Both human ferredoxins equally efficiently rescue ferredoxin deficiency in Trypanosoma brucei

Molecular Microbiology

Volumn 89, Issue 1, 2013, Pages 135-151

  Changmai, Piya ^a   Horáková, Eva ^a   Long, Shaojun ^a,b   Černotíková Stříbrná, Eva ^a   Mcdonald, Lindsay M ^a,c   Bontempi, Esteban J ^a,d   Lukeš, Julius ^a  

^a UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d Ministerio de Salud ^*  (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

FDXA PROTEIN; FDXB PROTEIN; FERREDOXIN; HEME; IRON SULFUR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EUKARYOTE; FLAGELLATE; GENE SILENCING; GENOME; HUMAN; KINETOPLASTIDA; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

CLUSTER ANALYSIS; ELECTRON TRANSPORT; FERREDOXINS; GENE KNOCKDOWN TECHNIQUES; GENETIC COMPLEMENTATION TEST; HUMANS; PHYLOGENY; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; HEXAPODA; KINETOPLASTIDA; MAMMALIA; MASTIGOPHORA (FLAGELLATES); TRYPANOSOMA BRUCEI;

EID: 84879499453     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12264     Document Type: Article

References (67)

1. Adam, A.C., Bornhovd, C., Prokisch, H., Neupert, W., and Hell, K. (2006) The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J 25: 174-183.
2. Alsford, S., Turner, D.J., Obado, S.O., Sanchez-Flores, A., Glover, L., Berriman, M., etal. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 21: 915-924.
3. Barrientos, A., Gouget, K., Horn, D., Soto, I.C., and Fontanesi, F. (2009) Suppression mechanisms of COX assembly defects in yeast and human: insights into the COX assembly process. Biochim Biophys Acta 1793: 97-107.
4. Barros, M.H., and Nobrega, F.G. (1999) YAH1 of Saccharomyces cerevisiae: a new essential gene that codes for a protein homologous to human adrenodoxin. Gene 233: 197-203.
5. Barros, M.H., Carlson, C.G., Glerum, D.M., and Tzagoloff, A. (2001) Involvement of mitochondrial ferredoxin and Cox15p in hydroxylation of heme O. FEBS Lett 492: 133-138.
6. Barros, M.H., Nobrega, F.G., and Tzagoloff, A. (2002) Mitochondrial ferredoxin is required for heme A synthesis in Saccharomyces cerevisiae. J Biol Chem 277: 9997-10002.
7. Besteiro, S., Biran, M., Biteau, N., Coustou, V., Baltz, T., Canioni, P., and Bringaud, F. (2002) Succinate secreted by Trypanosoma brucei is produced by a novel and unique glycosomal enzyme, NADH-dependent fumarate reductase. J Biol Chem 277: 38001-38012.
8. Besteiro, S., Barrett, M., Riviere, L., and Bringaud, F. (2005) Energy generation in insect stages of Trypanosoma brucei: metabolism in flux. Trends Parasitol 21: 185-191.
9. 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.
10. Bringaud, F., Riviere, L., and Coustou, V. (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol 149: 1-9.
11. Bruhn, D.F., Sammartino, M., and Klingbeil, M.M. (2011) Three mitochondrial DNA polymerases are essential for kinetoplast DNA replication and survival of bloodstream form Trypanosoma brucei. Eukaryot Cell 10: 734-743.
12. Carnes, J., Trotter, J.R., Ernst, N.L., Steinberg, A., and Stuart, K. (2005) An essential RNase III insertion editing endonuclease in Trypanosoma brucei. Proc Natl Acad Sci USA 102: 16614-16619.
13. Cavalier-Smith, T. (2010) Deep phylogeny, ancestral groups and the four ages of life. Philos Trans R Soc Lond B Biol Sci 365: 111-132.
