Disulfide Bond Formation: Sulfhydryl Oxidase ALR Controls Mitochondrial Biogenesis of Human MIA40

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Volumn 14, Issue 3, 2013, Pages 309-320

  Sztolsztener, Malgorzata E ^a   Brewinska, Anita ^a   Guiard, Bernard ^b   Chacinska, Agnieszka ^a  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^b CNRS   (France)

Author keywords

ALR GFER; disease, MIA pathway; mitochondria; oxidative folding; protein biogenesis

Indexed keywords

MITOCHONDRIAL INTERMEMBRANE SPACE ASSEMBLY PROTEIN; MITOCHONDRIAL PROTEIN; THIOL OXIDASE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL MEMBRANE; CONTROLLED STUDY; DISULFIDE BOND; ENZYME MODIFICATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

DISULFIDES; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84873470266     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12030     Document Type: Article

References (64)

1. 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. The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci USA 2003;100:13207-13212.
2. Becker T, Böttinger L, Pfanner N. Mitochondrial protein import: from transport pathways to an integrated network. Trends Biochem Sci 2012;37:85-91.
3. Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell 2012;148:1145-1159.
4. Dolezal P, Likić V, Tachezy J, Lithgow T. Evolution of the molecular machines for protein import into mitochondria. Science 2006;313:314-318.
5. Neupert W, Herrmann JM. Translocation of proteins into mitochondria. Annu Rev Biochem 2007;76:723-749.
6. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. Importing mitochondrial proteins: machineries and mechanisms. Cell 2009;138:628-644.
7. Glick BS, Brandt A, Cunningham K, Müller S, Hallberg RL, Schatz G. Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell 1992;69:809-822.
8. Chacinska A, van der Laan M, Mehnert CS, Guiard B, Mick DU, Hutu DP, Truscott KN, Wiedemann N, Meisinger C, Pfanner N, Rehling P. Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting. Mol Cell Biol 2010;30:307-318.
9. Koehler CM. The small Tim proteins and the twin Cx3C motif. Trends Biochem Sci 2004;29:1-4.
10. Lu H, Allen S, Wardleworth L, Savory P, Tokatlidis K. Functional TIM10 chaperone assembly is redox-regulated in vivo. J Biol Chem 2004;279:18952-18958.
11. Arnesano F, Balatri E, Banci L, Bertini I, Winge DR. Folding studies of Cox17 reveal an important interplay of cysteine oxidation and copper binding. Structure 2005;13:713-722.
12. Webb CT, Gorman MA, Lazarou M, Ryan MT, Gulbis JM. Crystal structure of the mitochondrial chaperone TIM9.10 reveals a six-bladed alpha-propeller. Mol Cell 2006;21:123-133.
13. Gabriel K, Milenkovic D, Chacinska A, Müller J, Guiard B, Pfanner N, Meisinger C. Novel mitochondrial intermembrane space proteins as substrates of the MIA import pathway. J Mol Biol 2007;365:612-620.
14. Longen S, Bien M, Bihlmaier K, Kloeppel C, Kauff F, Hammermeister M, Westermann B, Herrmann JM, Riemer J. Systematic analysis of the twin Cx(9)C protein family. J Mol Biol 2009;393:356-368.
15. Stojanovski D, Bragoszewski P, Chacinska A. The MIA pathway: a tight bond between protein transport and oxidative folding in mitochondria. Biochim Biophys Acta 2012;1823:1142-1150.
16. Riemer J, Bulleid N, Herrmann JM. Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 2009;324:1284-1287.
17. Deponte M, Hell K. Disulphide bond formation in the intermembrane space of mitochondria. J Biochem 2009;146:599-608.
18. Koehler CM, Tienson HL. Redox regulation of protein folding in the mitochondrial intermembrane space. Biochim Biophys Acta 2009;1793:139-145.
19. Sideris DP, Tokatlidis K. Oxidative protein folding in the mitochondrial intermembrane space. Antioxid Redox Signal 2010;13:1189-1204.
20. Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuán Szklarz LK, Schulze-Specking A, Truscott KN, Guiard B, Meisinger C, Pfanner N. Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J 2004;23:3735-3746.
21. Naoé M, Ohwa Y, Ishikawa D, Ohshima C, Nishikawa S, Yamamoto H, Endo T. Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J Biol Chem 2004;279:47815-47821.
22. Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N, Neupert W, Herrmann JM, Hell K. Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett 2005;579:179-184.
