Lipoamide dehydrogenase is essential for both bloodstream and procyclic Trypanosoma brucei

Molecular Microbiology

Volumn 81, Issue 3, 2011, Pages 623-639

  Roldán, Angela ^a   Comini, Marcelo A ^b   Crispo, Martina ^b   Krauth Siegel, R Luise ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

Author keywords

[No Author keywords available]

Indexed keywords

BRANCHED CHAIN AMINO ACID; DIHYDROLIPOAMIDE DEHYDROGENASE; GLYCINE CLEAVAGE SYSTEM; MESSENGER RNA; OXOGLUTARATE DEHYDROGENASE; THYMIDINE PHOSPHATE;

AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD FLOW; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME DEGRADATION; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA INTERFERENCE; TRYPANOSOMA BRUCEI;

ANIMALS; DIHYDROLIPOAMIDE DEHYDROGENASE; DISEASE MODELS, ANIMAL; DNA, PROTOZOAN; GENE DELETION; METABOLIC NETWORKS AND PATHWAYS; MICE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; RODENT DISEASES; SEQUENCE ANALYSIS, DNA; SURVIVAL ANALYSIS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN; VIRULENCE FACTORS;

MUS; TRYPANOSOMA BRUCEI;

EID: 79960718370     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07721.x     Document Type: Article

References (65)

