Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-26T09:18:37.037Z Has data issue: false hasContentIssue false

Energy metabolism in the developing larval stages of Ancylostoma tubaeforme and Haemonchus contortus: glycolytic and tncarboxylic acid cycle enzymes

Published online by Cambridge University Press:  06 April 2009

C. O. E. Onwuliri
Affiliation:
Parasitic Nematodes Research Project, Department of Zoology, University of Nigeria, Nsukka, Nigeria

Extract

The activities of glycolytic and related enzymes and the tricarboxylic acid cycle enzymes were measured in freshly isolated 1st- (Li), 2nd- (L2) and 3rd-stage (L3) larvae of both Ancylostoma tubaeforme and Haemonchus contortus. All enzymes of the glycolytic pathway were present in all developmental stages of both strongylid nematodes although higher levels of activities were obtained in the pre-infective 1st- and 2nd-stage larvae than in the infective 3rd stage. However, the pre-infective larvae contained lower levels of pyruvate kinase (PK) than the infective larvae. Consequently, the pyruvate kinase to phosphoenolpyruvate carboxykinase (PEPCK) ratios were 0·23 and 0·26 for the L1s and L2s for A. tubaeforme and 0·36 and 0·21 for those of H. contortus respectively. High levels of activity of glucose-6-phosphate dehydrogenase obtained in the bacteriophagous pre-infective larvae were consistent with high rates of morphogenesis and substrate synthesis characteristic of the pre-infective stages. All the tricarboxylic acid cycle enzymes were present in the infective larvae of both nematodes while in the pre-infective Li and L2 stages, the enzymes at the beginning of the cycle, namely aconitate hydratase and NAD-linked isocitrate dehydrogenase, were not detected. A scheme was proposed for the energy metabolism of these developing larvae. In this scheme, the pre-infective larvae were shown to operate an anaerobic metabolic pathway involving the carboxylation of phosphoenolpyruvate (PEP) by phosphoenolpyru vate carboxykinase (PEPCK) to form oxaloacetate (OAA), whereas in the infective larvae the metabolic pathway favouring the direct dephosphorylation of PEP, as in vertebrate tissues, was followed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1985

