Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-23T04:08:22.808Z Has data issue: false hasContentIssue false
  • English
  • Français

The enigmatic presence of all gluconeogenic enzymes in Schistosoma mansoni adults

Published online by Cambridge University Press:  06 April 2009

A. G. M. Tielens ,
P. Van Der Meer ,
J. M. Van Den Heuvel  and
S. G. Van Den Bergh
A. G. M. Tielens
Affiliation:
Laboratory of Veterinary Biochemistry, Utrecht University, P.O. Box 80176, 3508 TD Utrecht, The Netherlands
P. Van Der Meer
Affiliation:
Department of Cardiology, University Hospital, Utrecht University, The Netherlands
J. M. Van Den Heuvel
Affiliation:
Laboratory of Veterinary Biochemistry, Utrecht University, P.O. Box 80176, 3508 TD Utrecht, The Netherlands
S. G. Van Den Bergh
Affiliation:
Laboratory of Veterinary Biochemistry, Utrecht University, P.O. Box 80176, 3508 TD Utrecht, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Summary

The activities of glucose-6-phosphatase (G6Pase), frucrose-1,6-bisphosphatase (FBPase), phosphoenolpyruvate carboxykinase (PEPCK) and pyruvate carboxylase (PC) were determined in homogenates of adult Schistosoma mansoni worms and compared with the activities in homogenates of rat liver and rat skeletal muscle, tissues with a high and a low gluconeogenic capacity, respectively. All four gluconeogenic enzymes were present in S. mansoni. The enzymes were less active than in rat liver, but the activities of G6Pase, PEPCK and PC were at least an order of magnitude higher than in rat skeletal muscle whereas FBPase was approximately equally active in S. mansoni and in rat muscle. Experiments with 14C-labelled substrates or [14C]NaHCO3 failed to demonstrate the actual occurrence of gluconeogenesis in S. mansoni. Some possible other functions of the gluconeogenic enzymes were investigated. Experiments with inhibitors of PEPCK gave no indications that this enzyme was involved in the degradation of glucose. This was confirmed by 13C-NMR experiments which indicated that lactate was formed from phosphoenolpyruvate via the actions of pyruvate kinase and lactate dehydrogenase, and that PEPCK did not participate in the formation of lactate. Substrate cycling between fructose-6-phosphate and fructose-1,6-bisphosphate was demonstrated to occur in adult S. mansoni. This shows that FBPase participates in the glucose metabolism of this parasite.

