Cytosolic iron-sulphur protein assembly is functionally conserved and essential in procyclic and bloodstream Trypanosoma brucei

Molecular Microbiology

Volumn 93, Issue 5, 2014, Pages 897-910

  Basu, Somsuvro ^a,b   Netz, Daili J ^c,d   Haindrich, Alexander C ^b   Herlerth, Nils ^c,d   Lagny, Thibaut J ^c   Pierik, Antonio J ^c,e   Lill, Roland ^c,d,f   Lukeš, Julius ^a,b  

^a INSTITUTE OF PARASITOLOGY   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^e Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^f Offensive for the Development of Scientific and Economic Excellence of the State of Hesse LOEWE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; CYTOSOLIC IRON SULFUR PROTEIN; IRON SULFUR PROTEIN; MEMBRANE PROTEIN; PROTEIN TBCFD1; PROTEIN TBCIA1; PROTEIN TBDRE2; PROTEIN TBNAR1; PROTEIN TBNBP35; PROTEIN TBTAH18; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG; PROTOZOAL PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; BIOGENESIS; CELL FRACTIONATION; CHROMATOPHORE; CONTROLLED STUDY; ELECTROPORATION; ENZYME ACTIVITY; GENETIC CONSERVATION; GROWTH RATE; MITOCHONDRION; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PURIFICATION; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TRYPANOSOMA BRUCEI; AFRICAN TRYPANOSOMIASIS; AMINO ACID SEQUENCE; CHEMISTRY; CYTOSOL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; EXCAVATA; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; CYTOSOL; HUMANS; IRON-SULFUR PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

EID: 84906933588     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12706     Document Type: Article

References (57)