1. Abramoff, M.D., Magelhaes, P.J., and Ram, S.J. (2004) Image processing with ImageJ. Biophotonics Int 11: 36-42.
2. Aussel, C., Cynober, L., Lioret, N., Coudray-Lucas, C., Vaubourdolle, M., Saizy, R., and Giboudeau, J. (1986) Plasma branched-chain keto acids in burn patients. Am J Clin Nutr 44: 825-831.
3. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D.C., etal. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
4. Biebinger, S., Wirtz, L.E., Lorenz, P., and Clayton, C. (1997) Vectors for inducible expression of toxic gene products in bloodstream and procyclic Trypanosoma brucei. Mol Biochem Parasitol 85: 99-112.
5. Blount, B.C., Mack, M.M., Wehr, C.M., MacGregor, J.T., Hiatt, R.A., Wang, G., etal. (1997) Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci USA 94: 3290-3295.
6. Blum, J.J. (1991) Oxidation of leucine by Leishmania donovani. J Protozool 38: 527-531.
7. Blumenstiel, K., Schöneck, R., Yardley, V., Croft, S.L., and Krauth-Siegel, R.L. (1999) Nitrofuran drugs as common subversive substrates of Trypanosoma cruzi lipoamide dehydrogenase and trypanothione reductase. Biochem Pharmacol 58: 1791-1799.
8. Bochud-Allemann, N., and Schneider, A. (2002) Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei. J Biol Chem 277: 32849-32854.
9. Böhringer, S., and Hecker, H. (1975) Quantitative ultrastructural investigations of the life cycle of Trypanosoma brucei: a morphometric analysis. J Protozool 22: 463-467.
10. Breidbach, T., Ngazoa, E., and Steverding, D. (2002) Trypanosoma brucei: in vitro slender-to-stumpy differentiation of culture-adapted, monomorphic bloodstream forms. Exp Parasitol 101: 223-230.
11. Brosnan, J.T., and Brosnan, M.E. (2006) Branched-chain amino acids: enzyme and substrate regulation. J Nutr 136: 207S-211S.
12. Bryk, R., Arango, N., Venugopal, A., Warren, J.D., Park, Y.H., Patel, M.S., etal. (2010) Triazaspirodimethoxybenzoyls as selective inhibitors of mycobacterial lipoamide dehydrogenase. Biochemistry 49: 1616-1627.
13. Castillo-Acosta, V.M., Estévez, A.M., Vidal, A.E., Ruiz-Perez, L.M., and González-Pacanowska, D. (2008) Depletion of dimeric all-alpha dUTPase induces DNA strand breaks and impairs cell cycle progression in Trypanosoma brucei. Int J Biochem Cell Biol 40: 2901-2913.
14. Ceylan, S., Seidel, V., Ziebart, N., Berndt, C., Dirdjaja, N., and Krauth-Siegel, R.L. (2010) The dithiol glutaredoxins of African trypanosomes have distinct roles and are closely linked to the unique trypanothione metabolism. J Biol Chem 45: 35224-35237.
15. Chello, P.L., and Jaffe, J.J. (1972) Comparative properties of trypanosomal and mammalian thymidine kinases. Comp Biochem Physiol B 43: 543-562.
16. Chuang, D.T., Chuang, J.L., and Wynn, R.M. (2006) Lessons from genetic disorders of branched-chain amino acid metabolism. J Nutr 136: 243S-249S.
17. Clarke, S.J., Farrugia, D.C., Aherne, G.W., Pritchard, D.M., Benstead, J., and Jackman, A.L. (2000) Balb/c mice as a preclinical model for raltitrexed-induced gastrointestinal toxicity. Clin Cancer Res 6: 285-296.
18. Colasante, C., Alibu, V.P., Kirchberger, S., Tjaden, J., Clayton, C., and Voncken, F. (2006) Characterization and developmentally regulated localization of the mitochondrial carrier protein homologue MCP6 from Trypanosoma brucei. Eukaryot Cell 5: 1194-1205.
19. Comini, M.A., Rettig, J., Dirdjaja, N., Hanschmann, E.M., Berndt, C., and Krauth-Siegel, R.L. (2008) Monothiol glutaredoxin-1 is an essential iron-sulfur protein in the mitochondrion of African trypanosomes. J Biol Chem 283: 27785-27798.
20. Coustou, V., Biran, M., Breton, M., Guegan, F., Rivière, L., Plazolles, N., etal. (2008) Glucose-induced remodeling of intermediary and energy metabolism in procyclic Trypanosoma brucei. J Biol Chem 283: 16342-16354.
21. Cristodero, M., Seebeck, T., and Schneider, A. (2010) Mitochondrial translation is essential in bloodstream forms of Trypanosoma brucei. Mol Microbiol 78: 757-769.
22. Cunningham, M.P., and Vickerman, K. (1962) Antigenic analysis in the Trypanosoma brucei group, using the agglutination reaction. Trans R Soc Trop Med Hyg 56: 48-59.
23. Danson, M.J., Conroy, K., McQuattie, A., and Stevenson, K.J. (1987) Dihydrolipoamide dehydrogenase from Trypanosoma brucei. Characterization and cellular location. Biochem J 243: 661-665.
24. Durieux, P.O., Schütz, P., Brun, R., and Köhler, P. (1991) Alterations in Krebs cycle enzyme activities and carbohydrate catabolism in two strains of Trypanosoma brucei during in vitro differentiation of their bloodstream to procyclic stages. Mol Biochem Parasitol 45: 19-27.
