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Biochemical and morphological pathology of the foot of the schistosome vector Biomphalaria glabrata infected with Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

S. N. Thompson
Affiliation:
Departments of Entomology and Chemistry, University of California, Riverside, California 92521, USA
R. W. K. Lee
Affiliation:
Departments of Entomology and Chemistry, University of California, Riverside, California 92521, USA
V. Mejia-Scales
Affiliation:
Departments of Entomology and Chemistry, University of California, Riverside, California 92521, USA
M. Shams El-Din
Affiliation:
Departments of Entomology and Chemistry, University of California, Riverside, California 92521, USA

Summary

Infection by Schistosoma mansoni resulted in morphological and biochemical changes to the foot of its intermediate host, Biomphalaria glabrata. Migration through, and emergence of cercariae from, the foot was observed and evidenced by lesions on the ciliated foot surface. This was accompanied by a significant decrease in the velocity of movement by infected individuals. In vivo31P NMR spectral analyses demonstrated that the foot of infected snails had a lower phosphoarginine (PA)/adenosine 5' triphosphate (ATP) ratio than that of uninfected controls. Moreover, kinetic experiments, employing saturation transfer, demonstrated the pseudo-first-order rate constant for the arginine kinase-catalysed exchange reaction in the forward direction, that is, PA→ATP was decreased by infection. The reverse reaction was not observed by the NMR methods used. PA was depleted upon exposure to hypoxic conditions suggesting its traditional role in preserving ATP level. Partly oxidized metabolic end-products were not observed in snails maintained under aerobic conditions, but succinate, propionate, acetate and lactate rapidly accumulated under hypoxic conditions.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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References

