exposure to infection increased heterogeneity of plasma agglutinins and provoked production of unique specificities not found in unexposed snails. However, the overall pattern of agglutination responses for snails with successfully developed parasites did not differ from those in which parasite development was unsuccessful. Agglutinating activity was inhibitable by several different monosaccharides, although plasma from infected snails was relatively unaffected by N-acetyl-glucosamine or N-acetyl-galactosamine. Wounding of snails provoked no change in plasma agglutination activity. As the highest agglutination titres were produced in snails with successfully developing parasites and agglutinin composition did not differ between snails with successful or unsuccessful parasites, the functional relevance of the response remains enigmatic. The production of unique agglutinins following exposure deserves additional study.

Keywords

Biomphalaria glabrataGastropodaMolluscaEchinostoma paraenseiTrematodaagglutinationimmunobiologyhumoral response
Type
Research Article
Information
Parasitology , Volume 108 , Issue 1 , January 1994 , pp. 17 - 26
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Boswell, C. A. & Bayne, C. J. (1984). Isolation, characterization and functional assessment of a hemagglutinin from the plasma of Biomphalaria glabrata, intermediate host of Schistosoma mansoni. Developmental and Comparative Immunology 8, 559–68.CrossRefGoogle ScholarPubMed
Couch, L., Hertel, L. A. & Loker, E. S. (1990). Humoral response of the snail Biomphalaria glabrata to trematode infection: observations on a circulating hemagglutinin. Journal of Experimental Zoology 255, 340–9.CrossRefGoogle ScholarPubMed
Fryer, S. E. & Bayne, C. J. (1989). Opsonization of yeast by the plasma of Biomphalaria glabrata (Gastropoda): a strain-specific and time-dependent process. Parasite Immunology 11, 269–78.CrossRefGoogle ScholarPubMed
Fryer, S. E., Hull, C. J. & Bayne, C. J. (1989). Phagocytosis of yeast by Biomphalaria glabrata: carbohydrate specificity of hemocyte receptors and a plasma opsonin. Developmental and Comparative Immunology 13, 9–16.CrossRefGoogle Scholar
Jeong, K. H., Sussman, S. D., Rosen, K. J. & Heyneman, D. (1981). Distribution and variation of hemagglutinating activity in the hemolymph of Biomphalaria glabrata. Journal of Invertebrate Pathology 38, 256–63.CrossRefGoogle ScholarPubMed
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, 104–15.CrossRefGoogle ScholarPubMed
Loker, E. S., Cimino, D. F., Stryker, G. A. & Hertel, L. A. (1987). The effect of size of M line Biomphalaria glabrata on the course of development of Echinostoma paraensei. Journal of Parasitology 73, 1090–8.CrossRefGoogle ScholarPubMed
Loker, E. S. & Hertel, L. A. (1987). Alterations in Biomphalaria glabrata plasma induced by infection with the digenetic trematode Echinostoma paraensei. Journal of Parasitology 73, 503–13.CrossRefGoogle ScholarPubMed
Monroy, F. G., Hertel, L. A. & Loker, E. S. (1992). Carbohydrate-binding plasma proteins from the gastropod Biomphalaria glabrata: effects of strain and trematode infection. Developmental and Comparative Immunology 16, 355–66.CrossRefGoogle ScholarPubMed
Mounkassa, J. B. & Jourdane, J. (1990). Dynamics of the leukocytic response of Biomphalaria glabrata during the larval development of Schistosoma mansoni and Echinostoma liei. Journal of Invertebrate Pathology 55, 306–11.CrossRefGoogle ScholarPubMed
Mullainadhan, P. & Renwrantz, L. (1989). Comparative analysis of agglutinins from hemolymph and albumin gland of Helix pomatia. Journal of Comparative Physiology 159, 443–52.CrossRefGoogle ScholarPubMed
Olafsen, J. A. (1986). Invertebrate lectins: biochemical heterogeneity as a possible key to their biological function. In Immunity in Invertebrates: Cells, Molecules and Defense Reactions (ed. Brehelin, M.), pp. 94–111. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Renwrantz, L. (1983). Involvement of agglutinins (lectins) in invertebrate defense reactions: the immunobiological importance of carbohydrate-specific binding molecules. Developmental and Comparative Immunology 7, 2603–8.CrossRefGoogle Scholar
Renwrantz, L. (1986). Lectins in molluscs and arthropods: their occurrence, origin and roles in immunity. Symposium of the Zoological Society of London 56, 81–93.Google Scholar
Spray, F. J. & Granath, W. O. Jr, (1990). Differential binding of hemolymph proteins from schistosome-resistant and -susceptible Biomphalaria glabrata to Schistosoma mansoni sporocysts. Journal of Parasitology 76, 225–9.CrossRefGoogle ScholarPubMed
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, 223–32.CrossRefGoogle ScholarPubMed
van der Knaap, W. P. W., Boerrigter-Barendsen, L. H., van den Hoeven, D. S. P. & Sminia, T. (1981). Immunocytochemical demonstration of a humoral defence factor in blood cells (amoebocytes) of the pond snail, Lymnaea stagnalis. Cell and Tissue Research 219, 291–6.CrossRefGoogle ScholarPubMed
van der Knaap, W. P. W., Meuleman, E. A. & Sminia, T. (1987). Alterations in the internal defense system of the pond snail Lymnaea stagnalis induced by infection with the schistosome Trichobilharzia ocellata. Parasitology Research 73, 57–65.CrossRefGoogle ScholarPubMed
Vasta, G. R. & Marchalonis, J. J. (1987). Invertebrate agglutinins and the evolution of humoral and cellular recognition factors. In Invertebrate Models: Cell Receptors and Cell Communication (ed. Greenberg, A. H.), pp. 104–117. Basel: Karger.Google Scholar
Yang, R. & Yoshino, T. P. (1990 a). Immunorecognition in the freshwater bivalve, Corbicula fluminea. I. Electrophoretic and immunologic analyses of opsonic plasma components. Developmental and Comparative Immunology 14, 385–95.CrossRefGoogle ScholarPubMed
Yang, R. & Yoshino, T. P. (1990 b). Immunorecognition in the freshwater bivalve, Corbicula fluminea. II. Isolation and characterization of a plasma opsonin with hemagglutinating activity. Developmental and Comparative Immunology 14, 397–404.CrossRefGoogle ScholarPubMed
Zar, J. H. (1984). Biostatistical Analysis, 2nd Edn.Englewood Cliffs, New Jersey: Prentice-Hall.Google Scholar