Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T00:36:50.817Z Has data issue: false hasContentIssue false
  • English
  • Français

Intermediary carbohydrate metabolism in protoscoleces of Echinococcus granulosus (horse and sheep strains) and E. multilocularis

Published online by Cambridge University Press:  06 April 2009

D. P. McManus  and
J. D. Smyth
D. P. McManus
Affiliation:
Department of Zoology and Applied Entomology, Imperial College of Science and Technology, London SW7 2BB
J. D. Smyth
Affiliation:
Department of Zoology and Applied Entomology, Imperial College of Science and Technology, London SW7 2BB
Get access Rights & Permissions [Opens in a new window]

Summary

With few exceptions, the specific activities of the glycolytic enzymes and the steady-state content of glycolytic and associated intermediates in protoscoleces of the horse (E.g.H) and sheep (E.g.S) strains of Echinococcus granulosus and the closely related E. multilocularis (E.m.) are very similar. Phosphorylase, hexokinase, phosphofructokinase and pyruvate kinase catalyse non-equilibrium reactions and the patterns of activity for pyruvate kinase, phosphoenolpyruvate carboxykinase and malic enzyme are similar in the three organisms. The levels of tricarboxylic acid cycle intermediates in E.g.H., E.g.S. and E.m. are of the same order as those reported in tissues with an active cycle. Each has a complete sequence of cycle enzymes but there are substantial differences between the three parasites with regard to the activity of individual enzymes, The activities of NAD and NADP-linked isocitrate dehydrogenases are significantly lower in E.g.H. than in E.g.S. and particularly in E.m. which suggests that the tricarboxylic acid cycle may play a more important role in carbohydrate metabolism and energy production in the latter parasites. Nevertheless, the three organisms utilize fermentative pathways for alternative energy production, fix carbon dioxide via phosphoenolpyruvate carboxykinase and have a partial reversed tricarboxylic acid cycle. It is speculated that in vivo more carbon will be channelled towards oxaloacetate than pyruvate at the phosphoenolpyruvate branch point. The steady state content of ATP and the ATP/AMP ratios are low in the three organisms, suggesting a low rate of ATP utilization in each.

Type
Research Article
Information
Parasitology , Volume 84 , Issue 2 , April 1982 , pp. 351 - 366
Copyright
Copyright © Cambridge University Press 1982