14. Chandramouli, K., Unciuleac, M.C., Naik, S., Dean, D.R., Huynh, B.H., and Johnson, M.K. (2007) Formation and properties of [4Fe-4S] clusters on the IscU scaffold protein. Biochemistry 46: 6804-6811.
15. 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.
16. Coustou, V., Biran, M., Besteiro, S., Riviere, L., Baltz, T., Franconi, J.M., and Bringaud, F. (2006) Fumarate is an essential intermediary metabolite produced by the procyclic Trypanosoma brucei. J Biol Chem 281: 26832-26846.
17. Estévez, A.M., Haile, S., Steinbuchel, M., Quijada, L., and Clayton, C. (2004) Effects of depletion and overexpression of the Trypanosoma brucei ribonuclease L inhibitor homologue. Mol Biochem Parasitol 133: 137-141.
18. Ewen, K.M., Kleser, M., and Bernhardt, R. (2011) Adrenodoxin: the archetype of vertebrate-type [2Fe-2S] cluster ferredoxins. Biochim Biophys Acta Proteins Proteomics 1814: 111-125.
19. Gnipová, A., Panicucci, B., Paris, Z., Verner, Z., Horváth, A., Lukeš, J., and Zíková, A. (2012) Disparate phenotypic effects from the knockdown of various Trypanosoma brucei cytochrome c oxidase subunits. Mol Biochem Parasitol 184: 90-98.
20. Grant, P.T., and Sargent, J.R. (1960) Properties of L-α-glycerophosphate oxidase and its role in the respiration of Trypanosoma rhodesiense. Biochem J 76: 229-237.
21. Hashimi, H., Zíková, A., Panigrahi, A.K., Stuart, K.D., and Lukeš, J. (2008) TbRGG1, an essential protein involved in kinetoplastid RNA metabolism that is associated with a novel multiprotein complex. RNA 14: 970-980.
22. Horváth, A., Horáková, E., Dunajčíková, P., Verner, Z., Pravdová, E., Šlapetová, I., etal. (2005) Downregulation of the nuclear-encoded subunits of the complexes III and IV disrupts their respective complexes but not complex I in procyclic Trypanosoma brucei. Mol Microbiol 58: 116-130.
23. Kakuta, Y., Horio, T., Takahashi, Y., and Fukuyama, K. (2001) Crystal structure of Escherichia coli Fdx, an adrenodoxin-type ferredoxin involved in the assembly of iron-sulfur clusters. Biochemistry 40: 11007-11012.
24. Kořený, L., Lukeš, J., and Oborník, M. (2010) Evolution of the haem synthetic pathway in kinetoplastid flagellates: an essential pathway that is not essential after all? Int J Parasitol 40: 149-156.
25. Lange, H., Kaut, A., Kispal, G., and Lill, R. (2000) A mitochondrial ferredoxin is essential for biogenesis of cellular iron-sulfur proteins. Proc Natl Acad Sci USA 97: 1050-1055.
26. Lartillot, N., Lepage, T., and Blanquart, S. (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25: 2286-2288.
27. Li, J., Saxena, S., Pain, D., and Dancis, A. (2001) Adrenodoxin reductase homolog (Arh1p) of yeast mitochondria required for iron homeostasis. J Biol Chem 276: 1503-1509.
28. Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature 460: 831-838.
29. Long, S., Jirků, M., Ayala, F.J., and Lukeš, J. (2008) Mitochondrial localization of human frataxin is necessary but processing is not for rescuing frataxin deficiency in Trypanosoma brucei. Proc Natl Acad Sci USA 105: 13468-13473.
30. Long, S.J., Changmai, P., Tsaousis, A.D., Skalický, T., Verner, Z., Wen, Y.Z., etal. (2011) Stage-specific requirement for Isa1 and Isa2 proteins in the mitochondrion of Trypanosoma brucei and heterologous rescue by human and Blastocystis orthologues. Mol Microbiol 81: 1403-1418.