1. Ali, V., and Nozaki, T. (2013) Iron-sulphur clusters, their biosynthesis, and biological functions in protozoan parasites. Adv Parasitol 83: 1-92.
2. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
3. Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B.P., Carrington, M., etal. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38: D457-D462.
4. Balk, J., Pierik, A.J., Netz, D.J., Mühlenhoff, U., and Lill, R. (2004) The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J 23: 2105-2115.
5. Balk, J., Netz, D.J., Tepper, K., Pierik, A.J., and Lill, R. (2005) The essential WD40 protein Cia1 is involved in a late step of cytosolic and nuclear iron-sulfur protein assembly. Mol Cell Biol 25: 10833-10841.
6. Banci, L., Ciofi-Baffoni, S., Mikolajczyk, M., Winkelmann, J., Bill, E., and Pandelia, M.E. (2013) Human anamorsin binds [2Fe-2S] clusters with unique electronic properties. J Biol Inorg Chem 18: 883-893.
7. Basu, S., Leonard, J.C., Desai, N., Mavridou, D.A., Tang, K.H., Goddard, A.D., etal. (2013) Divergence of Erv1-associated mitochondrial import and export pathways in trypanosomes and anaerobic protists. Eukaryot Cell 12: 343-355.
8. Bernard, D.G., Netz, D.J., Lagny, T.J., Pierik, A.J., and Balk, J. (2013) Requirements of the cytosolic iron-sulfur cluster assembly pathway in Arabidopsis. Philos Trans R Soc Lond B Biol Sci 368: 20120259.
9. Bringaud, F., Rivière, L., and Coustou, V. (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol 149: 1-9.
10. Brun, R., and Schönenberger (1979) Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop 36: 289-292.
11. Bruske, E.I., Sendfeld, F., and Schneider, A. (2009) Thiolated tRNAs of Trypanosoma brucei are imported into mitochondria and dethiolated after import. J Biol Chem 284: 36491-36499.
12. Bych, K., Netz, D.J., Vigani, G., Bill, E., Lill, R., Pierik, A.J., and Balk, J. (2008) The essential cytosolic iron-sulfur protein Nbp35 acts without Cfd1 partner in the green lineage. J Biol Chem 283: 35797-35804.
13. Changmai, P., Horáková, E., Long, S., Černotíková-Stříbrná, E., McDonald, L.M., Bontempi, E.J., and Lukeš, J. (2013) Both human ferredoxins equally efficiently rescue ferredoxin deficiency in Trypanosoma brucei. Mol Microbiol 89: 135-151.
14. Clarkson, A.B., Jr, Bienen, E.J., Pollakis, G., and Grady, R.W. (1989) Respiration of bloodstream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase. J Biol Chem 264: 17770-17776.
15. Gari, K., Ortiz, A.M., Borel, V., Flynn, H., Skehel, J.M., and Boulton, S.J. (2012) MMS19 links cytoplasmic iron-sulfur cluster assembly to DNA metabolism. Science 337: 243-245.
16. Hausmann, A., Netz, D.J., Balk, J., Pierik, A.J., Mühlenhoff, U., and Lill, R. (2005) The eukaryotic P loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc Natl Acad Sci USA 102: 3266-3271.
17. Hirumi, H., and Hirumi, K. (1989) Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol 75: 985-989.
18. Jedelský, P.L., Doležal, P., Rada, P., Pyrih, J., Smíd, O., Hrdý, I., etal. (2011) The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS ONE 6: e17285.
19. Kafková, L., Ammerman, M.L., Faktorová, D., Fisk, J.C., Zimmer, S.L., Sobotka, R., etal. (2012) Functional characterization of two paralogs that are novel RNA binding proteins influencing mitochondrial transcripts of Trypanosoma brucei. RNA 18: 1846-1861.
20. Kispal, G., Csere, P., Prohl, C., and Lill, R. (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18: 3981-3989.
21. Klinge, S., Hirst, J., Maman, J.D., Krude, T., and Pellegrini, L. (2007) An iron-sulfur domain of the eukaryotic primase is essential for RNA primer synthesis. Nat Struct Mol Biol 14: 875-877.
22. Kovářová, J., Horáková, E., Changmai, P., Vancová, M., and Lukeš, J. (2014) Mitochondrial and nucleolar localization of cysteine desulfurase Nfs and the scaffold protein Isu in Trypanosoma brucei. Eukaryot Cell 13: 353-362.
23. Lange, H., Lisowsky, T., Gerber, J., Muhlenhoff, U., Kispal, G., and Lill, R. (2001) An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep 2: 715-720.
24. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
25. Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature 460: 831-838.
26. Long, S., 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.
27. Lukeš, J., Hashimi, H., and Zíková, A. (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet 48: 277-299.
28. Marchler-Bauer, A., Panchenko, A.R., Shoemaker, B.A., Thiessen, P.A., Geer, L.Y., and Bryant, S.H. (2002) CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res 30: 281-283.
29. Montagnes, D., Roberts, E., Lukeš, J., and Lowe, C. (2012) The rise of model protozoa. Trends Microbiol 20: 184-191.
30. Nakai, Y., Nakai, M., Lill, R., Suzuki, T., and Hayashi, H. (2007) Thio modification of yeast cytosolic tRNA is an iron-sulfur protein-dependent pathway. Mol Cell Biol 27: 2841-2847.