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

Agosin, M. (1957). Studies on the metabolism of Echinococcus granulosus. II. Some observations on the carbohydrate metabolism of hydatid cyst scolices. Experimental Parasitology 6, 586–93.CrossRefGoogle Scholar
Agosin, M. & Aravena, L. (1959). Studies on the metabolism of Echinococcus granulosus. III. Glycolysis with special reference to hexokinases and related glycolytic enzymes. Biochimica et biophysica acta 34, 90–102.CrossRefGoogle Scholar
Agosin, M. & Aravena, L. (1960 a). Studies on the metabolism of Echinococcus granulosus. IV. Enzymes of the pentose phosphate pathway. Experimental Parasitology 10, 28–38.CrossRefGoogle Scholar
Agosin, M. & Aravena, L. (1960 b). Studies on the metabolism of Echinococcus granulosus. V. The phosphopentose isomerase of hydatid cyst scolices. Enzymologia 22, 281–94.Google Scholar
Agosin, M., von Brand, T., Rivera, G. F. & McMahon, P. (1957). Studies on the metabolism of Echinococcus granulosus. I. General chemical composition and respiratory reactions. Experimental Parasitology 6, 37–51.CrossRefGoogle Scholar
Agosin, M. & Repetto, Y. (1962). Studies on the metabolism of Echinococcus granulosus. VI. Pathways of glucose C14 metabolism in Echinococcus granulosus scolices. Biologica 32, 33–8.Google Scholar
Agosin, M. & Repetto, Y. (1963). Studies on the metabolism of Echinococcus granulosus. VII. Reactions of the tricarboxylic acid cycle in E. granulosus scolices. Comparative Biochemistry and Physiology 8, 245–61.CrossRefGoogle Scholar
Agosin, M. & Repetto, Y. (1965). Studies on the metabolism of Echinococcus granulosus. VIII. The pathway to succinate in E. granulosus scolices. Comparative Biochemistry and Physiology 14, 299–309.CrossRefGoogle Scholar
Alp, P. R., Newsholme, E. A. & Zammit, V. A. (1976). Activities of citrate synthase and NAD+-linked and NADP+-linked isocitrate dehydrogenase in muscle from vertebrates and invertebrates. The Biochemical Journal 154, 689–700.CrossRefGoogle ScholarPubMed
Barrett, J. (1981). Biochemistry of Parasitic Helmin hs. London and Basingstoke: Macmillan.CrossRefGoogle Scholar
Barrett, J. & Beis, I. (1973). Studies on glycolysis in the muscle tissue of Ascaris lumbricoides (Nematoda). Comparative Biochemistry and Physiology 44B, 751–62.Google ScholarPubMed
Behm, C. A. & Bryant, C. (1975). Studies of regulatory metabolism in Moniezia expansa: general considerations. International Journal for Parasitology 5, 209–17.CrossRefGoogle ScholarPubMed
Behm, C. A. & Bryant, C. (1980). Regulatory properties of a partially purified preparation of pyruvate kinase from Fasciola hepatica. International Journal for Parasitology 10, 107–14.CrossRefGoogle ScholarPubMed
Beis, I. & Barrett, J. (1979). The contents of adenine nucleotides and glycolytic and tricarboxylic acid cycle intermediates in activated and non-activated plerocercoids of Schistocephalus solidus (Cestoda: Pseudophylidea). International Journal for Parasitology 9, 465–8.CrossRefGoogle Scholar
Beis, I. & Newsholme, E. A. (1975). The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. The Biochemical Journal 152, 23–32.CrossRefGoogle ScholarPubMed
Bergmeyer, H. U. (1974). Methods of Enzymatic Analysis, 2nd ed.New York and London: Academic Press.Google Scholar
von Brand, T. (1952). Chemical Physiology of Endoparasitic Animals. New York: Academic Press.Google Scholar
von Brand, T. (1979). Biochemistry and Physiology of Endoparasites. Amsterdam, New York and Oxford: Elsevier/North Holland Biomedical Press.Google Scholar
Bryant, C. (1972). Metabolic regulation in Moniezia expansa (Cestoda): the role of pyruvate kinase. International Journal for Parasitology 2, 333–40.CrossRefGoogle ScholarPubMed
Bryant, C. (1978). The regulation of respiratory metabolism in parasitic helminths. Advances in Parasitology 16, 311–31.CrossRefGoogle ScholarPubMed
Carter, C. & Fairbairn, D. (1975). Multienzymatic nature of pyruvate kinase during development of Hymenolepis diminuta (Cestoda). Journal of Experimental Zoology 194, 439–48.CrossRefGoogle Scholar
Cornish, R. A. & Bryant, C. (1976). The metabolic integrity of Fasciola hepatica during in vitro maintenance. International Journal for Parasitology 6, 387–92.CrossRefGoogle ScholarPubMed
Crabtree, B. & Newsholme, E. A. (1972). The activities of phosphorylase hexokinase, phosphofructokinase, lactate dehydrogenase and the glycerol 3-phosphate dehydrogenases in muscles from vertebrates and invertebrates. The Biochemical Journal 126, 49–58.CrossRefGoogle ScholarPubMed
Dicowsky, L., Repetto, Y. & Agosin, M. (1968). Studies of the metabolism of Echinococcus granulosus. X. The mechanism of production of volatile fatty acids. Comparative Biochemistry and Physiology 24, 763–72.CrossRefGoogle Scholar
Farhan, I., Schwabe, C. W. & Zobel, C. R. (1959). Host-parasite relationships in echinococcosis. III. Relation of environmental oxygen tension to the metabolism of hydatid scolices. American Journal of Tropical Medicine and Hygiene 8, 473–8.CrossRefGoogle Scholar
Frayha, G. J. & Haddad, R. (1980). Comparative chemical composition of protoscolices and hydatid cyst fluid of Echinococcus granulosus (Cestoda). International Journal for Parasitology 10, 359–64.CrossRefGoogle ScholarPubMed