31. Lukeš, J., Hashimi, H., and Ziková, A. (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet 48: 277-299.
32. Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., etal. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: 225-229.
33. Miao, R., Holmes-Hampton, G., and Lindahl, P.A. (2011) Biophysical Investigation of the Iron in Aft1-1(up) and Gal-YAH1 Saccharomyces cerevisiae. Biochemistry 50: 2660-2671.
34. Michel, H., Behr, J., Harrenga, A., and Kannt, A. (1998) Cytochrome C oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct 27: 329-356.
35. Moraes, C.T., Diaz, F., and Barrientos, A. (2004) Defects in the biosynthesis of mitochondrial heme c and heme a in yeast and mammals. Biochim Biophys Acta Bioenerg 1659: 153-159.
36. Mortenson, L.E., Carnahan, J.E., and Valentine, R.C. (1962) An electron transport factor from Clostridium pasteurianum. Biochem Biophys Res Commun 7: 448-452.
37. Mühlenhoff, U., Gerber, J., Richhardt, N., and Lill, R. (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J 22: 4815-4825.
38. Mühlenhoff, U., Gerl, M.J., Flauger, B., Pirner, H.M., Balser, S., Richhardt, N., etal. (2007) The iron-sulfur cluster proteins Isa1 and Isa2 are required for the function but not for the de novo synthesis of the Fe/S clusters of biotin synthase in Saccharomyces cerevisiae. Eukaryot Cell 6: 753-753.
39. Netz, D.J.A., Stith, C.M., Stumpfig, M., Kopf, G., Vogel, D., Genau, H.M., etal. (2012) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nature Chem Biol 8: 125-132.
40. Paris, Z., Changmai, P., Rubio, M.A., Zíková, A., Stuart, K.D., Alfonzo, J.D., and Lukeš, J. (2010) The Fe/S cluster assembly protein Isd11 is essential for tRNA thiolation in Trypanosoma brucei. J Biol Chem 285: 22394-22402.
41. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
42. Pierrel, F., Hamelin, O., Douki, T., Kieffer-Jaquinod, S., Mühlenhoff, U., Ozeir, M., etal. (2010) Involvement of mitochondrial ferredoxin and para-aminobenzoic acid in yeast coenzyme Q biosynthesis. Chem Biol 17: 449-459.
43. Pusnik, M., Charrière, F., Mäser, P., Waller, R.F., Dagley, M.J., Lithgow, T., and Schneider, A. (2009) The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. Mol Biol Evol 26: 671-680.
44. Py, B., and Barras, F. (2010) Building Fe-S proteins: bacterial strategies. Nat Rev Microbiol 8: 436-446.
45. Rouault, T.A. (2012) Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis Model Mech 5: 155-164.
46. Saas, J., Ziegelbauer, K., von Haeseler, A., Fast, B., and Boshart, M. (2000) A developmentally regulated aconitase related to iron-regulatory protein-1 is localized in the cytoplasm and in the mitochondrion of Trypanosoma brucei. J Biol Chem 275: 2745-2755.
47. Schnaufer, A., Panigrahi, A.K., Panicucci, B., Igo, P., Wirtz, E., Salavati, R., and Stuart, K. (2001) An RNA ligase essential for RNA editing and survival of the bloodstream form of Trypanosoma brucei. Science 291: 2159-2162.
48. Schneider, A., Bursać, D., and Lithgow, T. (2008) The direct route: a simplified pathway for protein import into the mitochondrion of trypanosomes. Trends Cell Biol 18: 12-18.
49. Seeber, F. (2002) Eukaryotic genomes contain a [2Fe-2S] ferredoxin isoform with a conserved C-terminal sequence motif. Trends Biochem Sci 27: 545-547.