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

Agostn, M. & Aravena, L. C. (1959). Anaerobic glycolysis in homogenates of Trichinella spiralis larvae. Experimental Parasitology 8, 1030.CrossRefGoogle Scholar
Atkinson, H. J. (1980). Respiration in nematodes. In Nematodes as Biological Models, vol. 2 (ed. Zuckerman, B. M.), pp. 101–42. New York and London: Academic Press.Google Scholar
Barrett, J. (1976 a). Energy metabolism in nematodes. In The Organisation of Nematodes (ed. Croll, N. A.), pp. 1270. New York and London: Academic Press.Google Scholar
Barrett, J. (1976 b). ioenergetics in helminths. In Biochemistry of Parasite and Host–Parasite Relationships (ed. Bossche, H. Van den), pp. 6780. Amsterdam: Elsevier/North Holland Biomedical Press.Google Scholar
Barrett, J. & Beis, I. (1973 a). Studies on glycolysis in the muscle tissue of Ascaris lumbricoides (Nematoda). Comparative Biochemistry and Physiology 44B, 751–61.Google ScholarPubMed
Barrett, J. & Beis, I. (1973 b). The redox state of the free nicotinamide adenine dinucleotide couple in the cytoplasm and mitochondria of muscle tissue from Ascaris lumbricoides (Nematoda). Comparative Biochemistry and Physiology 44A, 331–40.CrossRefGoogle ScholarPubMed
Barrett, J. & Beis, I. (1975). Energy metabolism in developing Ascaris lumbricoides eggs. I. The glycolytic enzymes. Developmental Biology 42, 181–9.Google Scholar
Beisenherz, O. (1955). Methods in Enzymology, vol. 1 (ed. Colowick, S. P. and Kaplan, N. O.), pp. 387–91. New York and London: Academic Press.CrossRefGoogle Scholar
Bergmeyer, H. U. & Bernt, E. (1963). Methods in Enzymatic Analysis (ed. Bergmeyer, H. U.), pp. 757–60. New York and London: Academic Press.Google Scholar
Brazier, J. O. & Jaffe, J. J. (1973). Two types of pyruvate kinase in schistosomes and fllariae. Comparative Biochemistry and Physiology 44B, 145–55.Google Scholar
Bryant, C. (1975). Carbon dioxide utilization and the regulation of respiratory metabolic pathways in the parasitic helminths. In Advances in Parasitology, vol. 13 (ed. Dawes, B.), pp. 3569. New York and London: Academic Press.Google Scholar
Bücher, T. & Pfleiderer, G. (1955). Methods in Enzymology, vol. 1 (ed. Colowick, S. P. and Kaplan, N. O.), pp. 435–40. New York and London: Academic Press.CrossRefGoogle Scholar
Bueding, E. (1949). Studies on the metabolism of the filarial worm Litomosoides carinii. Journal of Experimental Medicine 89, 107–30.CrossRefGoogle Scholar
Bueding, E. & Saz, H. J. (1968). Pyruvate kinase and phosphoenolpyruvate carboxykinase activities of Ascaris muscle, Hymenolepis diminuta and Schistosoma mansoni. Comparative Biochemistry and Physiology 24, 511–18.CrossRefGoogle ScholarPubMed
Costello, L. C. & Grollman, S. (1959). Studies on the reaction of the Kreb's Cycle in Strongyloide papillosus infective larvae. Experimental Parasitology 8, 83–9.CrossRefGoogle Scholar
De Ley, J. & Vercruysse, R. (1955). Glucose-6-phosphateandgluconate-6-phosphatedehydrogenase in worms. Biochimica et Biophysica Acta 16, 615–16.CrossRefGoogle ScholarPubMed
De Pietro, D. & Weinhouse, S. (1960). Hepatic glucokinase in the fed, fasted and alloxan diabetic rat. Journal of Biological Chemistry 235, 2542–5.Google Scholar
Evans, M. C. W. (1965). The photoassimilation of succinate to hexose by Rhodospirillum rubrum. The Biochemical Journal 95, 669–77.CrossRefGoogle ScholarPubMed
Fernando, M. A. (1963). Metabolism of hookworms. I. Observations on the oxidative metabolism and glycogen synthesis in adult female Ancylostoma caninum. Experimental Parasitology 15, 284–92.Google Scholar
Fodge, D. W., Gracy, R. W. & Harris, B. G. (1972). Studies on enzymes from parasitic helminths. I. Purification and physical properties of malic enzymes from the muscle tissue of Ascaris suum. Biochimica et Biophysica Acta 268, 271–84.CrossRefGoogle ScholarPubMed
Glock, G. E. & Maclean, P. (1953). Further studies on the properties and assay of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase of rat liver. The Biochemical Journal 55, 400–8.CrossRefGoogle ScholarPubMed
Goebell, H. & Klingenberg, M. (1964). DPN-spezifische Isocitrate-dehydrogenaseder Mitochondrien. I. Kinetische Eigenschaften, Vorkommen und Funktion der DPN-spezifischen isocitrate dehydrogenase. Biochemische Zeitschrift 340, 441–64.Google Scholar
Hutchinson, G. W. & Fernando, M. A. (1974). Enzymes of glycolysis and the pentose phosphate pathway during development of the rabbit stomach worm Obeliscoides cuniculi. International Journal for Parasitology 4, 389–95.CrossRefGoogle ScholarPubMed
Hutchinson, W. F. & McNeill, K. M. (1970). Glycolysis in the adult dog heartworm Dirofilaria immitis. Comparative Biochemistry and Physiology 35, 721–7.CrossRefGoogle Scholar
