Differential expression of glycosomal and mitochondrial proteins in the two major life-cycle stages of Trypanosoma brucei

Molecular and Biochemical Parasitology

Volumn 158, Issue 2, 2008, Pages 189-201

  Vertommen, Didier ^a   Van Roy, Joris ^a   Szikora, Jean Pierre ^a   Rider, Mark H ^a   Michels, Paul A M ^a   Opperdoes, Fred R ^a  

^a DE DUVE INSTITUTE   (Belgium)

Author keywords

Cell fractionation; Glycolysis; Glycosome; Liquid chromatography; Mass spectrometry; Metabolism; Mitochondrion; Proteomics; Trypanosoma brucei

Indexed keywords

6 PHOSPHOFRUCTOKINASE; CYTOCHROME C; CYTOCHROME C OXIDASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE (NAD); GLYCEROL KINASE; GLYCOPROTEIN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEXOKINASE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INOSINATE DEHYDROGENASE; IRON SULFUR PROTEIN; ISOMERASE; MITOCHONDRIAL PROTEIN; PEROXIDASE; PYRUVATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE; SUPEROXIDE DISMUTASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; LIFE CYCLE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE METABOLISM; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TRYPANOSOMA BRUCEI;

ANIMALS; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION; LIFE CYCLE STAGES; MASS SPECTROMETRY; MICROBODIES; MITOCHONDRIAL PROTEINS; PARASITEMIA; PROTEOMICS; PROTOZOAN PROTEINS; RATS; RATS, WISTAR; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

HEXAPODA; TRYPANOSOMA BRUCEI;

EID: 39049118320     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2007.12.008     Document Type: Article

References (48)