50. Sheftel, A.D., Stehling, O., Pierik, A.J., Elsasser, H.P., Mühlenhoff, U., Webert, H., etal. (2010) Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis. Proc Natl Acad Sci USA 107: 11775-11780.
51. Shi, Y.B., Ghosh, M.C., Tong, W.H., and Rouault, T.A. (2009) Human ISD11 is essential for both iron-sulfur cluster assembly and maintenance of normal cellular iron homeostasis. Hum Mol Genet 18: 3014-3025.
52. Shi, Y.B., Ghosh, M., Kovtunovych, G., Crooks, D.R., and Rouault, T.A. (2012) Both human ferredoxins 1 and 2 and ferredoxin reductase are important for iron-sulfur cluster biogenesis. Biochim Biophys Acta Mol Cell Res 1823: 484-492.
53. Singha, U.K., Hamilton, V., Duncan, M.R., Weems, E., Tripathi, M.K., and Chaudhuri, M. (2012) Protein translocase of mitochondrial inner membrane in Trypanosoma brucei. J Biol Chem 287: 14480-14493.
54. Smíd, O., Horáková, E., Vilímová, V., Hrdý, I., Cammack, R., Horváth, A., etal. (2006) Knock-downs of iron-sulfur cluster assembly proteins IscS and IscU down-regulate the active mitochondrion of procyclic Trypanosoma brucei. J Biol Chem 281: 28679-28686.
55. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
56. Stemmler, T.L., Lesuisse, E., Pain, D., and Dancis, A. (2010) Frataxin and mitochondrial FeS cluster biogenesis. J Biol Chem 285: 26737-26743.
57. Sutak, R., Doležal, P., Fiumera, H.L., Hrdý, I., Dancis, A., Delgadillo-Correa, M., etal. (2004) Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc Natl Acad Sci USA 101: 10368-10373.
58. Tielens, A.G., and Van Hellemond, J.J. (1998) The electron transport chain in anaerobically functioning eukaryotes. Biochim Biophys Acta 1365: 71-78.
59. Tokumoto, U., and Takahashi, Y. (2001) Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur protein. J Biochem (Tokyo) 130: 63-71.
60. Tovar, J., Leon-Avila, G., Sanchez, L.B., Šuták, R., Tachezy, J., van der Giezen, M., etal. (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426: 172-176.
61. Tripodi, K.E., Menendez, S.M., and Cricco, J.A. (2011) Role of heme and heme-proteins in trypanosomatid essential metabolic pathways. Enzyme Res 2011: 873230.
62. Tsaousis, A.D., de Choudens, S.O., Gentekaki, E., Long, S.J., Gaston, D., Stechmann, A., etal. (2012) Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis. Proc Natl Acad Sci USA 109: 10426-10431.
63. Vaňáčová, S., Rasoloson, D., Razga, J., Hrdý, I., Kulda, J., and Tachezy, J. (2001) Iron-induced changes in pyruvate metabolism of Tritrichomonas foetus and involvement of iron in expression of hydrogenosomal proteins. Microbiology 147: 53-62.
64. Vondrušková, E., van den Burg, J., Zíková, A., Ernst, N.L., Stuart, K., Benne, R., and Lukeš, J. (2005) RNA interference analyses suggest a transcript-specific regulatory role for mitochondrial RNA-binding proteins MRP1 and MRP2 in RNA editing and other RNA processing in Trypanosoma brucei. J Biol Chem 280: 2429-2438.
65. Wiedemann, N., Urzica, E., Guiard, B., Muller, H., Lohaus, C., Meyer, H.E., etal. (2006) Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins. EMBO J 25: 184-195.
66. Žárský, V., Tachezy, J., and Doležal, P. (2012) Tom40 is likely common to all mitochondria. Curr Biol 22: R479-R481.
67. Zheng, L.M., White, R.H., Cash, V.L., Jack, R.F., and Dean, D.R. (1993) Cysteine desulfurase activity indicates a role for Nifs in metallocluster biosynthesis. Proc Natl Acad Sci USA 90: 2754-2758.