Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Oct;84(20):7129–7133. doi: 10.1073/pnas.84.20.7129

Products of Leishmania braziliensis glucose catabolism: release of D-lactate and, under anaerobic conditions, glycerol.

T N Darling 1, D G Davis 1, R E London 1, J J Blum 1
PMCID: PMC299243  PMID: 3478686

Abstract

Leishmania braziliensis panamensis promastigotes were incubated with glucose as the sole carbon source. About one-fifth of the glucose consumed under aerobic conditions was oxidized to CO2. Nuclear magnetic resonance studies with [1-13C]glucose showed that the other products released were succinate, acetate, alanine, pyruvate, and lactate. Under anaerobic conditions, lactate output increased, glycerol became a major product, and, surprisingly, glucose consumption decreased. Enzymatic assays showed that the lactate formed was D(-)-lactate. The release of alanine during incubation with glucose as the sole carbon source suggested that appreciable proteolysis occurred, consistent with our observation that a large amount of ammonia was released under these conditions. The discoveries that D-lactate is a product of L. braziliensis glucose catabolism, that glycerol is produced under anaerobic conditions, and that the cells exhibit a "reverse" Pasteur effect open the way for detailed studies of the pathways of glucose metabolism and their regulation in this organism.

Full text

PDF
7133

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brandt R. B. Determination of D-lactate in plasma. Methods Enzymol. 1982;89(Pt 500):35–40. doi: 10.1016/s0076-6879(82)89008-3. [DOI] [PubMed] [Google Scholar]
  2. CHATTERJEE A. N., GHOSH J. J. Transaminases of Leishmania donovani, the causative organism of kala-azar. Nature. 1957 Dec 21;180(4599):1425–1425. doi: 10.1038/1801425a0. [DOI] [PubMed] [Google Scholar]
  3. CROWTHER S., FULTON J. D., JOYNER L. P. The metabolism of Leishmania donovani in culture. Biochem J. 1954 Feb;56(2):182–185. doi: 10.1042/bj0560182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cazzulo J. J., Franke de Cazzulo B. M., Engel J. C., Cannata J. J. End products and enzyme levels of aerobic glucose fermentation in trypanosomatids. Mol Biochem Parasitol. 1985 Sep;16(3):329–343. doi: 10.1016/0166-6851(85)90074-x. [DOI] [PubMed] [Google Scholar]
  5. Collins N., Merrett M. J. The localization of glycollate-pathway enzymes in Euglena. Biochem J. 1975 May;148(2):321–328. doi: 10.1042/bj1480321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coombs G. H., Sanderson B. E. Amine production by Leishmania mexicana. Ann Trop Med Parasitol. 1985 Aug;79(4):409–415. doi: 10.1080/00034983.1985.11811939. [DOI] [PubMed] [Google Scholar]
  7. Cooper R. A., Anderson A. The formation and catabolism of methylglyoxal during glycolysis in Escherichia coli. FEBS Lett. 1970 Dec 11;11(4):273–276. doi: 10.1016/0014-5793(70)80546-4. [DOI] [PubMed] [Google Scholar]
  8. Darling T. N., Blum J. J. In vitro reversible transformation of Leishmania braziliensis panamensis between promastigote and ellipsoidal forms. J Protozool. 1987 May;34(2):166–168. doi: 10.1111/j.1550-7408.1987.tb03154.x. [DOI] [PubMed] [Google Scholar]
  9. FULTON J. D., JOYNER L. P. Studies on protozoa; the metabolism of Leishman-Donovan bodies and flagellates of Leishmania donovani. Trans R Soc Trop Med Hyg. 1949 Nov;43(3):273-86, pl. doi: 10.1016/0035-9203(49)90004-8. [DOI] [PubMed] [Google Scholar]
