Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins

EMBO Journal

Volumn 25, Issue 1, 2006, Pages 184-195

  Wiedemann, Nils ^a   Urzica, Eugen ^b   Guiard, Bernard ^c   Müller, Hanne ^a   Lohaus, Christiane ^d   Meyer, Helmut E ^d   Ryan, Michael T ^e   Meisinger, Chris ^a   Mühlenhoff, Ulrich ^b   Lill, Roland ^b   Pfanner, Nikolaus ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c CNRS   (France)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e LA TROBE UNIVERSITY   (Australia)

Author keywords

Essential cellular functions; Fe S proteins; Mitochondria; Saccharomyces cerevisiae

Indexed keywords

CYSTATHIONINE GAMMA LYASE; IRON SULFUR PROTEIN; ISD11 PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL FUNCTION; CONTROLLED STUDY; EUKARYOTE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN SYNTHESIS;

AMINO ACID SEQUENCE; CARBON-SULFUR LYASES; CELL NUCLEUS; CYTOSOL; ENZYME STABILITY; IRON-SULFUR PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 30444449009     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600906     Document Type: Article

References (47)

1. Balk J, Pierik AJ, Netz DJ, Mühlenhoff U, Lill R (2004) The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J 23: 2105-2115
2. Chacinska A, Lind M, Frazier AE, Dudek J, Meisinger C, Geissler A, Sickmann A, Meyer HE, Truscott KN, Guiard B, Pfanner N, Rehling P (2005) Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120: 817-829
3. Chacinska A, Rehling P, Guiard B, Frazier AE, Schulze-Specking A, Pfanner N, Voos W, Meisinger C (2003) Mitochondrial translocation contact sites: separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex. EMBO J 22: 5370-5381
4. Chen OS, Crisp RJ, Valachovic M, Bard M, Winge DR, Kaplan J (2004) Transcription of the yeast iron regulon does not respond directly to iron but rather to iron-sulfur cluster biosynthesis. J Biol Chem 279: 29513-29518
5. Contamine V, Picard M (2000) Maintenance and integrity of the mitochondrial genome: a plethora of nuclear genes in the budding yeast. Microbiol Mol Biol Rev 64: 281-315
6. 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
7. Gabriel K, Egan B, Lithgow T (2003) Tom40, the import channel of the mitochondrial outer membrane, plays an active role in sorting imported proteins. EMBO J 22: 2380-2386
8. Gerber J, Mühlenhoff 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
9. Gerber J, Neumann K, Prohl C, Mühlenhoff 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
10. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Véronneau S, Dow S, Lucau-Danila A, Anderson K, André 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, Güldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kötter 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
11. 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
12. Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74: 247-281
13. 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
14. 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
15. Kispal G, Sipos K, Lange H, Fekete Z, Bedekovics T, Janaky T, Bassler J, Aguilar Netz DJ, Balk J, Rotte C, Lill R (2005) Biogenesis of cytosolic ribosomes requires the essential iron-sulphur protein Rli1p and mitochondria. EMBO J 24: 589-598
16. Knight SA, Sepuri NB, Pain D, Danois A (1998) Mt-Hsp70 homolog, Ssc2p, required for maturation of yeast frataxin and mitochondrial iron homeostasis. J Biol Chem 273: 18389-18393
17. Koehler CM (2004) New developments in mitochondrial assembly. Annu Rev Cell Dev Biol 20: 309-335
18. 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
19. Lange H, Lisowsky T, Gerber J, Mühlenhoff U, Kispal G, 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
20. 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
21. 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
22. Lill R, Mühlenhoff U (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30: 133-141
23. 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
24. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, Herrmann JM (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121: 1059-1069
25. Mühlenhoff 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
26. Mühlenhoff 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
27. Mühlenhoff U, Richhardt N, Ristow M, Kispal G, Lill R (2002) The yeast frataxin homolog Yfhlp plays a specific role in the maturation of cellular Fe/S proteins. Hum Mol Genet 11: 2025-2036
28. Neupert W (1997) Protein import into mitochondria. Annu Rev Biochem 66: 863-917
29. Ollagnier-de-Choudens S, Lascoux D, Loiseau L, Barras F, Forest E, Fontecave M (2003) Mechanistic studies of the SufS-SufE cysteine desulfurase: evidence for sulfur transfer from SufS to SufE. FEBS Lett 555: 263-267
30. Pfanner N, Wiedemann N, Meisinger C, Lithgow T (2004) Assembling the mitochondrial outer membrane. Nat Struct Mol Biol 11: 1044-1048
31. 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
32. Rissler M, Wiedemann N, Pfannschmidt S, Gabriel K, Guiard B, Pfanner N, Chacinska A (2005) The essential mitochondrial protein Erv1 cooperates with Mia40 in biogenesis of intermembrane space proteins. J Mol Biol 353: 485-492
33. Rutherford JC, Jaron S, Ray E, Brown PO, Winge DR (2001) A second iron-regulatory system in yeast independent of Aft1p. Proc Natl Acad Sci USA 98: 14322-14327
34. Rutherford JC, Ojeda L, Balk J, Mühlenhoff U, Lill R, Winge DR (2005) Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis. J Biol Chem 280: 10135-10140
35. Ryan MT, Voos W, Pfanner N (2001) Assaying protein import into mitochondria. Methods Cell Biol 65: 189-215
36. Schilke B, Forster J, Davis J, James P, Walter W, Laloraya S, Johnson J, Miao B, Craig E (1996) The cold sensitivity of a mutant of Saccharomyces cerevisiae lacking a mitochondrial heat shock protein 70 is suppressed by loss of mitochondrial DNA. J Cell Biol 134: 603-613
37. 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
38. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schönfisch 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
39. Smith AD, Agar JN, Johnson KA, Frazzon J, Amster IJ, Dean DR, Johnson MK (2001) Sulfur transfer from IscS to IscU: the first step in iron-sulfur cluster biosynthesis. J Am Chem Soc 123: 11103-11104
40. 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
41. Truscott KN, Voos W, Frazier AE, Lind M, Li Y, Geissler A, Dudek J, Müller H, Sickmann A, Meyer HE, Meisinger C, Guiard B, Rehling P, Pfanner N (2003) A J-protein is an essential subunit of the presequence translocase-associated protein import motor of mitochondria. J Cell Biol 163: 707-713
42. Truscott KN, Wiedemann N, Rehling P, Müller H, Meisinger C, Pfanner N, Guiard B (2002) Mitochondrial import of the ADP/ ATP carrier: the essential TIM complex of the intermembrane space is required for precursor release from the TOM complex. Mol Cell Biol 22: 7780-7789
43. Urbina HD, Silberg JJ, Hoff KG, Vickery LE (2001) Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J Biol Chem 276: 44521-44526
44. 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
45. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, Mittmann M, Pai C, Rebischung C, Revuelta JL, Riles L, Roberts CJ, Ross-MacDonald P, Scherens B, Snyder M, Sookhai-Mahadeo S, Storms RK, Véronneau S, Voet M, Volckaert G, Ward TR, Wysocki R, Yen GS, Yu K, Zimmermann K, Philippsen P, Johnston M, Davis RW (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906
46. Zheng L, Cash VL, Flint DH, Dean DR (1998) Assembly of iron-sulfur clusters: identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273: 13264-13272
47. Zheng L, White RH, Cash VL, Dean DR (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33: 4714-4720