Keywords

Schistosoma mansonigluconeogenesisfutile cyclingsubstrate cycleserotoninglycogen
Type
Research Article
Information
Parasitology , Volume 102 , Issue 2 , April 1991 , pp. 267 - 276
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Barrett, J. (1981). Biochemistry of Parasitic Helminths. London: Macmillan.Google Scholar
Bensadoun, A. & Weinstein, D. (1976). Assay of proteins in the presence of interfering materials. Analytical Biochemistry 70, 241–50.Google Scholar
Bergmeyer, H. U., Grabl, M. & Walter, H. E. (1983). L-(+)-lactate dehydrogenase. In Methods of Enzymatic Analysis, 3rd edn, vol. 2 (ed. Bergmeyer, H. U.), pp. 232–233. Weinstein: Verlag Chemie.Google Scholar
Bryant, C. & Behm, C. A. (1989). Biochemical Adaptation in Parasites. London: Chapman & Hall.Google Scholar
Beuding, E. (1950). Carbohydrate metabolism of Schistosoma mansoni. Journal of General Physiology 33, 475–95.Google Scholar
Challiss, R. A. J., Arch, J. R. S., Crabtree, B. & Newsholme, E. A. (1984). Measurement of the rate of substrate cycling between fructose 6-phosphate and fructose 1,6-bisphosphate in skeletal muscle by using a single-isotope technique. The Biochemical Journal 233, 849–53.Google Scholar
Chambost, J. P. & Fraenkel, D. G. (1980). The use of 6-labeled glucose to assess futile cycling in Escherichia coli. Journal of Biological Chemistry 255, 2867–9.Google Scholar
Coles, G. C. (1973). Enzyme levels in cercariae and adult Schistosoma mansoni. Internal Journal for Parasitology 3, 505–10.Google Scholar
Duff, D. A. & Snell, K. (1982). Limitations of commonly used spectrophotometric assay methods for phosphoenolpyruvate carboxykinase in crude extracts of muscle. The Biochemical Journal 206, 147–52.CrossRefGoogle ScholarPubMed
Granner, D., Andreone, T., Sasaki, K. & Beale, E. (1983). Inhibition of transcription of the phosphoenolpyruvate carboxykinase gene by insulin. Nature, London 305, 549–51.Google Scholar
Hammerstedt, R. H. (1980). A rapid method for isolating glucose metabolites involved in substrate cycling. Analytical Biochemistry 109, 443–8.Google Scholar
Harder, A., Abbink, J., Andrews, P. & Thomas, H. (1987). Praziquantel impairs the ability of exogenous serotonin to stimulate carbohydrate metabolism in intact Schistosoma mansoni. Parasitology Research 73, 442–5.Google Scholar
Kane, H. J. & Bryant, C. (1984). 3-Mercaptopicolinic acid and energy metabolism in the liver fluke: Fasciola hepatica. International Journal for Parasitology 14, 383–9.Google Scholar
Karnovsky, M. L., Anchors, J. M. & Zoccoli, M. A. (1982). Glucose-6-phosphatase from cerebrum. In Methods in Enzymology, vol. 90 (ed. Wood, W. A.), pp. 396–402. New York: Academic Press.Google Scholar
Katz, J. & Rognstad, R. (1978). Futile cycling in glucose metabolism. Trends in Biochemical Sciences 3, 171–4.Google Scholar
KÖHLER, P. (1988). Nutrition and metabolism. In Parasitology in Focus (ed. Melhorn, H.) pp. 412–453. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Lamers, W. H., Hanson, R. W. & Meisner, H. M. (1982). cAMP stimulates transcription of the gene for cytosolic phosphoenolpyruvate carboxykinase in rat liver nuclei. Proceedings of the National Academy of Sciences, USA 79, 5137–41.Google Scholar
Lloyd, G. M. & Barrett, J. (1983). Fasciola hepatica: inhibition of phosphoenolpyruvate carboxykinase, and end-product formation by quinolinic acid and 3-mercaptopicolinic acid. Experimental Parasitology 56, 259–65.CrossRefGoogle ScholarPubMed
Loverde, P. T., Dewald, J. & Minchella, D. J. (1985). Further studies of genetic variation in Schistosoma mansoni. Journal of Parasitology 71, 732–4.CrossRefGoogle ScholarPubMed
Newgard, C. B., Hirsch, L. J., Foster, D. W. & McGarry, J. D. (1983). Studies on the mechanism by which exogenous glucose is converted into liver glycogen in the rat. A direct or an indirect pathway? Journal of Biological Chemistry 258, 8046–52.Google Scholar
Newsholme, E. A., Challiss, R. A. J. & Crabtree, B. (1984). Substrate cycles: their role in improving sensitivity in metabolic control. Trends in Biochemical Sciences 9, 277–80.Google Scholar