  10. Fair D. S., Krassner S. M. Alanine aminotransferase and aspartate aminotransferase in Leishmania tarentolae. J Protozool. 1971 Aug;18(3):441–444. doi: 10.1111/j.1550-7408.1971.tb03352.x. [DOI] [PubMed] [Google Scholar]
  11. GRANT P. T., FULTON J. D. The catabolism of glucose by strains of Trypanosoma rhodesiense. Biochem J. 1957 Jun;66(2):242–250. doi: 10.1042/bj0660242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hammond D. J., Bowman I. B. Trypanosoma brucei: the effect of glycerol on the anaerobic metabolism of glucose. Mol Biochem Parasitol. 1980 Dec;2(2):63–75. doi: 10.1016/0166-6851(80)90032-8. [DOI] [PubMed] [Google Scholar]
  13. Hart D. T., Coombs G. H. Leishmania mexicana: energy metabolism of amastigotes and promastigotes. Exp Parasitol. 1982 Dec;54(3):397–409. doi: 10.1016/0014-4894(82)90049-2. [DOI] [PubMed] [Google Scholar]
  14. Hart D. T., Coombs G. H. The effects of carbon dioxide and oxygen upon the growth and in vitro transformation of Leishmania mexicana mexicana. Mol Biochem Parasitol. 1981 Nov;4(1-2):117–127. doi: 10.1016/0166-6851(81)90034-7. [DOI] [PubMed] [Google Scholar]
  15. Husic D. W., Tolbert N. E. Anaerobic Formation of d-Lactate and Partial Purification and Characterization of a Pyruvate Reductase from Chlamydomonas reinhardtii. Plant Physiol. 1985 Jun;78(2):277–284. doi: 10.1104/pp.78.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ingledew W. J., Poole R. K. The respiratory chains of Escherichia coli. Microbiol Rev. 1984 Sep;48(3):222–271. doi: 10.1128/mr.48.3.222-271.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Keegan F. P., Sansone L., Blum J. J. Oxidation of glucose, ribose, alanine, and glutamate by Leishmania braziliensis panamensis. J Protozool. 1987 May;34(2):174–179. doi: 10.1111/j.1550-7408.1987.tb03156.x. [DOI] [PubMed] [Google Scholar]
  18. Krassner S. M., Flory B. Physiologic interactions between L-proline and D-glucose in Leishmania tarentolae, L. donovani and Trypanosoma scelopori culture forms. Acta Trop. 1977 Jun;34(2):157–166. [PubMed] [Google Scholar]
  19. Kreutzer R. D., Souraty N., Semko M. E. Biochemical identities and differences among Leishmania species and subspecies. Am J Trop Med Hyg. 1987 Jan;36(1):22–32. doi: 10.4269/ajtmh.1987.36.22. [DOI] [PubMed] [Google Scholar]
  20. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  21. Le Blancq S. M., Lanham S. M. Aspartate aminotransferase in Leishmania is a broad-spectrum transaminase. Trans R Soc Trop Med Hyg. 1984;78(3):373–375. doi: 10.1016/0035-9203(84)90125-1. [DOI] [PubMed] [Google Scholar]
  22. Mackenzie N. E., Hall J. E., Flynn I. W., Scott A. I. 13C nuclear magnetic resonance studies of anaerobic glycolysis in Trypanosoma brucei spp. Biosci Rep. 1983 Feb;3(2):141–151. doi: 10.1007/BF01121945. [DOI] [PubMed] [Google Scholar]
  23. Mackenzie N. E., Hall J. E., Seed J. R., Scott A. I. Carbon-13 nuclear-magnetic-resonance studies of glucose catabolism by Trypanosoma brucei gambiense. Eur J Biochem. 1982 Jan;121(3):657–661. doi: 10.1111/j.1432-1033.1982.tb05836.x. [DOI] [PubMed] [Google Scholar]
  24. Martin A. W., Jones R., Mann T. D(--)Lactic acid formation and D(--)lactate dehydrogenase in octopus spermatozoa. Proc R Soc Lond B Biol Sci. 1976 May 18;193(1112):235–243. doi: 10.1098/rspb.1976.0043. [DOI] [PubMed] [Google Scholar]