25. Else, A.J., Hough, D.W., and Danson, M.J. (1993) Cloning, sequencing, and expression of Trypanosoma brucei dihydrolipoamide dehydrogenase. Eur J Biochem 212: 423-429.
26. Else, A.J., Clarke, J.F., Willis, A., Jackman, S.A., Hough, D.W., and Danson, M.J. (1994) Dihydrolipoamide dehydrogenase in the Trypanosoma subgenus, trypanozoon. Mol Biochem Parasitol 64: 233-239.
27. Fenn, K., and Matthews, K.R. (2007) The cell biology of Trypanosoma brucei differentiation. Curr Opin Microbiol 10: 539-546.
28. Ginger, M.L., Prescott, M.C., Reynolds, D.G., Chance, M.L., and Goad, L.J. (2000) Utilization of leucine and acetate as carbon sources for sterol and fatty acid biosynthesis by Old and New World Leishmania species, Endotrypanum monterogeii and Trypanosoma cruzi. Eur J Biochem 267: 2555-2566.
29. Goldshmidt, H., Matas, D., Kabi, A., Carmi, S., Hope, R., and Michaeli, S. (2010) Persistent ER stress induces the spliced leader RNA silencing pathway (SLS), leading to programmed cell death in Trypanosoma brucei. PLoS Pathog 6: e1000731.
30. Gutiérrez-Correa, J. (2010) Trypanosoma cruzi dihydrolipoamide dehydrogenase as target of reactive metabolites generated by cytochrome c/hydrogen peroxide (or linoleic acid hydroperoxide)/phenol systems. Free Radic Res 44: 1345-1358.
31. Hammarton, T.C. (2007) Cell cycle regulation in Trypanosoma brucei. Mol Biochem Parasitol 153: 1-8.
32. Jackman, S.A., Hough, D.W., Danson, M.J., Stevenson, K.J., and Opperdoes, F.R. (1990) Subcellular localisation of dihydrolipoamide dehydrogenase and detection of lipoic acid in bloodstream forms of Trypanosoma brucei. Eur J Biochem 193: 91-95.
33. Kasinski, A., Doering, C.B., and Danner, D.J. (2004) Leucine toxicity in a neuronal cell model with inhibited branched chain amino acid catabolism. Brain Res Mol Brain Res 122: 180-187.
34. Lamour, N., Rivière, L., Coustou, V., Coombs, G.H., Barrett, M.P., and Bringaud, F. (2005) Proline metabolism in procyclic Trypanosoma brucei is down-regulated in the presence of glucose. J Biol Chem 280: 11902-11910.
35. Li, Y., Holmes, W.B., Appling, D.R., and RajBhandary, U.L. (2000) Initiation of protein synthesis in Saccharomyces cerevisiae mitochondria without formylation of the initiator tRNA. J Bacteriol 182: 2886-2892.
36. Lohrer, H., and Krauth-Siegel, R.L. (1990) Purification and characterization of lipoamide dehydrogenase from Trypanosoma cruzi. Eur J Biochem 194: 863-869.
37. Misaka, E., Kawahara, Y., and Nakanishi, K. (1965) Studies on menadione reductase of bakers' yeast. III. The identity of menadione reductase with lipoamide dehydrogenase. J Biochem 58: 436-443.
38. Murta, S.M., Nogueira, F.B., Dos Santos, P.F., Campos, F.M., Volpe, C., Liarte, D.B., etal. (2008) Differential gene expression in Trypanosoma cruzi populations susceptible and resistant to benznidazole. Acta Trop 107: 59-65.
39. Murta, S.M., Vickers, T.J., Scott, D.A., and Beverley, S.M. (2009) Methylene tetrahydrofolate dehydrogenase/cyclohydrolase and the synthesis of 10-CHO-THF are essential in Leishmania major. Mol Microbiol 71: 1386-1401.
40. o-ATPase. Eur J Biochem 209: 207-216.
41. Ochsenreiter, T., Cipriano, M., and Hajduk, S.L. (2008) Alternative mRNA editing in trypanosomes is extensive and may contribute to mitochondrial protein diversity. PLoS ONE 3: e1566.
42. Opperdoes, F.R., Baudhuin, P., Coppens, I., De Roe, C., Edwards, S.W., Weijers, P.J., and Misset, O. (1984) Purification, morphometric analysis, and characterization of the glycosomes (microbodies) of the protozoan hemoflagellate Trypanosoma brucei. J Cell Biol 98: 1178-1184.
43. Petrat, F., Paluch, S., Dogruöz, E., Dörfler, P., Kirsch, M., Korth, H.G., etal. (2003) Reduction of Fe(III) ions complexed to physiological ligands by lipoyl dehydrogenase and other flavoenzymes in vitro: implications for an enzymatic reduction of Fe(III) ions of the labile iron pool. J Biol Chem 278: 46403-46413.
44. Pino, P., Aeby, E., Foth, B.J., Sheiner, L., Soldati, T., Schneider, A., and Soldati-Favre, D. (2010) Mitochondrial translation in absence of local tRNA aminoacylation and methionyl tRNA Met formylation in Apicomplexa. Mol Microbiol 76: 706-718.
45. Ramos, E.I., Garza, K.M., Krauth-Siegel, R.L., Bader, J., Martinez, L.E., and Maldonado, R.A. (2009) 2, 3-Diphenyl-1, 4-naphthoquinone: a potential chemotherapeutic agent against Trypanosoma cruzi. J Parasitol 95: 461-466.
