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Transhydrogenase and the anaerobic mitochondrial metabolism of adult Hymenolepis diminuta

Published online by Cambridge University Press:  21 September 2009

C. F. FIORAVANTI  and
K. P. VANDOCK
C. F. FIORAVANTI*
Affiliation:
Department of Biological Sciences, Bowling Green State University, Bowling Green Ohio 43403USA
K. P. VANDOCK
Affiliation:
Department of Biological Sciences, Bowling Green State University, Bowling Green Ohio 43403USA
*
*Corresponding author: Department of Biological Sciences, Bowling Green State University, Bowling Green Ohio 43402USA. Tel: (1) 419 372 2634. Fax: (1) 419 372 2024. E-mail: [email protected]
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Summary

The adult cestode, Hymenolepis diminuta, is essentially anaerobic energetically. Carbohydrate dissimilation results in acetate, lactate and succinate accumulation with succinate being the major end product. Succinate accumulation results from the anaerobic, mitochondrial, ‘malic’ enzyme-dependent utilization of malate coupled to ATP generation via the electron transport-linked fumarate reductase. A lesser peroxide-forming oxidase is apparent, however, fumarate reduction to succinate predominates even in air. The H. diminuta matrix-localized ‘malic’ enzyme is NADP-specific whereas the inner membrane (IM)-associated electron transport system prefers NADH. This dilemma is circumvented by the mitochondrial, IM-associated NADPH→NAD+ transhydrogenase in catalyzing hydride ion transfer from NADPH to NAD+ on the IM matrix surface. Hydride transfer is reversible and phospholipid-dependent. NADP+ reduction occurs as a non energy-linked and energy-linked reaction with the latter requiring electron transport NADH utilization or ATP hydrolysis. With NAD+ reduction, the cestode transhydrogenase also engages in concomitant proton translocation from the mitochondrial matrix to the intermembrane space and supports net ATP generation. Thus, the cestode NADPH→NAD+ system can serve not only as a metabolic connector, but an additional anaerobic phosphorylation site. Although its function(s) is unknown, a separate IM-associated NADH→ NAD+ transhydrogenation, catalyzed by the lipoamide and NADH dehydrogenases, is noted.

Keywords

Transhydrogenasemitochondriaanaerobic energeticsHymenolepis diminutacestodemetabolism
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 395 - 410
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Azzi, A., Chance, B., Radda, G. K. and Lee, C. P. (1969). A fluorescence probe of energy-dependent structure changes in fragmented membranes. Proceedings of the National Academy of Sciences, USA 62, 612–619.Google Scholar
Barrett, J. and Beis, I. (1982). Catalase in free-living and parasitic platyhelminths. Experientia 38, 536.CrossRefGoogle ScholarPubMed
Bueding, E. and Saz, H. J. (1968). Pyruvate kinase and phosphoenolpyruvate carboxykinase activities of Ascaris muscle, Hymenolepis diminuta and Schistosoma mansoni. Comparative Biochemistry and Physiology 24, 511–518.Google Scholar
Danielson, L. and Ernster, L. (1963). Demonstration of a mitochondrial energy-dependent, pyridine nucleotide transhydrogenase reaction. Biochemical and Biophysical Research Communications 10, 91–96.CrossRefGoogle ScholarPubMed
Donstov, A. E., Grinius, L. L., Jasaitis, A. A., Severina, I. I. and Skulachev, V. P. (1972). A study on the mechanism of energy coupling in the redox chain. I. Transhydrogenase: the fourth site of the redox chain energy coupling. Journal of Bioenergetics 3, 277–303.Google Scholar
