The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria

EMBO Journal

Volumn 25, Issue 1, 2006, Pages 174-183

  Adam, Alexander C ^a,c   Bornhövd, Carsten ^a   Prokisch, Holger ^b   Neupert, Walter ^a   Hell, Kai ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

Cysteine desulfurase; Fe S cluster formation; Fe S protein; Isd11; Mitochondria

Indexed keywords

ACONITATE HYDRATASE; FERREDOXIN; IRON RESPONSIVE SURFACE DETERMINANT 11 PROTEIN; IRON SULFUR PROTEIN; PROTEIN; PROTEIN NFS 1; SUCCINATE DEHYDROGENASE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CLUSTER ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC CONSERVATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

AMINO ACID SEQUENCE; CARBON-SULFUR LYASES; CYSTEINE; DOWN-REGULATION; IRON-SULFUR PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 30444433568     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600905     Document Type: Article

References (62)

1. Babcock M, de Silva D, Oaks R, Davis-Kaplan S, Jiralerspong S, Montermini L, Pandolfo M, Kaplan J (1997) Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 276: 1709-1712
2. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ, Yeats C, Eddy SR (2004) The Pfam protein families database. Nucleic Acids Res 32 (database issue): D138-D141
3. Cheng MY, Hartl FU, Martin J, Pollock RA, Kalousek F, Neupert W, Hallberg EM, Hallberg RL, Horwich AL (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337: 620-625
4. Craig EA, Marszalek J (2002) A specialized mitochondrial molecular chaperone system: a role in formation of Fe/S centers. Cell Mol Life Sci 59: 1658-1665
5. Craig EA, Voisine C, Schilke B (1999) Mitochondrial iron metabolism in the yeast Saccharomyces cerevisiae. Biol Chem 380: 1167-1173
6. 2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 257: 13028-13033
7. Dutkiewicz R, Schilke B, Knieszner H, Walter W, Craig EA, Marszalek J (2003) Ssq1, a mitochondrial Hsp70 involved in iron-sulfur (Fe/S) center biogenesis. Similarities to and differences from its bacterial counterpart. J Biol Chem 278: 29719-29727
8. Endo T, Yamamoto H, Esaki M (2003) Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles. J Cell Sci 116: 3259-3267
9. Englard S, Siegel L (1969) Mitochondrial L-malate dehydrogenase of beef heart. Methods Enzymol 12: 99-106
10. Fansler B, Lowenstein JM (1969) Aconitase from pig heart. Methods Enzymol 12: 26-30
11. Foury F, Cazzalini O (1997) Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett 411: 373-377
12. Frazzon J, Dean DR (2003) Formation of iron-sulfur clusters in bacteria: an emerging field in bioinorganic chemistry. Curr Opin Chem Biol 7: 166-173
13. Garland SA, Hoff K, Vickery LE, Culotta VC (1999) Saccharomyces cerevisiae ISU1 and ISU2: members of a well-conserved gene family for iron-sulfur cluster assembly. J Mol Biol 294: 897-907
14. Gerber J, Muhlenhoff U, Lill R (2003) An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep 4: 906-911
15. Gerber J, Neumann K, Prohl C, Muhlenhoff U, Lill R (2004) The yeast scaffold proteins Isu1p and Isu2p are required inside mitochondria for maturation of cytosolic Fe/S proteins. Mol Cell Biol 24: 4848-4857
16. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker DD, Sookhai-Mahadeo S, Storms RK, Strathern JN, Valle G, Voet M, Volckaert G, Wang CY, Ward TR, Wilhelmy J, Winzeler EA, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke JD, Snyder M, Philippsen P, Davis RW, Johnston M (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391
17. Harlow E, Lane D (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
18. Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381: 571-579
19. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691
20. Kim R, Saxena S, Gordon DM, Pain D, Dancis A (2001) J-domain protein, Jac1p, of yeast mitochondria required for iron homeostasis and activity of Fe-S cluster proteins. J Biol Chem 276: 17524-17532
21. Kispal G, Csere P, Prohl C, Lill R (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18: 3981-3989
22. Knight SA, Sepuri NB, Pain D, Dancis A (1998) Mt-Hsp70 homolog, Ssc2p, required for maturation of yeast frataxin and mitochondrial iron homeostasis. J Biol Chem 273: 18389-18393
23. Knop M, Siegers K, Pereira G, Zachariae W Winsor B, Nasmyth K, Schiebel E (1999) Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15: 963-972
24. Koehler CM (2004) New developments in mitochondrial assembly. Annu Rev Cell Dev Biol 20: 309-335
25. Lafontaine D, Tollervey D (1996) One-step PCR mediated strategy for the construction of conditionally expressed and epitope tagged yeast proteins. Nucleic Acids Res 24: 3469-3471
26. Lange H, Kaut A, Kispal G, Lill R (2000) A mitochondrial ferredoxin is essential for biogenesis of cellular iron-sulfur proteins. Proc Natl Acad Sci USA 97: 1050-1055
27. Li J, Kogan M, Knight SA, Pain D, Dancis A (1999) Yeast mitochondrial protein, Nfs1p, coordinately regulates iron-sulfur cluster proteins, cellular iron uptake, and iron distribution. J Biol Chem 274: 33025-33034
28. Li J, Saxena S, Pain D, Dancis A (2001) Adrenodoxin reductase homolog (Arh1p) of yeast mitochondria required for iron homeostasis. J Biol Chem 276: 1503-1509
29. Lill R, Kispal G (2000) Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem Sci 25: 352-356