Köitler, P. & Hanselmann, K. (1973). Intermediary metabolism in Dicrocoelium dendriticum (Trematoda). Comparative Biochemistry and Physiology 45B, 825–45.Google Scholar
Kornberg, A. (1955). Methods in Enzymology, vol. 1 (ed. Colowick, S. P. and Kaplan, N. O.), pp. 441–3. New York and London: Academic Press.Google Scholar
Körting, W. & Barrett, J. (1977). Carbohydrate catabolism in the plerocercoids of Schistocephalus solidus (Cestoda: Pseudophyllidea). international Journal for Parasitology 7, 411–17.Google Scholar
Körting, W. & Fairbairn, D. (1971). Changes in beta-oxidation and related enzymes during the life cycle of Strongyloides ratti (Nematoda). Journal of Parasitology 57, 1153–8.Google Scholar
Lascelles, J. (1960). The formation of ribulose-1,5-diphosphate carboxylase by growing cultures of Athiorhodaceae. Journal of General Microbiology 23, 499510.CrossRefGoogle ScholarPubMed
Lee, E. H. & Fernando, M. A. (1971). Terminal anaerobic carbohydrate metabolism of three developmental stages of the rabbit stomach worm Obeliscoides cuniculi. international Journal of Biochemistry 2, 403–8.CrossRefGoogle Scholar
Lowry, O. H., Rosebeougil, N. T., Farr, A. L. & Randall, H. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265–75.CrossRefGoogle ScholarPubMed
Najjar, V. A. (1948). The isolation and properties of phosphoglucomutase. Journal of Biological Chemistry 175, 281–90.CrossRefGoogle ScholarPubMed
Ochoa, S. (1955). Methods in Enzymology, vol. 1 (ed. Colowick, S. P. and Kaplan, N. O.), pp. 699704. New York and London: Academic Press.Google Scholar
Onwuliri, C. O. E. (1980). Studies on some cytophysiological and biochemical changes during development of parasitic nematodes with special reference to the Strongylida, Diesing, 1851. Ph.D. thesis, University of Nigeria.Google Scholar
Onwuliri, C. O. E. (1984). A simple technique for obtaining large numbers of nematode larvae for biochemical investigations. Nigerian Journal of Parasitology (in the Press).Google Scholar
Onwuliri, C. O. E., Nwosu, A. B. C. & Anya, A. O. (1981). Experimental Ancylostoma tubaeforme infection of cats: changes in blood values and worm burden in relation to single infections of varying size. Zeitschrift für Parasitenkunde 64, 149–55.CrossRefGoogle ScholarPubMed
Plant, G. W. E. & Sung, S. C. (1955). Methods in Enzymology, vol. 1 (ed. Colowick, S. P. and Kaplan, N. O.), pp. 710–14. New York and London: Academic Press.CrossRefGoogle Scholar
Prichard, R. K. & Schofield, P. J. (1968 a). The glycolytic pathway in adult liver fluke Fasciola hepatica. Comparative Biochemistry and Physiology 24, 696710.Google ScholarPubMed
Prichard, H. K. & Schofield, P. J. (1968 b). The glyoxylate cycle, fructose-1,6-diphosphatase and glyconeogenesis in Fasciola hepatica. Comparative Biochemistry and Physiology 29, 581–90.CrossRefGoogle Scholar
Racker, E. (1950). Spectrophotometric measurements of the enzymatic formation of fumaric and cis-aconitic acids. Biochimica et Biophysica Acta 4, 211–14.Google Scholar
Saz, H. J. & Lescure, O. L. (1969). The functions of phosphoenol pyruvate carboxylase and malic enzyme in anaerobic formation of succinate by Ascaris lumbricoides. Comparative Biochemistry and Physiology 30, 4960.CrossRefGoogle Scholar
Shonk, C. E. & Boxer, O. E. (1964). Enzyme pattern in human tissues. 1. Methods of the determination of glycolytic enzymes. Cancer Research 24, 709–21.Google ScholarPubMed
Sutherland, E. W. (1949). Activation of phosphoglucomutase by metal binding agents. Journal of Biological Chemistry 180, 1279–84.Google Scholar
Umezurike, G. M. & Anya, A. O. (1978). Studies of energy metabolism in the endoparasitic Strongyluris brevicaudata (Nematoda). Comparative Biochemistry and Physiology 59, 147–51.Google Scholar
Underwood, A. H. & Newsholme, E. A. (1965). Properties of phosphofructokinase from rat liver and their relation to the control of glycolysis and glyconeogenesis. The Biochemical Journal 95, 868–75.Google Scholar
Vaatstra, W. J. (1969). Intermediary metabolism of the cattle lungworm Dictyocaulus viviparus. Hoppe-Seyler's Zeitschrift für physiologische Chemie 350, 701–9.Google Scholar
Van Den Bossche, H., Vanparijs, D. F. J. & Thienpont, P. (1969). Studies on the carbohydrate metabolism of third-stage Haemonchus contortus larvae. Life Sciences 8, 1047–54.Google Scholar
Von Brand, T. (1974). The Biochemistry of Parasites. New York and London: Academic Press.Google Scholar
Ward, C. W. & Schofield, P. J. (1967 a). Glycolysis in Haemonchus contortus larvae and rat liver. Comparative Biochemistry and Physiology 22, 3352.Google Scholar
Ward, C. W. & Schofield, P. J. (1967 b). Comparative activity and intracellular distribution of tricarboxylic acid cycle enzymes in Haemonchus contortus larvae and rat liver. Comparative Biochemistry and Physiology 23, 335–59.CrossRefGoogle ScholarPubMed