Gabbott, P. A. (1976). Energy metabolism. In Marine Mussels: their Ecology and Physiology (ed.Bayne, B. L.), pp. 293–355. Cambridge, London, New York and Melbourne: Cambridge University Press.Google Scholar
Hochachka, P. W. (1980). Living without Oxygen, Closed and Open Systems in Hypoxia Tolerance. Harvard: Harvard University Press.CrossRefGoogle Scholar
Hoffmann, K. H., Mustafa, T. & Jorgensen, J. B. (1979). Role of pyruvate kinase, phosphoenolpyruvate carboxykinase, malic enzyme and lactate dehydrogenase in anaerobic energy metabolism of Tubifex spec. Journal of Comparative Physiology 130, 337–45.CrossRefGoogle Scholar
Hollman, S. (1964). Non-glycolytic Pathways of Metabolism of Glucose. New York and London: Academic Press.Google Scholar
Ivanovici, A. M. (1980). The adenylate energy charge in the estuarine mollusc, Pyrazus ebeninus. Laboratory studies of responses to salinity and temperature. Comparative Biochemistry and Physiology 66A, 43–55.CrossRefGoogle Scholar
Köhler, P. & Hanselmann, K. (1974). Anaerobic and aerobic energy metabolism in the larvae (Tetrathyridia) of Mesocestoides corti. Experimental Parasitology 36, 177–88.CrossRefGoogle ScholarPubMed
Körting, W. & Barrett, J. (1977). Carbohydrate catabolism in the plerocercoids of Schistocephalus solidus (Cestoda: Pseudophyllidea). International Journal for Parasitology 7, 411–17.CrossRefGoogle Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–75.CrossRefGoogle ScholarPubMed
Mansour, T. E. (1972). Phosphofructoklnase. In Current Topics in Cellular Regulation vol. 5, (ed. Horecker, B. L. and Stadtman, E. R.) pp. 1–46. New York: Academic Press.Google Scholar
McManus, D. P. (1981). A biological study of adult and cystic stages of Echinococcus granulosus of human and animal origin from Kenya. Journal of Helminthology 55, 21–7.CrossRefGoogle Scholar
McManus, D. P. & James, B. L. (1975). Pyruvate kinases and carbon dioxide fixating enzymes in the digestive gland of Littorina saxatilis rudis (Maton) and in the daughter sporocysts of Microphallus similis (Jag). Comparative Biochemistry and Physiology 51B, 299–306.Google ScholarPubMed
McManus, D. P. & Macpherson, C. N. L. (1980). A biochemical and isoenzymic study of adult and cystic stages of Echinococcus granulosus of human and animal origin from Kenya. Parasitology 81, xxxi–ii.Google Scholar
McManus, D. P. & Smyth, J. D. (1978). Differences in the chemical composition and carbohydrate metabolism of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 77, 103–9.CrossRefGoogle ScholarPubMed
McManus, D. P. & Smyth, J. D. (1979). Isoelectric focusing of some enzymes from Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 259–65.CrossRefGoogle ScholarPubMed
Moon, T. W., Mustafa, T., Hulbert, W. C., Podesta, R. B. & Mettrick, D. F. (1977). The phosphoenolpyruvate branchpoint in adult Hymenolepis diminuta (Cestoda): a study of pyruvate kinase and phosphoenolpyruvate carboxykinase. Journal of Experimental Zoology 200, 325–36.CrossRefGoogle Scholar
Rolleston, F. S. (1972). A theoretical background to the use of measured concentrations of intermediates in study of the control of intermediary metabolism. In Current Topics in Cellular Regulation (ed. Horecker, B. L. and Stadtman, E. R.), pp. 47–75. New York: Academic Press.Google Scholar
Scheibel, L. W. & Saz, H. J. (1966). The pathway for anaerobic carbohydrate dissimilation in Hymenolepis diminuta. Comparative Biochemistry and Physiology 18, 151–62.CrossRefGoogle ScholarPubMed
Scrutton, M. C. & Utter, M. F. (1968). The regulation of glycolysis and gluconeogenesis. Annual Review of Biochemistry 37, 249–302.CrossRefGoogle Scholar
Smyth, J. D. (1977). Strain differences in Echinococcus granulosus, with special reference to the status of equine hydatidosis in the United Kingdom. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 93–100.CrossRefGoogle Scholar
Smyth, J. D. & Heath, D. D. (1970). Pathogenesis of larval cestodes in mammals. Helminthological Abstracts, A 39, 1–23.Google Scholar
Sterry, P. R. (1980). Intermediary metabolism in Ligula intestinalis (Linnaeus, 1758) (Cestoda: Pseudophyllidea). Ph.D. thesis, University of London.Google Scholar
Van Vugt, F., Van der Meer, P. & Van den Bergh, S. G. (1979). The formation of propionate and acetate as terminal processes in the energy metabolism of the adult liver fluke Fasciola hepatica. International Journal of Biochemistry 10, 11–18.CrossRefGoogle ScholarPubMed
Weinbach, E. C. & von Brand, T. (1970). The biochemistry of cestode mitochondria. I. Aerobic metabolism of mitochondria from Taenia taeniaeformis. International Journal of Biochemistry 1, 39–56.CrossRefGoogle Scholar
Williamson, D. H. & Brosnan, J. T. (1974). Concentrations of metabolites in animal tissues. In Methods of Enzymatic Analysis 2nd ed., vol. 4., (ed. Bergmeyer, H. U.), pp. 226–2302. New York and London: Academic Press.Google Scholar
Zammit, V. A., Beis, I. & Newsholme, E. A. (1978). Maximum activities and effects of fructose bisphosphate on pyruvate kinase from muscles of vertebrates and invertebrates in relation to the control of glycolysis. The Biochemical Journal 174, 989–98.CrossRefGoogle Scholar
Zammit, V. A. & Newsholme, E. A. (1978). Properties of pyruvate kinase and phosphoenolpyruvate carboxykinase in relation to the direction and regulation of phosphoenolpyruvate metabolism in muscles of the frog and marine invertebrates. The Biochemical Journal 174, 979–87.CrossRefGoogle Scholar