46. Richterová, L., Vávrová, Z., and Lukeš, J. (2011) DEAD-box RNA helicase is dispensable for mitochondrial translation in Trypanosoma brucei. Exp Parasitol 127: 300-303.
47. Salmon-Chemin, L., Buisine, E., Yardley, V., Kohler, S., Debreu, M.A., Landry, V., etal. (2001) 2- and 3-substituted 1, 4-naphthoquinone derivatives as subversive substrates of trypanothione reductase and lipoamide dehydrogenase from Trypanosoma cruzi: synthesis and correlation between redox cycling activities and in vitro cytotoxicity. J Med Chem 44: 548-565.
48. Schaer, J.C., Maurer, U., and Schindler, R. (1978) Determination of thymidine in serum used for cell culture media. Exp Cell Biol 46: 1-10.
49. Schlecker, T., Schmidt, A., Dirdjaja, N., Voncken, F., Clayton, C., and Krauth-Siegel, R.L. (2005) Substrate specificity, localization, and essential role of the glutathione peroxidase-type tryparedoxin peroxidases in Trypanosoma brucei. J Biol Chem 280: 14385-14394.
50. Schnaufer, A., Clark-Walker, G.D., Steinberg, A.G., and Stuart, K. (2005) The F1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J 24: 4029-4040.
51. Schöneck, R., Billaut-Mulot, O., Numrich, P., Ouaissi, M.A., and Krauth-Siegel, R.L. (1997) Cloning, sequencing and functional expression of dihydrolipoamide dehydrogenase from the human pathogen Trypanosoma cruzi. Eur J Biochem 243: 739-747.
52. Scott, D.A., Hickerson, S.M., Vickers, T.J., and Beverley, S.M. (2008) The role of the mitochondrial glycine cleavage complex in the metabolism and virulence of the protozoan parasite Leishmania major. J Biol Chem 283: 155-165.
53. Sienkiewicz, N., Jaroslawski, S., Wyllie, S., and Fairlamb, A.H. (2008) Chemical and genetic validation of dihydrofolate reductase-thymidylate synthase as a drug target in African trypanosomes. Mol Microbiol 69: 520-533.
54. Sreider, C.M., Grinblat, L., and Stoppani, A.O. (1992) Reduction of nitrofuran compounds by heart lipoamide dehydrogenase: role of flavin and the reactive disulfide groups. Biochem Int 28: 323-334.
55. Stephens, J.L., Lee, S.H., Paul, K.S., and Englund, P.T. (2007) Mitochondrial fatty acid synthesis in Trypanosoma brucei. J Biol Chem 282: 4427-4436.
56. Tan, T.H., Bochud-Allemann, N., Horn, E.K., and Schneider, A. (2002) Eukaryotic-type elongator tRNAMet of Trypanosoma brucei becomes formylated after import into mitochondria. Proc Natl Acad Sci USA 99: 1152-1157.
57. Tasker, M., Wilson, J., Sarkar, M., Hendriks, E., and Matthews, K. (2000) A novel selection regime for differentiation defects demonstrates an essential role for the stumpy form in the life cycle of the African trypanosome. Mol Biol Cell 11: 1905-1917.
58. Thiel, M., Harder, S., Wiese, M., Kroemer, M., and Bruchhaus, I. (2008) Involvement of a Leishmania thymidine kinase in flagellum formation, promastigote shape and growth as well as virulence. Mol Biochem Parasitol 158: 152-162.
59. Tielens, A.G., and Van Hellemond, J.J. (1998) Differences in energy metabolism between trypanosomatidae. Parasitol Today 14: 265-272.
60. Tyler, K.M., Matthews, K.R., and Gull, K. (1997) The bloodstream differentiation-division of Trypanosoma brucei studied using mitochondrial markers. Proc Biol Sci 264: 1481-1490.
61. Vassella, E., Reuner, B., Yutzy, B., and Boshart, M. (1997) Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. J Cell Sci 110: 2661-2671.
62. Vickers, T.J., Murta, S.M., Mandell, M.A., and Beverley, S.M. (2009) The enzymes of the 10-formyl-tetrahydrofolate synthetic pathway are found exclusively in the cytosol of the trypanosomatid parasite Leishmania major. Mol Biochem Parasitol 166: 142-152.
63. van Weelden, S.W., Fast, B., Vogt, A., van der Meer, P., Saas, J., van Hellemond, J.J., etal. (2003) Procyclic Trypanosoma brucei do not use Krebs cycle activity for energy generation. J Biol Chem 278: 12854-12863.
64. van Weelden, S.W., van Hellemond, J.J., Opperdoes, F.R., and Tielens, A.G. (2005) New functions for parts of the Krebs cycle in procyclic Trypanosoma brucei, a cycle not operating as a cycle. J Biol Chem 280: 12451-12460.
65. Werner, C., Stubbs, M.T., Klebe, G., and Krauth-Siegel, R.L. (2002) The crystal structure of lipoamide dehydrogenase from Trypanosoma cruzi: a target for the design of new drugs against Chagas' disease. In Flavins and Flavoproteins. Chapman, S., Perham, R., and Scrutton, N. (eds). Berlin: Dr. Rudolf Weber Agency for Scientific Publications, pp. 917-922.