  25. Martin E., Simon M. W., Schaefer F. W., 3rd, Mukkada A. J. Enzymes of carbohydrate metabolism in four human species of Leishmania: a comparative survey. J Protozool. 1976 Nov;23(4):600–607. doi: 10.1111/j.1550-7408.1976.tb03850.x. [DOI] [PubMed] [Google Scholar]
  26. Medzon E. L., Brady M. L. Direct measurement of acetylesterase in living protist cells. J Bacteriol. 1969 Jan;97(1):402–415. doi: 10.1128/jb.97.1.402-415.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Opperdoes F. R., Borst P., Fonck K. The potential use of inhibitors of glycerol-3-phosphate oxidase for chemotherapy of African trypanosomiasis. FEBS Lett. 1976 Feb 15;62(2):169–172. doi: 10.1016/0014-5793(76)80045-2. [DOI] [PubMed] [Google Scholar]
  28. Prestwich K. N., Ing N. H. The activities of enzymes associated with anaerobic pathways, glycolysis and the Krebs cycle in spiders. Comp Biochem Physiol B. 1982;72(2):295–302. doi: 10.1016/0305-0491(82)90049-9. [DOI] [PubMed] [Google Scholar]
  29. RYLEY J. F. Studies on the metabolism of the Protozoa. 7. Comparative carbohydrate metabolism of eleven species of trypanosome. Biochem J. 1956 Feb;62(2):215–222. doi: 10.1042/bj0620215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Reeves R. E., Warren L. G., Susskind B., Lo H. S. An energy-conserving pyruvate-to-acetate pathway in Entamoeba histolytica. Pyruvate synthase and a new acetate thiokinase. J Biol Chem. 1977 Jan 25;252(2):726–731. [PubMed] [Google Scholar]
  31. Rew R. S., Saz H. J. The carbohydrate metabolism of Brugia pahangi microfilariae. J Parasitol. 1977 Feb;63(1):123–129. [PubMed] [Google Scholar]
  32. SYRETT P. J., WONG H. A. THE FERMENTATION OF GLUCOSE BY CHLORELLA VULGARIS. Biochem J. 1963 Nov;89:308–315. doi: 10.1042/bj0890308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Simon M. W., Jayasimhulu K., Mukkada A. J. The free amino acid pool in Leishmania tropica promastigotes. Mol Biochem Parasitol. 1983 Sep;9(1):47–57. doi: 10.1016/0166-6851(83)90056-7. [DOI] [PubMed] [Google Scholar]
  34. Simon M. W., Mukkada A. J. Intracellular protein degradation in Leishmania tropica promastigotes. Mol Biochem Parasitol. 1983 Jan;7(1):19–26. doi: 10.1016/0166-6851(83)90113-5. [DOI] [PubMed] [Google Scholar]
  35. Steiger R. F., Meshnick S. R. Amino-acid and glucose utilization of Leishmania donovani and L. braziliensis. Trans R Soc Trop Med Hyg. 1977;71(5):441–443. doi: 10.1016/0035-9203(77)90049-9. [DOI] [PubMed] [Google Scholar]
  36. Steinbüchel A., Müller M. Glycerol, a metabolic end product of Trichomonas vaginalis and Tritrichomonas foetus. Mol Biochem Parasitol. 1986 Jul;20(1):45–55. doi: 10.1016/0166-6851(86)90141-6. [DOI] [PubMed] [Google Scholar]
  37. Visser N., Opperdoes F. R. Glycolysis in Trypanosoma brucei. Eur J Biochem. 1980 Feb;103(3):623–632. doi: 10.1111/j.1432-1033.1980.tb05988.x. [DOI] [PubMed] [Google Scholar]
  38. Yoshida N., Camargo E. P. Ureotelism and ammonotelism in trypanosomatids. J Bacteriol. 1978 Dec;136(3):1184–1186. doi: 10.1128/jb.136.3.1184-1186.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. de los Santos C., Buldain G., Frydman B., Cannata J. J., Cazzulo J. J. Carbon-13 nuclear magnetic resonance analysis of [1-13C]glucose metabolism in Crithidia fasciculata. Evidence of CO2 fixation by phosphoenolpyruvate carboxykinase. Eur J Biochem. 1985 Jun 3;149(2):421–429. doi: 10.1111/j.1432-1033.1985.tb08942.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES