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Influence of larval schistosomes on polysaccharide synthesis in albumin glands of Biomphalaria glabrata

Published online by Cambridge University Press:  06 April 2009

A. E. Crews  and
T. P. Yoshino
A. E. Crews
Affiliation:
University of Wisconsin–Madison, Department of Pathobiological Sciences, 2015 Linden Drive West, Madison, Wl 53706, USA
T. P. Yoshino
Affiliation:
University of Wisconsin–Madison, Department of Pathobiological Sciences, 2015 Linden Drive West, Madison, Wl 53706, USA
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Summary

An in vitro bioassay was used to examine [14C]glucose incorporation into polysaccharides in albumen glands (AGs) of susceptible M-line Biomphalaria glabrata infected with the NMRI strain of Schistosoma mansoni. Polysaccharide and galactogen synthesis were unaffected by larval trematode infection in AGs of snails at days 14, 21, and 28 post-infection (p.i.) when compared to uninfected controls. Further experiments were conducted to determine if daughter sporocysts, hypothesized to be primary mediators of parasitic castration in this system, were able to exert direct effects on synthetic activity of uninfected AGs via haemolymph-borne molecules or in vitro culture-generated larval excretory–secretory (ES) products. When AGs were incubated in the presence of infected snail haemolymph, significant differences in quantities of polysaccharides and galactogen were detected only in test organs incubated in day 28 p.i. haemolymph. Daughter sporocyst ES products generated during the first 48 h of culture caused a significant reduction in polysaccharide and galactogen synthesis in test organs. When ES products from days 3 to 6 of in vitro culture were tested similarly, no significant differences in either polysaccharide or galactogen synthesis were observed between control and test organs. These data demonstrate that daughter sporocysts are able to modulate a specific aspect of the reproductive activity of the snail host through haemolymph-borne molecules of host or parasite origin, or directly through in vitro culture-generated ES products.

