Energy metabolism of trypanosomatids: Adaptation to available carbon sources

Molecular and Biochemical Parasitology

Volumn 149, Issue 1, 2006, Pages 1-9

  Bringaud, Frédéric ^a   Rivière, Loïc ^a   Coustou, Virginie ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Aerobic fermentation; ATP production; Energy metabolism; Glucose; Glucose repression effect; l Proline; Leishmania; Trypanosoma

Indexed keywords

ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; AMINO ACID; CARBON; GLUCOSE; LACTIC ACID; PROLINE; SUCCINIC ACID;

ADAPTATION; AEROBIC FERMENTATION; CARBON SOURCE; CATABOLISM; CRITHIDIA; CULTURE MEDIUM; DEVELOPMENTAL STAGE; ENERGY METABOLISM; IN VITRO STUDY; INSECT DEVELOPMENT; METABOLIC REGULATION; MICROBIAL GROWTH; NONHUMAN; NUCLEOTIDE METABOLISM; OXIDATION; OXIDATION REDUCTION REACTION; PARASITE DEVELOPMENT; PRIORITY JOURNAL; REVIEW; SPECIES HABITAT; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

CRITHIDIA; INSECTA; PROTOZOA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

EID: 33745810581     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2006.03.017     Document Type: Review

References (56)

