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Comparison of glycolysis and glutaminolysis in Onchocerca volvulus and Brugia pahangi by 13C nuclear magnetic resonance spectroscopy

Published online by Cambridge University Press:  06 April 2009

N. E. MacKenzie ,
E. A. Van De Waa ,
P. R. Gooley ,
J. F. Williams ,
J. L. Bennett ,
S. M. Bjorge ,
T. A. Baille  and
T. G. Geary
N. E. MacKenzie
Affiliation:
Department of Pharmaceutical Sciences, University of Arizona, Tucson, AZ 85721
E. A. Van De Waa
Affiliation:
Department of Microbiology and Public Health and Department of Medicinal Chemistry, University of Washington, Seattle, WA 98185
P. R. Gooley
Affiliation:
Department of Pharmaceutical Sciences, University of Arizona, Tucson, AZ 85721
J. F. Williams
Affiliation:
Department of Microbiology and Public Health and
J. L. Bennett
Affiliation:
Department of Pharmacology and Toxicolgy, Michigan State University, East Lansing, MI 48823
S. M. Bjorge
Affiliation:
Department of Medicinal Chemistry, University of Washington, Seattle, WA 98185
T. A. Baille
Affiliation:
Department of Medicinal Chemistry, University of Washington, Seattle, WA 98185
T. G. Geary
Affiliation:
The Upjohn Company, Parasitology Research, Kalamazoo, MI 49001
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Summary

Comparison of glycolysis in Brugia pahangi and Onchocerca volvulus by C nuclear magnetic resonance (NMR) spectroscopy showed that the former organism is predominantly a lactate fermenter and the latter resembles more closely the metabolism of a mixed acid fermenter producing lactate, succinate, acetate, ethanol, formate and carbon dioxide. Both organisms synthesize glycogen as a storage carbohydrate. Glutaminolysis in both organisms proceeds by the δ-aminobutyrate shunt to produce succinate which is then further metabolized to acetate and carbon dioxide as end-products.

Keywords

Onchocerca volvulusBrugia pahangiglycolysisglutaminolysisnuclear magnetic resonance spectroscopy.
Type
Research Article
Information
Parasitology , Volume 99 , Issue 3 , December 1989 , pp. 427 - 435
Copyright
Copyright © Cambridge University Press 1989