23. Lisowsky T. Dual function of a new nuclear gene for oxidative phosphorylation and vegetative growth in yeast. Mol Gen Genet 1992;232:58-64.
24. Allen S, Balabanidou V, Sideris DP, Lisowsky T, Tokatlidis K. Erv1 mediates the Mia40-dependent protein import pathway and provides a functional link to the respiratory chain by shuttling electrons to cytochrome c. J Mol Biol 2005;353:937-944.
25. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, Herrmann JM. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 2005;121:1059-1069.
26. Rissler M, Wiedemann N, Pfannschmidt S, Gabriel K, Guiard B, Pfanner N, Chacinska A. The essential mitochondrial protein Erv1 cooperates with Mia40 in biogenesis of intermembrane space proteins. J Mol Biol 2005;353:485-492.
27. Milenkovic D, Gabriel K, Guiard B, Schulze-Specking A, Pfanner N, Chacinska A. Biogenesis of the essential Tim9-Tim10 chaperone complex of mitochondria: site-specific recognition of cysteine residues by the intermembrane space receptor Mia40. J Biol Chem 2007;282:22472-22480.
28. Sideris DP, Tokatlidis K. Oxidative folding of small Tims is mediated by site-specific docking onto Mia40 in the mitochondrial intermembrane space. Mol Microbiol 2007;65:1360-1373.
29. Milenkovic D, Ramming T, Müller JM, Wenz LS, Gebert N, Schulze-Specking A, Stojanovski D, Rospert S, Chacinska A. Identification of the signal directing Tim9 and Tim10 into the intermembrane space of mitochondria. Mol Biol Cell 2009;20:2530-2539.
30. Sideris DP, Petrakis N, Katrakili N, Mikropoulou D, Gallo A, Ciofi-Baffoni S, Banci L, Bertini I, Tokatlidis K. A novel intermembrane space targeting signal docks cysteines onto Mia40 during mitochondrial oxidative folding. J Cell Biol 2009;187:1007-1022.
31. von der Malsburg K, Müller JM, Bohnert M, Oeljeklaus S, Kwiatkowska P, Becker T, Loniewska-Lwowska A, Wiese S, Rao S, Milenkovic D, Hutu DP, Zerbes RM, Schulze-Specking A, Meyer HE, Martinou JC, et al. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell 2011;21:694-707.
32. Müller JM, Milenkovic D, Guiard B, Pfanner N, Chacinska A. Precursor oxidation by Mia40 and Erv1 promotes vectorial transport of proteins into the mitochondrial intermembrane space. Mol Biol Cell 2008;19:226-236.
33. Stojanovski D, Milenkovic D, Müller JM, Gabriel K, Schulze-Specking A, Baker MJ, Ryan MT, Guiard B, Pfanner N, Chacinska A. Mitochondrial protein import: precursor oxidation in a ternary complex with disulfide carrier and sulfhydryl oxidase. J Cell Biol 2008;183:195-202.
34. Banci L, Bertini I, Cefaro C, Ciofi-Baffoni S, Gallo A, Martinelli M, Sideris DP, Katrakili N, Tokatlidis K. MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat Struct Mol Biol 2009;16:198-206.
35. Kawano S, Yamano K, Naoé M, Momose T, Terao K, Nishikawa S, Watanabe N, Endo T. Structural basis of yeast Tim40/Mia40 as an oxidative translocator in the mitochondrial intermembrane space. Proc Natl Acad Sci USA 2009;106:14403-14407.
36. Tienson HL, Dabir DV, Neal SE, Loo R, Hasson SA, Boontheung P, Kim SK, Loo JA, Koehler CM. Reconstitution of the Mia40-Erv1 oxidative folding pathway for the small Tim proteins. Mol Biol Cell 2009;20:3481-3490.
37. Banci L, Bertini I, Cefaro C, Cenacchi L, Ciofi-Baffoni S, Felli IC, Gallo A, Gonnelli L, Luchinat E, Sideris D, Tokatlidis K. Molecular chaperone function of Mia40 triggers consecutive induced folding steps of the substrate in mitochondrial protein import. Proc Natl Acad Sci USA 2010;107:20190-20195.
38. Grumbt B, Stroobant V, Terziyska N, Israel L, Hell K. Functional characterization of Mia40p, the central component of the disulfide relay system of the mitochondrial intermembrane space. J Biol Chem 2007;282:37461-37470.
39. Terziyska N, Grumbt B, Kozany C, Hell K. Structural and functional roles of conserved cysteine residues of the redox-regulated import receptor Mia40 in the intermembrane space of mitochondria. J Biol Chem 2009;284:1353-1363.
40. Daithankar VN, Farrell SC, Thorpe C. Augmenter of liver regeneration: substrate specificity of a flavin-dependent oxidoreductase from the mitochondrial intermembrane space. Biochemistry 2009;48:4828-4837.
41. Bien M, Longen S, Wagener N, Chwalla I, Herrmann JM, Riemer J. Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione. Mol Cell 2010;37:516-528.