1. Opperdoes F.R., Markos A., and Steiger R.F. Localization of malate dehydrogenase, adenylate kinase and glycolytic enzymes in glycosomes and the threonine pathway in the mitochondrion of cultured procyclic trypomastigotes of Trypanosoma brucei. Mol Biochem Parasitol 4 (1981) 291-309
2. Bowman I.B.R. Intermediary metabolism of pathogenic flagellates. Trypanosomiases and leishmaniases with special reference to Chagas' disease. CIBA Foundation Symposium 20 (New Series) (1974), Elsevier/North-Holland Biomedical Press, Amsterdam 255-271
3. Opperdoes F.R., Baudhuin P., Coppens I., et al. Purification, morphometric analysis, and characterization of the glycosomes (microbodies) of the protozoan hemoflagellate Trypanosoma brucei. J Cell Biol 98 (1984) 1178-1184
4. Tetley L., and Vickerman K. The glycosomes of trypanosomes: number and distribution as revealed by electron spectroscopic imaging and 3-D reconstruction. J Microsc 162 (1991) 83-90
5. Michels P.A., Bringaud F., Herman M., and Hannaert V. Metabolic functions of glycosomes in trypanosomatids. Biochim Biophys Acta 1763 (2006) 1463-1477
6. Berens R.L., Brun R., and Krassner S.M. A simple monophasic medium for axenic culture of hemoflagellates. J Parasitol 62 (1976) 360-365
7. Lanham S.M., and Godfrey D.G. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp Parasitol 28 (1970) 521-534
8. Opperdoes F.R. Compartmentation of carbohydrate metabolism in trypanosomes. Annu Rev Microbiol 41 (1987) 127-151
9. Misset O., and Opperdoes F.R. Simultaneous purification of hexokinase, class-I fructose-bisphosphate aldolase, triosephosphate isomerase and phosphoglycerate kinase from Trypanosoma brucei. Eur J Biochem 144 (1984) 475-483
10. Misset O., Bos O.J., and Opperdoes F.R. Glycolytic enzymes of Trypanosoma brucei. Simultaneous purification, intraglycosomal concentrations and physical properties. Eur J Biochem 157 (1986) 441-453
11. Hart D.T., Misset O., Edwards S.W., and Opperdoes F.R. A comparison of the glycosomes (microbodies) isolated from Trypanosoma brucei bloodstream form and cultured procyclic trypomastigotes. Mol Biochem Parasitol 12 (1984) 25-35
12. Opperdoes F.R., and Szikora J.P. In silico prediction of the glycosomal enzymes of Leishmania major and trypanosomes. Mol Biochem Parasitol 147 (2006) 193-206
13. Colasante C., Ellis M., Ruppert T., and Voncken F. Comparative proteomics of glycosomes from bloodstream form and procyclic culture form Trypanosoma brucei brucei. Proteomics 6 (2006) 3275-3293
14. Foucher A.L., McIntosh A., Douce G., Wastling J., Tait A., and Turner C.M. A proteomic analysis of arsenical drug resistance in Trypanosoma brucei. Proteomics 6 (2006) 2726-2732
15. Jones A., Faldas A., Foucher A., Hunt E., Tait A., Wastling J.M., and Turner C.M. Visualisation and analysis of proteomic data from the procyclic form of Trypanosoma brucei. Proteomics 6 (2006) 259-267
16. Opperdoes F.R., Borst P., Bakker S., and Leene W. Localization of glycerol-3-phosphate oxidase in the mitochondrion and particulate NAD-linked glycerol-3-phosphate dehydrogenase in the microbodies of the bloodstream form to Trypanosoma brucei. Eur J Biochem 76 (1977) 29-39
17. Opperdoes F.R. A rapid method for the isolation of intact glycosomes from Trypanosoma brucei by Percoll-gradient centrifugation in a vertical rotor. Mol Biochem Parasitol 3 (1981) 181-186
18. Liu H., Sadygov R.G., and Yates III J.R. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76 (2004) 4193-4201
19. Vertommen D., Depuydt M., Pan J., et al. The disulphide isomerase DsbC cooperates with the oxidase DsbA in a DsbD-independent manner. Mol Microbiol 67 (2008) 336-349
20. Old W.M., Meyer-Arendt K., Aveline-Wolf L., et al. Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteomics 4 (2005) 1487-1502
21. Coustou V., Biran M., Besteiro S., et al. Fumarate is an essential intermediary metabolite produced by the procyclic Trypanosoma brucei. J Biol Chem 281 (2006) 26832-26846
22. Getachew F., and Gedamu L. Leishmania donovani iron superoxide dismutase A is targeted to the mitochondria by its N-terminal positively charged amino acids. Mol Biochem Parasitol 154 (2007) 62-69
23. Roper J.R., Guther M.L., Macrae J.I., et al. The suppression of galactose metabolism in procylic form Trypanosoma brucei causes cessation of cell growth and alters procyclin glycoprotein structure and copy number. J Biol Chem 280 (2005) 19728-19736