1. Berriman M., Ghedin E., Hertz-Fowler C., et al. The genome of the African trypanosome Trypanosoma brucei. Science 309 (2005) 416-422
2. El-Sayed N.M., Myler P.J., Bartholomeu D.C., et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309 (2005) 409-415
3. Ivens A.C., Peacock C.S., Worthey E.A., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 309 (2005) 436-442
4. Cannata J.J., and Cazzulo J.J. The aerobic fermentation of glucose by Trypanosoma cruzi. Comp Biochem Physiol B 79 (1984) 297-308
5. Fairlamb A.H., and Opperdoes F.R. Carbohydrate metabolism in African trypanosomes, with special reference to the glycosome. In: Morgan M.J. (Ed). Carbohydrate metabolism in cultured cells (1986), Plenum Publishing Corporation 183-224
6. Bursell E. The role of proline in energy metabolism. In: Downer R.G.H. (Ed). Energy metabolism in insects (1981), Plenum Press, New York 135-154
7. Marr J.J., and Berens R.L. Regulation of aerobic fermentation in protozoans. VI. Comparative biochemistry of pathogenic and nonpathogenic protozoans. Acta Trop 34 (1977) 143-155
8. Cazzulo J.J. Protein and amino acid catabolism in Trypanosoma cruzi. Comp Biochem Physiol B 79 (1984) 309-320
9. Cazzulo J.J., Franke de Cazzulo B.M., Engel J.C., and Cannata J.J. End products and enzyme levels of aerobic glucose fermentation in trypanosomatids. Mol Biochem Parasitol 16 (1985) 329-343
10. Cazzulo J.J. Intermediate metabolism in Trypanosoma cruzi. J Bioenerg Biomembr 26 (1994) 157-165
11. North M.J., and Lockwood B.C. Amino acid and protein metabolism. In: Marr J., and Muller M. (Eds). Biochemistry and molecular biology of parasites (1995), Academic Press Ltd. 67-88
12. Lamour N., Riviere L., Coustou V., Coombs G.H., Barrett M.P., and Bringaud F. Proline metabolism in procyclic Trypanosoma brucei is down-regulated in the presence of glucose. J Biol Chem 280 (2005) 11902-11910
13. Chamond N., Gregoire C., Coatnoan N., et al. Biochemical characterization of proline racemases from the human protozoan parasite Trypanosoma cruzi and definition of putative protein signatures. J Biol Chem 278 (2003) 15484-15494
14. Atwood III J.A., Weatherly D.B., Minning T.A., et al. The Trypanosoma cruzi proteome. Science 309 (2005) 473-476
15. Chaumont F., Schanck A.N., Blum J.J., and Opperdoes F.R. Aerobic and anaerobic glucose metabolism of Phytomonas sp. isolated from Euphorbia characias. Mol Biochem Parasitol 67 (1994) 321-331
16. Hart D.T., and Coombs G.H. Leishmania mexicana: energy metabolism of amastigotes and promastigotes. Exp Parasitol 54 (1982) 397-409
17. Berman J.D., Gallalee J.V., Best J.M., and Hill T. Uptake, distribution, and oxidation of fatty acids by Leishmania mexicana amastigotes. J Parasitol 73 (1987) 555-560
18. Ullu E., Tschudi C., and Chakraborty T. RNA interference in protozoan parasites. Cell Microbiol 6 (2004) 509-519
19. Hannaert V., Bringaud F., Opperdoes F.R., and Michels P.A. Evolution of energy metabolism and its compartmentation in Kinetoplastida. Kinetoplastid Biol Dis 2 (2003) 1-30
20. Van Hellemond J.J., Bakker B.M., and Tielens A.G. Energy metabolism and its compartmentation in Trypanosoma brucei. Adv Microb Physiol 50 (2005) 199-226
21. Van Weelden S.W., Fast B., Vogt A., et al. Procyclic Trypanosoma brucei do not use Krebs cycle activity for energy generation. J Biol Chem 278 (2003) 12854-12863
22. Van Weelden S.W., Van Hellemond J.J., Opperdoes F.R., and Tielens A.G. New functions for parts of the Krebs cycle in procyclic Trypanosoma brucei, a cycle not operating as a cycle. J Biol Chem 280 (2005) 12451-12460
23. Furuya T., Kessler P., Jardim A., Schnaufer A., Crudder C., and Parsons M. Glucose is toxic to glycosome-deficient trypanosomes. Proc Natl Acad Sci USA 99 (2002) 14177-14182
24. Morris J.C., Wang Z., Drew M.E., and Englund P.T. Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. EMBO J 21 (2002) 4429-4438
25. Cross G.A., Klein R.A., and Linstead D.J. Utilization of amino acids by Trypanosoma brucei in culture: l-threonine as a precursor for acetate. Parasitology 71 (1975) 311-326
26. Turrens J. More differences in energy metabolism between Trypanosomatidae. Parasitol Today 15 (1999) 346-348
27. Tielens A.G., and Van Hellemond J.J. Reply. Parasitol Today 15 (1999) 347-348
28. Besteiro S., Biran M., Biteau N., et al. Succinate secreted by Trypanosoma brucei is produced by a novel and unique glycosomal enzyme. NADH-dependent fumarate reductase. J Biol Chem 277 (2002) 38001-38012
29. Coustou V., Besteiro S., Riviere L., et al. A mitochondrial NADH-dependent fumarate reductase involved in the production of succinate excreted by procyclic Trypanosoma brucei. J Biol Chem 280 (2005) 16559-16570
30. Colasante C, Ellis M, Ruppert T, Voncken F. Comparative proteomics of glycosomes from bloodstream form and procyclic culture form Trypanosoma brucei brucei. Proteomics, in press.