Newsholme, E. A. & Crabtree, B. (1970). The role of fructose-1,6-diphosphatase in the regulation of glycolysis in skeletal muscle. FEBS letters 7, 195–8.Google Scholar
Newsholme, E. A., Crabtree, B., Higgins, S. J., Thornton, S. D. & Start, C. (1972). The activities of fructose diphosphatase in flight muscles from the bumble-bee and the role of this enzyme in heat generation. The Biochemical Journal 128, 89–97.Google Scholar
Rahman, M. S. & Mettrick, D. F. (1985). Schistosoma mansoni: Effects of in vitro serotonin (5-HT) on aerobic and anaerobic carbohydrate metabolism. Experimental Parasitology 60, 10–17.CrossRefGoogle ScholarPubMed
Rognstad, R. & Katz, J. (1976). Effect of hormones and of ethanol on the fructose 6-P-fructose 1,6-P2 futile cycle during gluconeogenesis in the liver. Archives of Biochemistry and Biophysics 177, 337–45.Google Scholar
Rohrer, S. P., Saz, H. J. & Nowak, T. (1986). Purification and characterization of phosphoenolpyruvate carboxykinase from the parasitic helminth Ascaris suum. Journal of Biological Chemistry 261, 13049–55.Google Scholar
Rumjanek, F. D. (1987). Biochemistry and physiology. In The Biology of Schistosomes. From Genes to Latrines, (ed. Rollinson, D. & Simpson, A. J. G.), pp. 163–183. London: Academic Press.Google Scholar
Saz, H. J. (1981). Energy metabolism of parasitic helminths: adaptations to parasitism. Annual Reviews of Physiology 43, 323–41.Google Scholar
Scrutton, M. C., Olmsted, M. R. & Utter, M. F. (1969). Pyruvate carboxylase from chicken liver. In Methods in Enzymology, vol. 13 (ed. Lowenstein, J. M.), pp. 235–49. New York: Academic Press.Google Scholar
Senft, A. W. (1963). Observations on amino acid metabolism of Schistosoma mansoni in a chemically defined medium. Annals of the New York Academy of Sciences 113, 272–88.Google Scholar
Shapiro, T. A. & Talalay, P. (1982). Schistosoma mansoni: mechanisms in regulation of glycolysis. Experimental Parasitology 54, 379–90.Google Scholar
Shikama, H. & Ui, M. (1978). Glucose load diverts hepatic gluconeogenic product from glucose to glycogen in vivo. American Journal of Physiology 235, E354–360.Google Scholar
Tielens, A. G. M., Celik, C., Van Den Heuvel, J. M., Elfring, R. H. & Van Den Bergh, S. G. (1989 a). Synthesis and degradation of glycogen by Schistosoma mansoni worms in vitro. Parasitology 98, 67–73.Google Scholar
Tielens, A. G. M., Van Den Heuvel, J. M. & Van Den Bergh, S. G. (1987). Differences in intermediary energy metabolism between juvenile and adult Fasciola hepatica. Molecular and Biochemical Parasitology 24, 273–81.CrossRefGoogle ScholarPubMed
Tielens, A. G. M., Van Den Heuvel, J. M. & Van Den Bergh, S. G. (1990 a). Substrate cycling between glucose-6-phosphate and glycogen occurs in Schistosoma mansoni. Molecular and Biochemical Parasitology 39, 109–16.Google Scholar
Tielens, A. G. M., Van Den Heuvel, J. M. & Van Den Bergh, S. G. (1990 b). Continuous synthesis of glycogen by individual worm pairs of Schistosoma mansoni inside the veins of the final host. Molecular and Biochemical Parasitology 39, 195–202.Google Scholar
Tielens, A. G. M., Van Oordt, B. E. P, & Van Den Bergh, S. G. (1989 b). Carbohydrate metabolism in adult schistosomes of different strains and species. International Journal for Parasitology 19, 447–9.CrossRefGoogle ScholarPubMed
Tielens, A. G. M., Verwijs, A., Elfring, R. H., Van Den Heuvel, J. M. & Van Den Bergh, S. G. (1989 c). Schistosoma mansoni: rapid turnover of glycogen by adult worms in vivo. Experimental Parasitology 68, 235–7.Google Scholar
Ulm, E. H., Pogell, B. M., Demaine, M. M., Libby, C. B. & Benkovic, S. J. (1975). Fructose-1,6-diphosphatase from rabbit liver. In Methods in Enzymology, vol. 42 (ed. Wood, W. A.), pp. 369–74. New York: Academic Press.Google Scholar
Van Oordt, B. E. P. (1987). The energy metabolism of the blood fluke, Schistosoma mansoni. Ph.D. thesis, Utrecht, The Netherlands.Google Scholar
Van Oordt, B. E. P., Van Den Heuvel, J. M., Tielens, A. G. M. & Van Den Bergh, S. G. (1985). The energy metabolism of the adult Schistosoma mansoni is for a large part aerobic. Molecular and Biochemical Parasitology 16, 117–26.Google Scholar