Fairbairn, D., Wertheim, G., Harpur, R. P. and Schiller, E. L. (1961). Biochemistry of normal and irradiated strains of Hymenolepis diminuta. Experimental Parasitology 11, 248–263.Google Scholar
Fioravanti, C. F. (1981). Coupling of mitochondrial NADPH:NAD transhydrogenase with electron transport in adult Hymenolepis diminuta. Journal of Parasitology 67, 823–831.CrossRefGoogle ScholarPubMed
Fioravanti, C. F. (1982 a). Mitochondrial NADH oxidase activity of adult Hymenolepis diminuta (Cestoda). Comparative Biochemistry and Physiology 72B, 591–596.Google Scholar
Fioravanti, C. F. (1982 b). Mitochondrial malate dehydrogenase, decarboxylating (‘malic’ enzyme) and transhydrogenase activities of adult Hymenolepis microstoma (Cestoda). Journal of Parasitology 68, 213–220.Google Scholar
Fioravanti, C. F. and Kim, Y. (1983). Phospholipid dependence of the Hymenolepis diminuta mitochondrial NADPH→NAD transhydrogenase. Journal of Parasitology 69, 1048–1054.CrossRefGoogle Scholar
Fioravanti, C. F. and Kim, Y. (1988). Rhodoquinone requirement of the Hymenolepis diminuta mitochondrial electron transport system. Molecular and Biochemical Parasitology 28, 129–134.CrossRefGoogle ScholarPubMed
Fioravanti, C. F., McKelvey, J. R. and Reisig, J. M. (1992). Energy-linked mitochondrial pyridine nucleotide transhydrogenase of adult Hymenolepis diminuta. Journal of Parasitology 78, 774–778.CrossRefGoogle ScholarPubMed
Fioravanti, C. F. and Reisig, J. M. (1990). Mitochondrial hydrogen peroxide formation and the fumarate reductase of Hymenolepis diminuta. Journal of Parasitology 76, 457–463.Google Scholar
Fioravanti, C. F. and Saz, H. J. (1976). Pyridine nucleotide transhydrogenases of parasitic helminths. Archives of Biochemistry and Biophysics 175, 21–30.Google Scholar
Fioravanti, C. F. and Saz, H. J. (1978). ‘Malic’ enzyme, fumarate reductase and transhydrogenase systems in the mitochiondria of adult Spirometra mansonoides (Cestoda). Journal of Experimental Zoology 206, 167–177.CrossRefGoogle Scholar
Fioravanti, C. F. and Saz, H. J. (1980). Energy metabolism of adult Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H.), pp. 463–504. Academic Press, New York.Google Scholar
Fisher, R. R. and Earle, S. R. (1982). Membrane-bound pyridine nucleotide transhydrogenases. In The Pyridine Nucleotide Coenzymes (ed. Everse, J., Anderson, B. and You, K. S.), pp. 279–324. Academic Press, New York.Google Scholar
Galante, Y. M., Lee, Y. and Hatefi, Y. (1980). Effect of pH on the mitochondrial energy-linked and non-energy-linked transhydrogenation reactions. Journal of Biological Chemistry 255, 9641–9646.CrossRefGoogle ScholarPubMed
Hassinen, J. E. and Vuokila, P. T. (1993). Reaction of dicyclohexylcarbodiimide with mitochondrial proteins. Biochimica et Biophysica Acta 114, 107–124.CrossRefGoogle Scholar
Heytler, P. G. (1979). Uncouplers of oxidative phosphorylation. In Methods in Enzymology LV (ed. Fleischer, S. and Packer, L.), pp. 462–472. Academic Press, New York.Google Scholar
Kim, Y. and Fioravanti, C. F. (1985). Reduction and oxidation of cytochrome c by Hymenolepis diminuta (Cestoda) mitochondria. Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology 81, 335–339.CrossRefGoogle ScholarPubMed
Köhler, P. and Saz, H. J. (1976). Demonstration and possible function of NADH:NAD+ transhydrogenase from Ascaris muscle mitochondria. Journal of Biological Chemistry 251, 2217–2225.CrossRefGoogle ScholarPubMed
Komuniecki, R. and Saz, H. J. (1979). Purification of lipoamide dehydrogenase from Ascaris muscle mitochondria and its relationship to NADH→NAD+ transhydrogenase activity. Archives of Biochemistry and Biophysics 196, 239–247.Google Scholar