Keywords

Schistosoma mansoniBiomphalaria glabratadaughter sporocystsalbumen glandexcretory–secretory productshaemolymphpolysaccharide synthesisgalactogen
Type
Research Article
Information
Parasitology , Volume 101 , Issue 3 , December 1990 , pp. 351 - 359
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Bayomy, M. F. F., van Elk, R. & Joosse, J. (1989). Infection of Lymnaea stagnalis with Trichobilharzia ocellata inhibits the growth, synthetic activity and dorsal body hormone response of the albumen gland. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C 92, 153–63.Google Scholar
Becker, W. (1980). Metabolic interrelationships of parasitic trematodes and molluscs, especially Schistosoma mansoni in Biomphalaria glabrata. Zeitschrift für Parasitenkunde 63, 101–11.CrossRefGoogle ScholarPubMed
Von Brand, T. & Files, V. S. (1947). Chemical and histological observations on the influence of Schistosoma mansoni infection on Australorbis glabratus. Journal of Parasitology 33, 476–82.CrossRefGoogle ScholarPubMed
Buma, P., Roubos, E. W. & Brunekreef, K. (1986). Role of cAMP in electrical and secretory activity in the neuroendocrine caudo-dorsal cells of Lymnaea stagnalis. Brain Research. 380, 26–33.CrossRefGoogle ScholarPubMed
Cheng, T. C. & Lee, F. O. (1971). Glucose levels in the mollusc Biomphalaria glabrata infected with Schistosoma mansoni. Journal of Invertebrate Pathology 18, 395–9.CrossRefGoogle ScholarPubMed
Christie, J. D., Foster, W. B. & Stauber, L. A. (1974 a). The effect of parasitism and starvation on carbohydrate reserves of Biomphalaria glabrata. Journal of Invertebrate Pathology 23, 55–62.CrossRefGoogle ScholarPubMed
Christie, J. D., Foster, W. B. & Stauber, L. A. (1974 b). 14C uptake by Schistosoma mansoni from Biomphalaria glabrata exposed to [14C]glucose. Journal of Invertebrate Pathology 23, 297–302.CrossRefGoogle Scholar
Crews, A. E. & Yoshino, T. P. (1989). Schistosoma mansoni: effect of infection on reproduction and gonadal growth in Biomphalaria glabrata. Experimental Parasitology 68, 326–34.CrossRefGoogle ScholarPubMed
Diconza, J. J. & Basch, P. F. (1974). Axenic cultivation of Schistosoma mansoni daughter sporocysts. Journal of Parasitology 60, 757–63.CrossRefGoogle ScholarPubMed
Dogterom, G. E. S., Bohlken, S. & Joosse, J. (1983). Effect of the photoperiod on the time schedule of egg mass production in Lymnaea stagnalis, as induced by ovulation hormone injections. General and Comparative Endocrinology 49, 255–60.CrossRefGoogle ScholarPubMed
van Elk, R. & Joosse, J. (1981). The UDP-galactose 4-epimerase of the albumen gland of Lymnaea stagnalis and the effects of photoperiod, starvation, and trematode infection on its activity. Comparative Biochemistry and Physiology 70B, 45–52.Google Scholar
Goudsmit, E. M. (1976). Galactogen catabolism by embryos of the freshwater snails, Bulimnaea megasoma and Lymnaea stagnalis. Comparative Biochemistry and Physiology 53B, 439–42.Google ScholarPubMed
Goudsmit, E. M. (1978). Calcium-dependent release of a neurochemical messenger from the brain of the land snail, Helix pomatia. Brain Research 151, 418–23.CrossRefGoogle ScholarPubMed
Goudsmit, E. M. & Friedman, T. B. (1976). Enzymatic synthesis and interconversion of UDP-D-glucose and UDP-D-galactose in the albumen gland of the snail, Helix pomatia. Comparative Biochemistry and Physiology 54B, 135–9.Google Scholar
Goudsmit, E. M. & Ram, J. L. (1982). Stimulation of Helix pomatia albumen gland galactogen synthesis by putative neurohormone (galactogenin) and by cyclic AMP analogues. Comparative Biochemistry and Physiology 71B, 417–422.Google Scholar
Hansen, E. L. (1976). A cell line from embryos of Biomphalaria glabrata (Pulmonata): establishment and characteristics. In Invertebrate Tissue Culture: Research Applications (ed. Maramorosch, K.), pp. 75–99. New York: Academic Press.CrossRefGoogle Scholar
Ishak, M. M., Mohamed, A. M. & Sharaf, A. A. (1975). Carbohydrate metabolism in uninfected and trematode-infected snails Biomphalaria alexandrina and Bulinus truncatus. Comparative Biochemistry and Physiology 51B, 499–505.Google ScholarPubMed
Dejong-Brink, M. (1973). The effects of dessication and starvation upon the weight, histology and ultrastructure of the reproductive tract of Biomphalaria glabrata, intermediate host of Schistosoma mansoni. Zeitschrift für Zellforschung 136, 229–62.CrossRefGoogle Scholar
Dejong-Brink, M. & Bergamin-Sasson, M. J. M. (1989). Trichobilharzia ocellata: influence of infection on the interaction between the dorsal body hormone, a female gonadotropic hormone, and the follicle cells in the gonad of the intermediate snail host Lymnaea stagnalis. Experimental Parasitology 68, 93–8.CrossRefGoogle Scholar
Dejong-Brink, M., Elsaadany, M. M. & Boer, H. H. (1988 a). Trichobilharzia ocellata: interference with endocrine control of female reproduction of Lymnaea stagnalis. Experimental Parasitology 65, 91–100.CrossRefGoogle Scholar