31. Annoura T., Nara T., Makiuchi T., Hashimoto T., and Aoki T. The origin of dihydroorotate dehydrogenase genes of kinetoplastids, with special reference to their biological significance and adaptation to anaerobic, parasitic conditions. J Mol Evol 60 (2005) 113-127
32. Takashima E., Inaoka D.K., Osanai A., et al. Characterization of the dihydroorotate dehydrogenase as a soluble fumarate reductase in Trypanosoma cruzi. Mol Biochem Parasitol 122 (2002) 189-200
33. Bochud-Allemann N., and Schneider A. Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei. J Biol Chem 277 (2002) 32849-32854
34. Gilbert R.J., and Klein R.A. Pyruvate kinase: a carnitine-regulated site of ATP production in Trypanosoma brucei brucei. Comp Biochem Physiol B 78 (1984) 595-599
35. Van Hellemond J.J., Opperdoes F.R., and Tielens A.G. Trypanosomatidae produce acetate via a mitochondrial acetate: succinate CoA transferase. Proc Natl Acad Sci USA 95 (1998) 3036-3041
36. Rivière L., Van Weelden S.W., Glass P., et al. Acetyl: succinate CoA-transferase in procyclic Trypanosoma brucei. Gene identification and role in carbohydrate metabolism. J Biol Chem 279 (2004) 45337-45346
37. Takasaki K., Shoun H., Yamaguchi M., et al. Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol. Role of acetyl CoA synthetase in anaerobic ATP synthesis. J Biol Chem 279 (2004) 12414-12420
38. Schmalix W., and Bandlow W. The ethanol-inducible YAT1 gene from yeast encodes a presumptive mitochondrial outer carnitine acetyltransferase. J Biol Chem 268 (1993) 27428-27439
39. Hiesinger M., Wagner C., and Schuller H.J. The acetyl-CoA synthetase gene ACS2 of the yeast Saccharomyces cerevisiae is coregulated with structural genes of fatty acid biosynthesis by the transcriptional activators Ino2p and Ino4p. FEBS Lett 415 (1997) 16-20
40. Klein R.A., Angus J.M., and Waterhouse A.E. Carnitine in Trypanosoma brucei brucei. Mol Biochem Parasitol 6 (1982) 93-110
41. Cazzulo J.J. Aerobic fermentation of glucose by trypanosomatids. FASEB J 6 (1992) 3153-3161
42. Darling T.N., Balber A.E., and Blum J.J. A comparative study of d-lactate, l-lactate and glycerol formation by four species of Leishmania and by Trypanosoma lewisi and Trypanosoma brucei gambiense. Mol Biochem Parasitol 30 (1988) 253-257
43. Darling T.N., and Blum J.J. d-Lactate production by Leishmania braziliensis through the glyoxalase pathway. Mol Biochem Parasitol 28 (1988) 121-127
44. Vickers T.J., Greig N., and Fairlamb A.H. A trypanothione-dependent glyoxalase I with a prokaryotic ancestry in Leishmania major. Proc Natl Acad Sci USA 101 (2004) 13186-13191
45. Irsch T., and Krauth-Siegel R.L. Glyoxalase II of African trypanosomes is trypanothione-dependent. J Biol Chem 279 (2004) 22209-22217
46. Coustou V., Besteiro S., Biran M., et al. ATP generation in the Trypanosoma brucei procyclic form: cytosolic substrate level phosphorylation is essential, but not oxidative phosphorylation. J Biol Chem 278 (2003) 49625-49635
47. Besteiro S., Barrett M.P., Riviere L., and Bringaud F. Energy generation in insect stages of Trypanosoma brucei: metabolism in flux. Trends Parasitol 21 (2005) 185-191
48. Brown G.C. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J 284 (1992) 1-13
49. Van Hellemond J.J., and Tielens A.G. Inhibition of the respiratory chain results in a reversible metabolic arrest in Leishmania promastigotes. Mol Biochem Parasitol 85 (1997) 135-138
50. Stoppani A.O., Docampo R., de Boiso J.F., and Frasch A.C. Effect of inhibitors of electron transport and oxidative phosphorylation on Trypanosoma cruzi respiration and growth. Mol Biochem Parasitol 2 (1980) 3-21
51. Manning G., and Krasnow M.A. Development of the Drosophila tracheal system. In: Martinez-Arias A., and Bate M. (Eds). The development of Drosophila (1993), Cold Spring Harbor Press, Cold Spring Harbor, New York 609-685
52. El-Sayed N.M., Myler P.J., Blandin G., et al. Comparative genomics of trypanosomatid parasitic protozoa. Science 309 (2005) 404-409
53. Sanchez-Moreno M., Fernandez-Becerra M.C., Castilla-Calvente J.J., and Osuna A. Metabolic studies by 1H NMR of different forms of Trypanosoma cruzi as obtained by 'in vitro' culture. FEMS Microbiol Lett 133 (1995) 119-125
54. Rainey P.M., and MacKenzie N.E. A carbon-13 nuclear magnetic resonance analysis of the products of glucose metabolism in Leishmania pifanoi amastigotes and promastigotes. Mol Biochem Parasitol 45 (1991) 307-315
55. Darling T.N., Davis D.G., London R.E., and Blum J.J. Products of Leishmania braziliensis glucose catabolism: release of d-lactate and, under anaerobic conditions, glycerol. Proc Natl Acad Sci USA 84 (1987) 7129-7133
56. Gilroy F.V., Edwards M.R., Norton R.S., and O'Sullivan W.J. Metabolic studies of the protozoan parasite, Crithidia luciliae, using proton nuclear magnetic resonance spectroscopy. Mol Biochem Parasitol 31 (1988) 107-115