Lee, C. P. and Ernster, L. (1989). Energy-linked nicotinamide nucleotide transhydrogenase. Biochimica et Biophysica Acta 1000, 371–376.CrossRefGoogle ScholarPubMed
Li, T., Gracy, R. W. and Harris, B. G. (1972). Studies on enzymes from parasitic helminths. II. Purification and properties of malic enzyme from the tapeworm, Hymenolepis diminuta. Archives of Biochemistry and Biophysics 150, 397–406.Google Scholar
Lumsden, R. D., Oaks, J. A. and Mills, R. R. (1969). Mitochondrial oxidation of diaminobenzidine and its relationship to the cytochemical localization of tapeworm peroxidase. Journal of Parasitology 55, 1119–1133.CrossRefGoogle Scholar
Mayer, R. T., Svoboda, J. A. and Weirich, G. F. (1978). Ecdysone 20-hydroxylase in midgut mitochondria of Manduca sexta (L.). Hoppe-Seyler's Zeitschrift für Physiologische Chemie 359, 1247–1257.CrossRefGoogle ScholarPubMed
McKelvey, J. R. and Fioravanti, C. F. (1984). Coupling of ‘malic’, enzyme and NADPH→NAD transhydrogenase in the energetics of Hymenolepis diminuta (Cestoda). Comparative Biochemistry and Physiology 77B, 737–742.Google Scholar
McKelvey, J. R. and Fioravanti, C. F. (1985). Intramitochondrial localization of fumarate reductase, NADPH→NAD transhydrogenase, ‘malic’ enzyme and fumarase in adult Hymenolepis diminuta. Molecular and Biochemical Parasitology 17, 253–263.CrossRefGoogle ScholarPubMed
McKelvey, J. R. and Fioravanti, C. F. (1986). Localization of cytochrome c oxidase and cytochrome c peroxidase in mitochondria of Hymenolepis diminuta (Cestoda). Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology, 85, 333–335.CrossRefGoogle ScholarPubMed
Mercer-Haines, N. and Fioravanti, C. F. (2008). Hymenolepis diminuta: Mitochondrial transhydrogenase as an additional site for anaerobic phosphorylation. Experimental Parasitology 119, 24–29. doi:10.1016/j.exppara.2007.12.006.Google Scholar
Mercer, N. A., McKelvey, J. R. and Fioravanti, C. F. (1999). Hymenolepis diminuta: Catalysis of transmembrane proton translocation by mitochondrial NADPH→NAD transhydrogenase. Experimental Parasitology 91, 52–58. doi: 10.1006/expr.1999.4330.CrossRefGoogle Scholar
Olesen, J. B., Heckman, C. A., Lukinius, A., Schwab, D. W., Upite, D. V. and Fioravanti, C. F (1997). HACH: A polymer designed to optimize protein antigen localization. Microscopy and Microanalysis 3, 321–331.Google Scholar
Park, J. P. and Fioravanti, C. F. (2006). Catalysis of NADH→NADP+ transhydrogenation by adult Hymenolepis diminuta mitochondria. Parasitology Research 98, 200–206. doi: 10.1007/s00436-005-0020-z.Google Scholar
Paul, J. M. and Barrett, J. (1980). Peroxide metabolism in the cestodes Hymenolepis diminuta and Moniezia expansa. International Journal for Parasitology 10, 121–124.CrossRefGoogle Scholar
Prescott, L. M. and Campbell, J. W. (1965). Phosphoenolpyruvate carboxylase activity and glycogenesis in the flatworm Hymenolepis diminuta. Comparative Biochemistry and Physiology 14, 491–511.Google Scholar
Read, C. P. (1953). Contributions to cestode enzymology. I. The cytochrome system and succinic dehydrogenase in Hymenolepis diminuta. Experimental Parasitology 1, 353–362.Google Scholar
Rew, R. S. and Saz, H. J. (1974). Enzyme localization in the anaerobic mitochondria of Ascaris lumbricoides. Journal of Cell Biology 63, 125–135.Google Scholar
Roberts, L. S. (1961). The influence of population density on patterns and physiology of growth in Hymenolepis diminuta (Cestoda:Cyclophyllidea) in the definitive host. Experimental Parasitology 11, 332–371.CrossRefGoogle ScholarPubMed
Roberts, L. S. and Mong, F. N. (1969). Developmental physiology of cestodes. IV. In vitro development of Hymenolepis diminuta in presence and absence of oxygen. Experimental Parasitology 26, 166–174.CrossRefGoogle ScholarPubMed
Robinson, J. M. and Bogitsh, B. J. (1976). Cytochemical localization of peroxidase activity in the mitochondria of Hymenolepis diminuta. Journal of Parasitology 62, 761–765.CrossRefGoogle ScholarPubMed
Robinson, J. M. and Bogitsh, B. J. (1978). Hymenolepis diminuta: Biochemical properties of peroxidase activity in mitochondria. Experimental Parasitology 45, 169–174.CrossRefGoogle ScholarPubMed
Rydström, J., Kanner, N. and Racker, E. (1975). Resolution and reconstitution of mitochondrial nicotinamide nucleotide transhydrogenase. Biochemical and Biophysical Research Communications 67, 831–839.CrossRefGoogle ScholarPubMed
Saz, H. J., Berta, J. and Kowalski, J. (1972). Transhydrogenase and anaerobic phosphorylation in Hymenolepis diminuta mitochondria. Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology 43, 725–732.CrossRefGoogle ScholarPubMed
Scheibel, L. W. and Saz, H. J. (1966). The pathway for anaerobic carbohydrate dissimilation in Hymenolepis diminuta. Comparative Biochemistry and Physiology 18, 151–162.CrossRefGoogle ScholarPubMed
Scheibel, L. W., Saz, H. J. and Bueding, E. (1968). The anaerobic incorporation of 32P into adenosine triphosphate by Hymenolepis diminuta. Journal of Biological Chemistry 243, 2229–2235.Google Scholar
Schiller, E. L. (1965). A simplifed method for the in vitro cultivation of the rat tapeworm, Hymenolepis diminuta. Journal of Parasitology 51, 516–518.Google Scholar
Threadgold, L. T., Arme, C. and Read, C. P. (1968). Ultrastructural localization of a peroxidase in the tapeworm, Hymenolepis diminuta. Journal of Parasitology 54, 802–807.Google Scholar
Umezurike, G. M. and Anya, A. O. (1980). Nicotinamide nucleotide transhydrogenase in Fasciola gigantica. Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology 65, 575–577.CrossRefGoogle Scholar
Unnikrishnan, L. A. and Raj, R. K. (1995). Transhydrogenase activities and malate dismutation linked to fumarate reductase system in the filarial parasite Setaria digitata. International Journal for Parasitology 25, 779–785.Google Scholar
Van de Stadt, R., Nieuwenhuis, F. J. R. M. and Van Dam, K. (1971). On the reversibility of the energy-linked transhydrogenase. Biochimica et Biophysica Acta 234, 173–177.CrossRefGoogle ScholarPubMed
Vandock, K. P., Smith, S. L. and Fioravanti, C. F. (2008). Midgut mitochondrial transhydrogenase in wandering stage larvae of the tobacco hornworm, Manduca sexta. Archives of Insect Biochemistry and Physiology 69, 118–126. doi: 10.1002/arch.20277.Google Scholar
Voge, M., Jaffe, J., Bruckner, D. A. and Meymarian, E. (1976). Synergistic growth promoting action of L-cysteine and nitrogen upon Hymenolepis diminuta cysticercoids in vitro. Journal of Parasitology 62, 951–954.CrossRefGoogle ScholarPubMed
Walker, D. J. and Fioravanti, C. F. (1995). Mitochondrial NADH→NAD transhydrogenation in adult Hymenolepis diminuta. Journal of Parasitology 81, 350–353.Google Scholar
Walker, D. J., Burkhart, W. and Fioravanti, C. F. (1997). Hymenolepis diminuta: mitochondrial NADH→NAD transhydrogenation and the lipoamide dehydrogenase system. Experimental Parasitology 85, 158–167.Google Scholar
Watts, S. D. M. and Fairbairn, D. (1974). Anaerobic excretion of fermentation acids by Hymenolepis diminuta during development in the definitive host. Journal of Parasitology 60, 621–625.Google Scholar
Zenka, J. and Propkopic, J. (1988). Transhydrogenase activities in the mitochondria of Taenia crassiceps cysticerci. Folia Parasitologica 35, 31–36.Google Scholar