Dejong-Brink, M., Elsaadany, M. M. & Boer, H. H. (1988 b). Schistosomin, an antagonist of calfluxin. General and Comparative Endocrinology 65, 109–18.Google Scholar
Joosse, J. & van Elk, R. (1986). Trichobilharzia ocellata: physiological characterization of giant growth, glycogen depletion, and absence of reproductive activity in the intermediate snail host, Lymnaea stagnalis. Experimental Parasitology 62, 1–13.CrossRefGoogle ScholarPubMed
Joosse, J., van Elk, R., Mosselman, S., Wortelboer, H. & van Diepen, J. C. E. (1988). Schistosomin: a pronase-sensitive agent in the hemolymph of Trichobilharzia ocellata-infected Lymnaea stagnalis inhibits the activity of albumen glands in vitro. Parasitology Research 74, 228–34.CrossRefGoogle ScholarPubMed
Joosse, J. & Geraerts, W. P. M. (1983). Endocrinology. In The Mollusca, vol. 4 (ed. Saleuddin, A. S. M. & Wilbur, K. M.), pp. 317–406. New York: Academic Press.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, 853–62.CrossRefGoogle ScholarPubMed
Looker, D. L. & Etges, F. J. (1979). Effect of Schistosoma mansoni infection on fecundity and perivitelline fluid composition in Biomphalaria glabrata. Journal of Parasitology 65, 880–5.CrossRefGoogle ScholarPubMed
Meenakshi, V. R. & Scheer, B. T. (1969). Regulation of galactogen synthesis in the slug Ariolimax columbianis. Comparative Biochemistry and Physiology 29, 841–5.CrossRefGoogle Scholar
Miksys, S. & Saleuddin, A. S. M. (1985). The effect of the brain and dorsal bodies of Helisoma duryi (Mollusca: Pulmonata) on albumen gland synthetic activity in vitro. General and Comparative Endocrinology 60, 419–26CrossRefGoogle ScholarPubMed
van Minnen, J., Wijdenes, J. & Sokolove, P. G. (1983). Endocrine control of galactogen synthesis in the albumen gland of the slug. Limax maximus. General and Comparative Endocrinology 49, 307–14.CrossRefGoogle ScholarPubMed
Nolan, L. E. & Carriker, J. P. (1946). Observations on the biology of the snail Lymnaea stagnalis appressa during twenty years of laboratory culture. American Midland Naturalist 36, 467–493.CrossRefGoogle Scholar
Plesch, B., Dejong-Brink, M. & Boer, H. H. (1971). Histological and histochemical observations on the reproductive tract of the hermaphrodite snail Lymnaea stagnalis (L.). Netherlands Journal of Zoology 21, 180–201.Google Scholar
Rupprecht, H., Becker, W. & Schwanbek, A. (1989). Alterations in hemolymph components in Biomphalaria glabrata during long-term infections with Schistosoma mansoni. Parasitology Research 75, 233–7.CrossRefGoogle Scholar
Schwartz, C. F. & Carter, C. E. (1982). Effect of Schistosoma mansoni on glycogen synthase and phosphorylase from Biomphalaria glabrata (Mollusca). Journal of Parasitology 68, 236–42.CrossRefGoogle ScholarPubMed
Stanislawski, E. & Becker, W. (1979). Alterations of the free amino acid content in the hemolymph of Biomphalaria glabrata (Pulmonata) in starvation and after infection with Schistosoma mansoni (Trematoda). Comparative Biochemistry and Physiology 63B, 477–82.Google ScholarPubMed
Thomas, J. A., Schlender, K. K. & Larner, L. (1968). A rapid filter paper assay for UDP-glucose-glycogen glucosyltransferase including an improved biosynthesis of UDP-14C-glucose. Analytical Biochemistry 25, 486–99.CrossRefGoogle Scholar
Veldhuijzen, J. P. & Cuperus, R. (1976). Effects of starvation, low temperature and the dorsal body hormone on the in vitro synthesis of galactogen and glycogen in the albumen gland and the mantle of the pond snail Lymnaea stagnalis. Netherlands Journal of Zoology 26, 119–35.Google Scholar
Wijdenes, J., van Elk, R. & Joosse, J. (1983). Effects of two gonadotropic hormones on polysaccharide synthesis in the albumen gland of Lymnaea stagnalis, studied with the organ culture technique. General and Comparative Endocrinology 51, 263–71.CrossRefGoogle ScholarPubMed
Wijsman, T. C. M. & Wijck-Batenburg, H. (1987). Biochemical composition of the eggs of the freshwater snail Lymnaea stagnalis and oviposition-induced restoration of albumen gland secretion. International Journal for Invertebrate Reproduction and Development 12, 199–212.CrossRefGoogle Scholar
Yoshino, T. P. (1981). Comparison of concanavalin A-reactive determinants on haemocytes of Biomphalaria glabrata snail stocks: receptor binding and redistribution. Developmental and Comparative Immunology 6, 451–61.CrossRefGoogle Scholar
Yoshino, T. P. & Lodes, M. J. (1988). Secretory protein biosynthesis in snail haemocytes: in vitro modulation by larval schistosome excretory–secretory products. Journal of Parasitology 74, 538–47.CrossRefGoogle Scholar
Yoshino, T. P., Cheng, T. C. & Renwrantz, L. R. (1977). Lectin and human blood group determinants of Schistosoma mansoni: alterations following in vitro transformation of miracidium to mother sporocyst. Journal of Parasitology 63, 818–24.CrossRefGoogle ScholarPubMed