42. Banci L, Bertini I, Calderone V, Cefaro C, Ciofi-Baffoni S, Gallo A, Kallergi E, Lionaki E, Pozidis C, Tokatlidis K. Molecular recognition and substrate mimicry drive the electron-transfer process between MIA40 and ALR. Proc Natl Acad Sci USA 2011;108:4811-4816.
43. Hofmann S, Rothbauer U, Mühlenbein N, Baiker K, Hell K, Bauer MF. Functional and mutational characterization of human MIA40 acting during import into the mitochondrial intermembrane space. J Mol Biol 2005;353:517-528.
44. Lee JE, Hofhaus G, Lisowsky T. Erv1p from Saccharomyces cerevisiae is a FAD-linked sulfhydryl oxidase. FEBS Lett 2000;477:62-66.
45. Lisowsky T, Lee JE, Polimeno L, Francavilla A, Hofhaus G. Mammalian augmenter of liver regeneration protein is a sulfhydryl oxidase. Dig Liver Dis 2001;33:173-180.
46. Farrell SR, Thorpe C. Augmenter of liver regeneration: a flavin-dependent sulfhydryl oxidase with cytochrome c reductase activity. Biochemistry 2005;44:1532-1541.
47. Fass D. The Erv family of sulfhydryl oxidases. Biochim Biophys Acta 2008;1783:557-566.
48. Wu CK, Dailey TA, Dailey HA, Wang BC, Rose JP. The crystal structure of augmenter of liver regeneration: a mammalian FAD-dependent sulfhydryl oxidase. Protein Sci 2003;12:1109-1118.
49. Ang SK, Lu H. Deciphering structural and functional roles of individual disulfide bonds of the mitochondrial sulfhydryl oxidase Erv1p. J Biol Chem 2009;284:28754-28761.
50. Daithankar VN, Schaefer SA, Dong M, Bahnson BJ, Thorpe C. Structure of the human sulfhydryl oxidase augmenter of liver regeneration and characterization of a human mutation causing an autosomal recessive myopathy. Biochemistry 2010;49:6737-6745.
51. Kawamata H, Manfredi G. Different regulation of wild-type and mutant Cu, Zn superoxide dismutase localization in mammalian mitochondria. Hum Mol Genet 2008;17:3303-3317.
52. Chacinska A, Guiard B, Müller JM, Schulze-Specking A, Gabriel K, Kutik S, Pfanner N. Mitochondrial biogenesis, switching the sorting pathway of the intermembrane space receptor Mia40. J Biol Chem 2008;283:29723-29729.
53. Lange H, Lisowsky T, Gerber J, Muhlenhoff U, Kispal G, Lill R. An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep 2001;2:715-720.
54. Di Fonzo A, Ronchi D, Lodi T, Fassone E, Tigano M, Lamperti C, Corti S, Bordoni A, Fortunato F, Nizzardo M, Napoli L, Donadoni C, Salani S, Saladino F, Moggio M, et al. The mitochondrial disulfide relay system protein GFER is mutated in autosomal-recessive myopathy with cataract and combined respiratory-chain deficiency. Am J Hum Genet 2009;845:594-604.
55. Terziyska N, Grumbt B, Bien M, Neupert W, Herrmann JM, Hell K. The sulfhydryl oxidase Erv1 is a substrate of the Mia40-dependent protein translocation pathway. FEBS Lett 2007;581:1098-1102.
56. Böttinger L, Gornicka A, Czerwik T, Bragoszewski P, Loniewska-Lwowska A, Schulze-Specking A, Truscott KN, Guiard B, Milenkovic D, Chacinska A. In vivo evidence for cooperation of Mia40 and Erv1 in the oxidation of mitochondrial proteins. Mol Biol Cell 2012;23:3957-3969.
57. Botstein D, Fink GR. Yeast: an experimental organism for 21st century biology. Genetics 2011;189:695-704.
58. Koehler CM, Leuenberger D, Merchant S, Renold A, Junne T, Schatz G. Human deafness dystonia syndrome is a mitochondrial disease. Proc Natl Acad Sci USA 1999;96:2141-2146.
59. Reinhold R, Bareth B, Balleininger M, Wissel M, Rehling P, Mick DU. Mimicking a SURF1 allele reveals uncoupling of cytochrome c oxidase assembly from translational regulation in yeast. Hum Mol Genet 2011;20:2379-2393.
60. Kucharczyk R, Salin B, di Rago JP. Introducing the human Leigh syndrome mutation T9176G into Saccharomyces cerevisiae mitochondrial DNA leads to severe defects in the incorporation of Atp6p into the ATP synthase and in the mitochondrial morphology. Hum Mol Genet 2009;18:2889-2898.
61. Sikorski RH, Hieter PA. System of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 1989;122:19-27.
62. Meisinger C, Pfanner N, Truscott KN. Isolation of yeast mitochondria. Methods Mol Biol 2006;313:33-39.
63. Stojanovski D, Pfanner N, Wiedemann N. Import of proteins into mitochondria. Methods Cell Biol 2007;80:783-806.
64. Kushnirov VV. Rapid and reliable protein extraction from yeast. Yeast 2000;16:857-860.