24. Turnock D.C., and Ferguson M.A. Sugar Nucleotide Pools of Trypanosoma brucei, Trypanosoma cruzi, and Leishmania major. Eukaryot Cell 6 (2007) 1450-1463
25. Cronin C.N., Nolan D.P., and Voorheis H.P. The enzymes of the classical pentose phosphate pathway display differential activities in procyclic and bloodstream forms of Trypanosoma brucei. FEBS Lett 244 (1989) 26-30
26. Berriman M., Ghedin E., Hertz-Fowler C., et al. The genome of the African trypanosome Trypanosoma brucei. Science 309 (2005) 416-422
27. Hammond D.J., Gutteridge W.E., and Opperdoes F.R. A novel location for two enzymes of de novo pyrimidine biosynthesis in trypanosomes and Leishmania. FEBS Lett 128 (1981) 27-29
28. Shih S., Hwang H.Y., Carter D., Stenberg P., and Ullman B. Localization and targeting of the Leishmania donovani hypoxanthine-guanine phosphoribosyltransferase to the glycosome. J Biol Chem 273 (1998) 1534-1541
29. Bringaud F., Baltz D., and Baltz T. Functional and molecular characterization of a glycosomal PPi dependent enzyme in trypanosomatids: pyruvate, phosphate dikinase. Proc Natl Acad Sci USA 95 (1998) 7963-7968
30. 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
31. 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
32. Ginger M.L., Chance M.L., Sadler I.H., and Goad L.J. The biosynthetic incorporation of the intact leucine skeleton into sterol by the trypanosomatid Leishmania mexicana. J Biol Chem 276 (2001) 11674-11682
33. Heise N., and Opperdoes F.R. Localisation of a 3-hydroxy-3-methylglutaryl-coenzyme A reductase in the mitochondrial matrix of Trypanosoma brucei procyclics. Z Naturforsch [C] 55 (2000) 473-477
34. Heise N., and Opperdoes F.R. Purification, localisation and characterisation of glucose-6-phosphate dehydrogenase of Trypanosoma brucei. Mol Biochem Parasitol 99 (1999) 21-32
35. Opperdoes F.R. Localization of the initial steps in alkoxyphospholipid biosynthesis in glycosomes (microbodies) of Trypanosoma brucei. FEBS Lett 169 (1984) 35-39
36. Voncken F., van Hellemond J.J., Pfisterer I., Maier A., Hillmer S., and Clayton C. Depletion of GIM5 causes cellular fragility, a decreased glycosome number, and reduced levels of ether-linked phospholipids in trypanosomes. J Biol Chem 278 (2003) 35299-35310
37. Opperdoes F.R., and Cottem D. Involvement of the glycosome of Trypanosoma brucei in carbon dioxide fixation. FEBS Lett 143 (1982) 60-64
38. Plewes K.A., Barr S.D., and Gedamu L. Iron superoxide dismutases targeted to the glycosomes of Leishmania chagasi are important for survival. Infect Immun 71 (2003) 5910-5920
39. 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
40. Lorenz P., Maier A.G., Baumgart E., Erdmann R., and Clayton C. Elongation and clustering of glycosomes in Trypanosoma brucei overexpressing the glycosomal Pex11p. EMBO J 17 (1998) 3542-3555
41. Bringaud F., Peyruchaud S., Baltz D., Giroud C., Simpson L., and Baltz T. Molecular characterization of the mitochondrial heat shock protein 60 gene from Trypanosoma brucei. Mol Biochem Parasitol 74 (1995) 119-123
42. Engman D.M., Kirchhoff L.V., and Donelson J.E. Molecular cloning of mtp70, a mitochondrial member of the hsp70 family. Mol Cell Biol 9 (1989) 5163-5168
43. Koller J., Muller U.F., Schmid B., Missel A., Kruft V., Stuart K., and Goringer H.U. Trypanosoma brucei gBP21. An arginine-rich mitochondrial protein that binds to guide RNA with high affinity. J Biol Chem 272 (1997) 3749-3757
44. Opperdoes FR, Michels PAM. Complex I of Trypanosomatidae, does it exist? Trends Parasitol, in press.
45. Moyersoen J., Choe J., Fan E., Hol W.G., and Michels P.A. Biogenesis of peroxisomes and glycosomes: trypanosomatid glycosome assembly is a promising new drug target. FEMS Microbiol Rev 28 (2004) 603-643
46. Zomer A.W., Opperdoes F.R., and van den Bosch H. Alkyl dihydroxyacetone phosphate synthase in glycosomes of Trypanosoma brucei. Biochim Biophys Acta 1257 (1995) 167-173
47. Estevez A.M., Kierszenbaum F., Wirtz E., Bringaud F., Grunstein J., and Simpson L. Knockout of the glutamate dehydrogenase gene in bloodstream Trypanosoma brucei in culture has no effect on editing of mitochondrial mRNAs. Mol Biochem Parasitol 100 (1999) 5-17
48. Riviere 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