30. Lill R, Muhlenhoff U (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30: 133-141
31. Loiseau L, Ollagnier-de Choudens S, Lascoux D, Forest E, Fontecave M, Barras F (2005) Analysis of the heteromeric CsdA-CsdE cysteine desulfurase, assisting Fe-S cluster biogenesis in Escherichia coli. J Biol Chem 280: 26760-26769
32. Loiseau L, Ollagnier-de-Choudens S, Nachin L, Fontecave M, Barras F (2003) Biogenesis of Fe-S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase. J Biol Chem 278: 38352-38359
33. Lutz T, Westermann B, Neupert W Herrmann JM (2001) The mitochondrial proteins Ssq1 and Jac1 are required for the assembly of iron sulfur clusters in mitochondria. J Mol Biol 307: 815-825
34. Manzella L, Barros MH, Nobrega FG (1998) ARH1 of Saccharomyces cerevisiae: a new essential gene that codes for a protein homologous to the human adrenodoxin reductase. Yeast 14: 839-846
35. McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32: W20-W25
36. Mokranjac D, Paschen SA, Kozany C, Prokisch H, Hoppins SC, Nargang FE, Neupert W, Hell K (2003) Tim50, a novel component of the TIM23 preprotein translocase of mitochondria. EMBO J 22: 816-825
37. Muhlenhoff U, Balk J, Richhardt N, Kaiser JT, Sipos K, Kispal G, Lill R (2004) Functional characterization of the eukaryotic cysteine desulfurase Nfs1p from Saccharomyces cerevisiae. J Biol Chem 279: 36906-36915
38. Muhlenhoff U, Gerber J, Richhardt N, Lill R (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J 22: 4815-4825
39. Neupert W, Brunner M (2002) The protein import motor of mitochondria. Nat Rev Mol Cell Biol 3: 555-565
40. Outten FW, Djaman O, Storz G (2004) A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol Microbiol 52: 861-872
41. Outten FW, Wood MJ, Munoz FM, Storz G (2003) The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe-S cluster assembly in Escherichia coli. J Biol Chem 278: 45713-45719
42. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, Neupert W (2003) Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426: 862-866
43. Prokisch H, Scharfe C, Camp II DG, Xiao W, David L, Andreoli C, Monroe ME, Moore RJ, Gritsenko MA, Kozany C, Hixson KK, Mottaz HM, Zischka H, Ueffing M, Herman ZS, Davis RW, Meitinger T, Oefner PJ, Smith RD, Steinmetz LM (2004) Integrative analysis of the mitochondrial proteome in yeast. PLoS Biol 2: e160
44. Rehling P, Brandner K, Pfanner N (2004) Mitochondrial import and the twin-pore translocase. Nat Rev Mol Cell Biol 5: 519-530
45. Rehling P, Pfanner N, Meisinger C (2003) Insertion of hydrophobic membrane proteins into the inner mitochondrial membrane - a guided tour. J Mol Biol 326: 639-657
46. Reichert AS, Neupert W (2004) Mitochondriomics or what makes us breathe. Trends Genet 20: 555-562
47. Robinson KM, von Kieckebusch-Guck A, Lemire BD (1991) Isolation and characterization of a Saccharomyces cerevisiae mutant disrupted for the succinate dehydrogenase flavoprotein subunit. J Biol Chem 266: 21347-21350
48. Rodriguez-Manzaneque MT, Tamarit J, Belli G, Ros J, Herrero E (2002) Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13: 1109-1121
49. Rowley N, Prip-Buus C, Westermann B, Brown C, Schwarz E, Barrell B, Neupert W (1994) Mdj1p, a novel chaperone of the DnaJ family, is involved in mitochondrial biogenesis and protein folding. Cell 77: 249-259
50. Schilke B, Voisine C, Beinert H, Craig E (1999) Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96: 10206-10211
51. Schwartz CJ, Djaman O, Imlay JA, Kiley PJ (2000) The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc Natl Acad Sci USA 97: 9009-9014
52. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B, Rehling P, Pfanner N, Meisinger C (2003) The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci USA 100: 13207-13212
53. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27
54. Smith FE, Herbert J, Gaudin J, Hennessey DJ, Reid GR (1984) Serum iron determination using ferene triazine. Clin Biochem 17: 306-310
55. Strain J, Lorenz CR, Bode J, Garland S, Smolen GA, Ta DT, Vickery LE, Culotta VC (1998) Suppressors of superoxide dismutase (SOD1) deficiency in Saccharomyces cerevisiae. Identification of proteins predicted to mediate iron-sulfur cluster assembly. J Biol Chem 273: 31138-31144
56. Takahashi Y, Tokumoto U (2002) A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J Biol Chem 277: 28380-28383
57. Voisine C, Cheng YC, Ohlson M, Schilke B, Hoff K, Beinert H, Marszalek J, Craig EA (2001) Jac1, a mitochondrial J-type chaperone, is involved in the biogenesis of Fe/S clusters in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 98: 1483-1488
58. Voos W, Rottgers K (2002) Molecular chaperones as essential mediators of mitochondrial biogenesis. Biochim Biophys Acta 1592: 51-62
59. Ye H, Garifullina GF, Abdel-Ghany SE, Zhang L, Pilon-Smits EA, Pilon M (2005) The chloroplast NifS-like protein of Arabidopsis thaliana is required for iron-sulfur cluster formation in ferredoxin. Planta 220: 602-608
60. Yoon T, Cowan JA (2003) Iron-sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. J Am Chem Soc 125: 6078-6084
61. Zheng L, Cash VL, Flint DH, Dean DR, Outten FW, Djaman O, Storz G (1998) Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273: 13264-13272
62. Zheng L, White RH, Cash VL, Jack RF, Dean DR (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci USA 90: 2754-2758