31. Netz, D.J., Pierik, A.J., Stümpfig, M., Mühlenhoff, U., and Lill, R. (2007) The Cfd1-Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol. Nat Chem Biol 3: 278-286.
32. Netz, D.J., Stümpfig, M., Doré, C., Mühlenhoff, U., Pierik, A.J., and Lill, R. (2010) Tah18 transfers electrons to Dre2 in cytosolic iron-sulfur protein biogenesis. Nat Chem Biol 6: 758-765.
33. Netz, D.J., Stith, C.M., Stümpfig, M., Köpf, G., Vogel, D., Genau, H.M., etal. (2011) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nat Chem Biol 8: 125-132.
34. Netz, D.J., Pierik, A.J., Stümpfig, M., Bill, E., Sharma, A.K., Pallesen, L.J., etal. (2012) A bridging [4Fe-4S] cluster and nucleotide binding are essential for function of the Cfd1-Nbp35 complex as a scaffold in iron-sulfur protein maturation. J Biol Chem 287: 12365-12378.
35. Netz, D.J., Mascarenhas, J., Stehling, O., Pierik, A.J., and Lill, R. (2014) Maturation of cytosolic and nuclear iron-sulfur proteins. Trends Cell Biol 24: 303-312.
36. Nývltová, E., Šuták, R., Harant, K., Šedinová, M., Hrdy, I., Paces, J., etal. (2013) NIF-type iron-sulfur cluster assembly system is duplicated and distributed in the mitochondria and cytosol of Mastigamoeba balamuthi. Proc Natl Acad Sci USA 110: 7371-7376.
37. 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.
38. Pierik, A.J., Netz, D.J., and Lill, R. (2009) Analysis of iron-sulfur protein maturation in eukaryotes. Nat Protoc 4: 753-766.
39. Roche, B., Aussel, L., Ezraty, B., Mandin, P., Py, B., and Barras, F. (2013) Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity. Biochim Biophys Acta 1827: 455-469.
40. Roy, A., Solodovnikova, N., Nicholson, T., Antholine, W., and Walden, W.E. (2003) A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J 22: 4826-4835.
41. Rudolf, J., Makrantoni, V., Ingledew, W.J., Stark, M.J., and White, M.F. (2006) The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol Cell 23: 801-808.
42. 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.
43. Sipos, K., Lange, H., Fekete, Z., Ullmann, P., Lill, R., and Kispal, G. (2002) Maturation of cytosolic iron-sulfur proteins requires glutathione. J Biol Chem 277: 26944-26949.
44. Smíd, O., Horáková, E., Vilímová, V., Hrdy, 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.
45. Soler, N., Delagoutte, E., Miron, S., Facca, C., Baïlle, D., d'Autreaux, B., etal. (2011) Interaction between the reductase Tah18 and highly conserved Fe-S containing Dre2 C-terminus is essential for yeast viability. Mol Microbiol 82: 54-67.
46. Soler, N., Craescu, C.T., Gallay, J., Frapart, Y.M., Mansuy, D., Raynal, B., etal. (2012) A S-adenosylmethionine methyltransferase-like domain within the essential, Fe-S-containing yeast protein Dre2. FEBS J 279: 2108-2119.
47. Srinivasan, V., Netz, D.J., Webert, H., Mascarenhas, J., Pierik, A.J., Michel, H., and Lill, R. (2007) Structure of the yeast WD40 domain protein Cia1, a component acting late in iron-sulfur protein biogenesis. Structure 15: 1246-1257.
48. Srinivasan, V., Pierik, A.J., and Lill, R. (2014) Crystal structures of nucleotide-free and glutathione-bound mitochondrial ABC transporter Atm1. Science 343: 1137-1140.
49. Stehling, O., Vashisht, A.A., Mascarenhas, J., Jonsson, Z.O., Sharma, T., Netz, D.J., etal. (2012) MMS19 assembles iron-sulfur proteins required for DNA metabolism and genomic integrity. Science 337: 195-199.
50. Stehling, O., Mascarenhas, J., Vashisht, A.A., Sheftel, A.D., Niggemeyer, B., Rösser, R., etal. (2013) Human CIA2A-FAM96A and CIA2B-FAM96B integrate iron homeostasis and maturation of different subsets of cytosolic-nuclear iron-sulfur proteins. Cell Metab 18: 187-198.
51. Tachezy, J. (ed.) (2008) Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Berlin, Heidelberg: Springer Berlin Heidelberg.
52. Tsaousis, A.D., Gentekaki, E., Eme, L., Gaston, D., and Roger, A.J. (2014) Evolution of the cytosolic iron-sulfur cluster assembly machinery in Blastocystis species and other microbial eukaryotes. Eukaryot Cell 13: 143-153.
53. Vernis, L., Facca, C., Delagoutte, E., Soler, N., Chanet, R., Guiard, B., etal. (2009) A newly identified essential complex, Dre2-Tah18, controls mitochondria integrity and cell death after oxidative stress in yeast. PLoS ONE 4: e4376.
54. 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.
55. Wickstead, B., Ersfeld, K., and Gull, K. (2002) Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol Biochem Parasitol 125: 211-216.
56. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99: 89-101.
57. Yeeles, J.T., Cammack, R., and Dillingham, M.S. (2009) An iron-sulfur cluster is essential for the binding of broken DNA by AddAB-type helicase-nucleases. J Biol Chem 284: 7746-7755.