REFERENCES

Barrow, K. D., Jamieson, D. D. & Norton, R. S. (1980). 31P nuclear-magnetic-resonance studies of energy metabolism in tissue from the marine invertebrate Tapes watlingi. European Journal of Biochemistry 103, 289–97.CrossRefGoogle ScholarPubMed
Bayne, C. J. & Loker, E. S. (1987). Survival within the snail host. In The Biology of Schistosomes from Genes to Latrines (ed. Rollinson, D. & Simpson, A. J. G.), Pp. 321–46. New York: Academic Press.Google Scholar
Becker, w. (1980 a). Metabolic interrelationships of parasitic trematodes and molluscs, especially Schistosoma mansoni in Biomphalaria glabrata. Zeitschrift für Parasitenkunde 63, 101–11.CrossRefGoogle ScholarPubMed
Becker, w. (1980 b). Microcalorimetric studies in Biomphalaria glabrata: the influence of Schistosoma mansoni on the basal metabolism. Journal of Comparative Physiology 135B, 101–5.CrossRefGoogle Scholar
Bessman, S. P. & Geiger, P. J. (1981). Transport of energy in muscle: the phosphorylcreatine shuttle. Science 211, 448–52.CrossRefGoogle ScholarPubMed
Briggs, R. W., Radda, G. K. & Thulborn, K. R. (1985). 31P-NMR saturation transfer study of the in vivo kinetics of arginine kinase in Carcinus crab leg muscle. Biochimica et Biophysica Acta 845, 343–8.CrossRefGoogle Scholar
Butler, K. W., Deslauriers, R., Geoffrion, Y., Storey, J. M., Storey, K. B., Smith, I. C. P. & Somorjai, L. (1985). 31p nuclear magnetic resonance studies of crayfish (Orconectes virilis): the use of inversion spin transfer to monitor enzyme kinetics in vivo. European Journal of Biochemistry 149, 7983.CrossRefGoogle ScholarPubMed
Chernin, E. (1964). Maintenance in vitro of larval Schistosoma mansoni in tissues from the snail Australorbis glabratus. Journal of Parasitology 50, 531–45.CrossRefGoogle ScholarPubMed
Christen, R., Schackmann, R. W., Dahlquist, F. W. & Shapiro, B. M. (1983). 31P-NMR analysis of sea urchin sperm activation-reversible formation of high-energy phosphate compounds by changes in intracellular pH. Experimental Cell Research 149, 289–94.CrossRefGoogle Scholar
Copeland, M. (1919). Locomotion in two species of the gastropod genus Alectrion with observations on the behavior of pedal cilia. Biological Bulletin of the Marine Biological Laboratory 37, 126–38.CrossRefGoogle Scholar
Gade, G. & Grieshaber, M. K. (1986). Pyruvate reductases catalyze the formation of lactate and opines in anaerobic invertebrates. Comparative Biochemistry and Physiology 83B, 255–72.Google Scholar
Gadian, D. G. (1982). Nuclear Magnetic Resonance and its Applications to Living Systems. New York: Clarendon Press.Google Scholar
Gadian, D. G., Radda, G. K., Richards, R. E. & Seeley, P. J. (1979). 31P NMR in living tissue: the road from a promising to an important tool in biology. In Biological Applications of Magnetic Resonance (ed. Shulman, R. G.), New York, Academic Press.Google Scholar
Higashi, R. M., Fan, T. W.-M. & Macdonald, J. M. (1989). Monitoring the metabolic responses of intact Haliotis (abalones) under salinity stress by 31P surface probe localized NMR. Journal of Experimental Zoology 249, 350–6.CrossRefGoogle ScholarPubMed
Kassim, O. & Richards, C. S. (1979). Host reactions in Biomphalaria glabrata to Schistosoma mansoni miracidia, involving variations in parasite strains, numbers and sequence of exposures. International Journal for Parasitology 9, 565–70.CrossRefGoogle ScholarPubMed
Laukner, G. (1980). Diseases of Mollusca: Gastropoda. In Diseases of Marine Animals (ed Kinne, O.), Vol. 1, pp. 311424. New York: John Wiley.Google Scholar
Liebsch, M., Becker, W. & Gagelmann, G. (1978). An improvement of blood sampling technique for Biomphalaria glabrata using anesthesia and long-term relaxation and the role of this method in studies of the regulation of haemolymph glucose. Comparative Biochemistry and Physiology 59A, 169–74.CrossRefGoogle Scholar
Lipmann, F. (1977). Discovery of creatine phosphate in muscle. Trends in Biochemical Science 2, 21–2.CrossRefGoogle Scholar
Livingston, D. R. & De Zwaan, A. (1983). Carbohydrate metabolism of gastropods. In The Mollusca (ed. Wilbur, K. M.), Vol. 1, Metabolic Biochemistry and Molecular Biomechanics (ed. Hochahka, P. W.), pp. 177242. New York: Academic Press.Google Scholar
Macinis, A. J. & Voge, M. (1970). Experiments and Techniques in Parasitology. San Francisco: W. H. Freeman.Google Scholar
Malek, E. A. (1980). Trematodes and the molluscan hosts. In Snail-Transmitted Parasite Diseases, Vol. 1, pp. 1170. Boca Raton: CRC Press.Google Scholar
Malek, E. A. & Cheng, T. C. (1974). Parasite-induced pathology. In Medical and Economic Malacology, pp. 204–41. New York and London: Academic Press.Google Scholar
Miller, S. S. (1974). The classification, taxonomic distribution, and evolution of locomotor types among prosobranch gastropods. Proceedings of the Malacological Society of London 41, 233–71.Google Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–16.CrossRefGoogle Scholar
Pan, C.-T. (1965). Studies on the host-parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus. American Journal of Tropical Medicine and Hygiene 14, 931–76.CrossRefGoogle ScholarPubMed
Robitaille, P. A., Robitaille, P.-M. L. & Brown, G. G. (1986). 31P-NMR studies of Limulus polyphemus: Spermatozoa at rest and after motility. Journal of Experimental Zoology 238, 8998.CrossRefGoogle Scholar
Robitaille, P.-M. L., Robitaille, P. A., Martin, P. A. & Brown, G. G. (1987). Phosphorus-31 nuclear magnetic resonance studies of spermatozoa from the boar, ram, goat and bull. Comparative Biochemistry and Physiology 87B, 285–96.Google ScholarPubMed
Satir, P. (1974). How cilia move. Scientific American 231, 4463.Google ScholarPubMed
Schallig, H. D. F. H., Hordijk, P. L., Oosthoek, P. W. & De Jong-Brink, M. (1991). Schistosomin, a peptide present in the haemolymph of Lymnaea stagnalis infected with Trichobilharzia ocellata, is produced only in the snail's central nervous system. Parasitology Research 77, 152–6.CrossRefGoogle Scholar
Shoubridge, E. A. & Radda, G. K. (1984). A 31p nuclear magnetic resonance study of skeletal muscle metabolism in rats depleted of creatine with the analog β-guanidinopropionic acid. Biochimica et Biophysica Acta 805, 7988.CrossRefGoogle Scholar
Thompson, S. N. & Lee, R. W.-K. (1985). 31P NMR studies on adenylates and other phosphorus metabolites in the schistosome vector Biomphalaria glabrata. Journal of Parasitology 71, 652–61.CrossRefGoogle ScholarPubMed
Thompson, S. N. & Lee, R. W.-K. (1987). Characterization of the 31P NMR spectrum of the schistosome vector Biomphalaria glabrata and of the changes following infection by Schistosoma mansoni. Journal of Parasitology 73, 6476.CrossRefGoogle ScholarPubMed