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References

Albro, P. W. (1975). Determination of protein in preparations of microsomes. Analytical Biochemistry 64, 485–93.CrossRefGoogle ScholarPubMed
Barrett, J. (1981). Biochemistry of Parasitic Helminths. Baltimore: University Park Press.CrossRefGoogle Scholar
Barrett, J., Mendis, A. H. W. & Butterworth, P. E. (1986). Carbohydrate metabolism in Brugia pahangi (Nematoda; Filariodea). International Journal for Parasitology 16, 465–9.CrossRefGoogle Scholar
Barron, K. D., Rogers, P. L. & Smith, G. M. (1986). N M R studies of [l-2H]glucose metabolism in Zymomonas mobilis. European Journal of Biochemistry 157, 195–202.CrossRefGoogle Scholar
Baxter, R. L., MacKenzie, N. E. & Scott, A. I. (1983). CMR as a probe for metabolic pathways in vivo. In Biological Magnetic Resonance, vol. 5 (ed. Berliner, L. J) pp. 1–20. New York: Plenum.Google Scholar
Behm, C. A., Bryant, C. & Jones, A. J.(1987). Studies of glucose metabolism in Hymenolepis diminuta using 13C nuclear magnetic resonance. International Journal for Parasitology 17, 1333–61.CrossRefGoogle ScholarPubMed
Blackburn, B. J., Hutton, H. M., Novak, M. & Evans, W. S. (1986). Hymenolepis diminuta: Nuclear magnetic resonance analysis of the excretory products resulting from the metabolism of D-[13C6]glucose. Experimental Parasitology 62, 381–8.CrossRefGoogle Scholar
Christie, D. A., Powell, J. W., Stables, J. N. & Watt, R. A. (1987). A nuclear magnetic resonance study of the role of phosphoenol pyruvate carboxykinase (PEPCK) in the glucose metabolism of Dipetalomena viteae. Molecular and Biochemical Parasitology 24, 125–30.CrossRefGoogle ScholarPubMed
Cohen, S. M. (1987). Applications of 13C-NMR to the study of metabolic regulation in the living cell. In NMR Spectroscopy of Cells and Organisms, vol. 1, (ed. Gupta, P. K), pp. 31–49. Florida: CRC Press Inc.Google Scholar
Cox, R. B. & Zatman, L. J. (1973). Isocitrate lyase and adenosine triphosphate malate lyase as key enzymes for the methylotrophic growth of bacterium 5H2. Biochemical Society Transactions 1, 669–70.CrossRefGoogle Scholar
Darling, T. N., Davis, D. G., London, R. E. & Blum, J. J. (1987). Products of Leishmania braziliensis glucose catabolism: Release of D-lactate and, under anaerobic conditions, glycerol. Proceedings of the National Academy of Sciences, USA 84, 7129–33.CrossRefGoogle ScholarPubMed
Den Hollander, J. A., Brown, T. R., Ugurbil, K. & Shulman, R. (1979). 13C nuclear magnetic resonance studies of anaerobic glycolysis in suspensions of yeast cells. Proceedings of the National Academy of Sciences, USA 76, 6096–100.CrossRefGoogle ScholarPubMed
Deslauries, R., Ekiel, I., Kroft, T., Leveille, L. & Smith, I. C. P. (1984). NMR Studies of malaria: glycolysis in red cells of mice infected with Plasmodium berghei and the effects thereon of antimalarial drugs. Tetrahedron 39, 3543–8.CrossRefGoogle Scholar
Goodwin, L. G. (1984). Recent advances in research on filariasis; 1. Chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 78 (Suppl.), 1–8.CrossRefGoogle Scholar
Hall, J. E., MacKenzie, N. E., Mansfield, M. J., Mccloskey, D. E. & Scott, A. I. (1988). 13C-N M R analysis of alanine metabolism by isolated perfused livers from C3HeB/FeJ mice infected with African trypanosomes. Comparative Biochemistry and Physiology 89B, 679–85.Google Scholar
Hunter, B. K., Nicholls, K. M. & Sanders, J. K. M. (1984). Formaldehyde metabolism by Escherichia coli. In vivo carbon, deuterium, and two-dimensional NMR observations of multiple detoxifying pathways. Biochemistry 23, 508–14.CrossRefGoogle ScholarPubMed
Kallinowski, F., Runkel, SL., Fortmeyer, H. P., Forster, H. & Vaupel, P. (1987). L-glutamine: a major substrate for tumor cells in vivo ? Journal of Cancer Research and Clinical Oncology 113, 209–15.CrossRefGoogle Scholar
Köhler, P. (1985). The strategies of energy conversion in helminths. Molecular and Biochemical Parasitology 17, 1–18.CrossRefGoogle Scholar
Körting, W. & Fairbairn, D. (1972). Anaerobic energy metabolism in Moniliformis dubius (Acanthocephala). Journal of Parasitology 58, 45–50.CrossRefGoogle ScholarPubMed
Laurie, J. S. (1959). Aerobic metabolism of Moniliformis dubius (Acanthocephala). Experimental Parasitology 8, 188–97.CrossRefGoogle ScholarPubMed
MacKenzie, N. E., Baxter, R. L., Scott, A. I. & Fagerness, P. E. (1982 a). Uniformly 13C-enriched substrates as NMR probes for metabolic events in vivo. Application of double quantum coherence to a biochemical problem. Journal of the Chemical Society Chemical Communications 145–7.CrossRefGoogle Scholar
MacKenzie, N. E. & Gooley, P. R. (1988). Applications of NMR to biological systems. Medicinal Research Reviews 8, 57–76.CrossRefGoogle ScholarPubMed
MacKenzie, N. E., Hall, J. E., Flynn, I. W. & Scott, A. I. (1983). 13C Nuclear magnetic resonance studies of anaerobic glycolysis in Trypanosoma brucei spp. Bioscience Reports 3, 141–51.CrossRefGoogle ScholarPubMed
MacKenzie, N. E., Hall, J. E., Seed, J. R. & Scott, A. I. (1982 b). Carbon-13 nuclear magnetic resonance studies of glucose catabolism by Trypanosoma brucei gambiense. European Journal of Biochemistry 121, 657–61.CrossRefGoogle ScholarPubMed
MacKenzie, N. E., Johnson, J., Burton, G., Wagner, G. G. & Scott, A. I. (1984). 13C NMR studies of glycolysis in intra- and extra-erythrocytic Babesia microti. Molecular and Biochemical Parasitology 13, 13–20.CrossRefGoogle ScholarPubMed
Mcilwaen, H. & Bachelard, H. S. (1985). Biochemistry and the Central Nervous System. New York: Churchill Livingstone.Google Scholar
Powell, J. W., Stables, J. N. & Watt, R. A. (1986 a). An investigation of the glucose metabolism of Brugia pahangi and Dipetalomena viteae by nuclear magnetic resonance spectroscopy. Molecular and Biochemical Parasitology 18, 171–82.CrossRefGoogle ScholarPubMed
Powell, J. W., Stables, J. N., & Watt, R. A. (1986 b). An NMR study on the effect of glucose availability on carbohydrate metabolism in Dipetalomena viteae and Brugia pahangi. Molecular and Biochemical Parasitology 19, 265–71.CrossRefGoogle Scholar
Ramp, TH. & Köhler, P. (1984). Glucose and pyruvate catabolism in Litomosoides carinii. Parasitology 89, 229–44.CrossRefGoogle Scholar
Schulz-Key, H., Albiez, E. J. & Buttner, D. W. (1977). Isolation of living adult Onchocera volvulus from nodules. Tropenmedizin und Parasitologie 28, 428–40.Google Scholar
Silerud, L. O. & Shulman, R. G. (1983). Structure and metabolism of mammalian liver glycogen monitored by carbon-13 nuclear magnetic resonance. Biochemistry 22, 1087–94.CrossRefGoogle Scholar
Tielens, A. G. M. & Van Den Bergh, S. G. (1985). The (An) aerobic energy metabolism of parasitic helminths. Molecular Parasitology 8, 359–69.Google Scholar
Tuboi, S. & Kikuchi, G. (1963). Enzymic cleavage of malate to glyoxalate and acetyl coenzyme A. Journal of Biochemistry 53, 364–73.CrossRefGoogle Scholar
Ugurbil, K., Brown, T. R., Den Hollander, J. A., Glynn, P. & Shulman, R. G. (1978). High-resolution 13C nuclear magnetic resonance studies of glucose metabolism in Escherichia coli. Proceedings of the National Academy of Sciences, USA 75, 3742–6.CrossRefGoogle ScholarPubMed
Van De Waa, E. A., Foster, L. A., Deruiter, J., Williams, J. F. & Geary, T. G. (1989). Glutamine-supported motility of adult filarial parasites in vitro and the effects of glutamine antimetabolites. Experimental Parasitology (in the Press).Google Scholar
Wang, E. J. & Saz, H. J. (1974). Comparative biochemical studies of Litomosoides carinii, Dipetalomena viteae, and Brugia pahagi adults. Journal of Parasitology 60, 316–21.CrossRefGoogle Scholar
Wittich, R. M. & Walter, R. D. (1987). Onchocerca volvulus: Partial glucose catabolism via fumarate and succinate. Experimental Parasitology 64, 517–18.CrossRefGoogle ScholarPubMed