Biogenesis of yeast Mia40 - Uncoupling folding from import and atypical recognition features

FEBS Journal

Volumn 280, Issue 20, 2013, Pages 4960-4969

  Chatzi, Afroditi ^a,b   Sideris, Dionisia P ^a,c   Katrakili, Nitsa ^a   Pozidis, Charalampos ^a   Tokatlidis, Kostas ^a,b  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

biogenesis; Erv1; import; Mia40; mitochondria

Indexed keywords

EID: 84885321622     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12482     Document Type: Article

References (38)

1. Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuan Szklarz LK, Schulze-Specking A, Truscott KN, Guiard B, Meisinger C, &, Pfanner N, (2004) Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J 23, 3735-3746.
2. Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N, Neupert W, Herrmann JM, &, Hell K, (2005) Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett 579, 179-184.
3. 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.
4. Lu H, Allen S, Wardleworth L, Savory P, &, Tokatlidis K, (2004) Functional TIM10 chaperone assembly is redox-regulated in vivo. J Biol Chem 279, 18952-18958.
5. Milenkovic D, Gabriel K, Guiard B, Schulze-Specking A, Pfanner N, &, Chacinska A, (2007) 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 282, 22472-22480.
6. Sideris DP, Petrakis N, Katrakili N, Mikropoulou D, Gallo A, Ciofi-Baffoni S, Banci L, Bertini I, &, Tokatlidis K, (2009) A novel intermembrane space-targeting signal docks cysteines onto Mia40 during mitochondrial oxidative folding. J Cell Biol 187, 1007-1022.
7. Milenkovic D, Ramming T, Muller JM, Wenz LS, Gebert N, Schulze-Specking A, Stojanovski D, Rospert S, &, Chacinska A, (2009) Identification of the signal directing Tim9 and Tim10 into the intermembrane space of mitochondria. Mol Biol Cell 20, 2530-2539.
8. Grumbt B, Stroobant V, Terziyska N, Israel L, &, Hell K, (2007) Functional characterization of Mia40p, the central component of the disulfide relay system of the mitochondrial intermembrane space. J Biol Chem 282, 37461-37470.
9. Banci L, Bertini I, Cefaro C, Ciofi-Baffoni S, Gallo A, Martinelli M, Sideris DP, Katrakili N, &, Tokatlidis K, (2009) MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat Struct Mol Biol 16, 198-206.
10. Kawano S, Yamano K, Naoe M, Momose T, Terao K, Nishikawa S, Watanabe N, &, Endo T, (2009) Structural basis of yeast Tim40/Mia40 as an oxidative translocator in the mitochondrial intermembrane space. Proc Natl Acad Sci USA 106, 14403-14407.
11. Banci L, Bertini I, Calderone V, Cefaro C, Ciofi-Baffoni S, Gallo A, Kallergi E, Lionaki E, Pozidis C, &, Tokatlidis K, (2011) Molecular recognition and substrate mimicry drive the electron-transfer process between MIA40 and ALR. Proc Natl Acad Sci USA 108, 4811-4816.
12. Banci L, Bertini I, Calderone V, Cefaro C, Ciofi-Baffoni S, Gallo A, &, Tokatlidis K, (2012) An electron-transfer path through an extended disulfide relay system: the case of the redox protein ALR. J Am Chem Soc 134, 1442-1445.
13. Dabir DV, Leverich EP, Kim SK, Tsai FD, Hirasawa M, Knaff DB, &, Koehler CM, (2007) A role for cytochrome c and cytochrome c peroxidase in electron shuttling from Erv1. EMBO J 26, 4801-4811.
14. Ang SK, &, Lu H, (2009) Deciphering structural and functional roles of individual disulfide bonds of the mitochondrial sulfhydryl oxidase Erv1p. J Biol Chem 284, 28754-28761.
15. Bien M, Longen S, Wagener N, Chwalla I, Herrmann JM, &, Riemer J, (2010) Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione. Mol Cell 37, 516-528.
16. Kloppel C, Suzuki Y, Kojer K, Petrungaro C, Longen S, Fiedler S, Keller S, &, Riemer J, (2011) Mia40-dependent oxidation of cysteines in domain I of Ccs1 controls its distribution between mitochondria and the cytosol. Mol Biol Cell 22, 3749-3757.
17. Gross DP, Burgard CA, Reddehase S, Leitch JM, Culotta VC, &, Hell K, (2011) Mitochondrial Ccs1 contains a structural disulfide bond crucial for the import of this unconventional substrate by the disulfide relay system. Mol Biol Cell 22, 3758-3767.
18. Potting C, Wilmes C, Engmann T, Osman C, &, Langer T, (2010) Regulation of mitochondrial phospholipids by Ups1/PRELI-like proteins depends on proteolysis and Mdm35. EMBO J 29, 2888-2898.
19. Tamura Y, Endo T, Iijima M, &, Sesaki H, (2009) Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria. J Cell Biol 185, 1029-1045.
20. Banci L, Bertini I, Ciofi-Baffoni S, Boscaro F, Chatzi A, Mikolajczyk M, Tokatlidis K, &, Winkelmann J, (2011) Anamorsin is a [2Fe-2S] cluster-containing substrate of the Mia40-dependent mitochondrial protein trapping machinery. Chem Biol 18, 794-804.
21. Banci L, Bertini I, Cefaro C, Cenacchi L, Ciofi-Baffoni S, Felli IC, Gallo A, Gonnelli L, Luchinat E, Sideris D, et al,. (2010) Molecular chaperone function of Mia40 triggers consecutive induced folding steps of the substrate in mitochondrial protein import. Proc Natl Acad Sci USA 107, 20190-20195.
22. Weckbecker D, Longen S, Riemer J, &, Herrmann JM, (2012) Atp23 biogenesis reveals a chaperone-like folding activity of Mia40 in the IMS of mitochondria. EMBO J 31, 4348-4358.
23. 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.
24. Terziyska N, Grumbt B, Bien M, Neupert W, Herrmann JM, &, Hell K, (2007) The sulfhydryl oxidase Erv1 is a substrate of the Mia40-dependent protein translocation pathway. FEBS Lett 581, 1098-1102.
25. Chacinska A, Guiard B, Muller JM, Schulze-Specking A, Gabriel K, Kutik S, &, Pfanner N, (2008) Mitochondrial biogenesis, switching the sorting pathway of the intermembrane space receptor Mia40. J Biol Chem 283, 29723-29729.
26. Sztolsztener ME, Brewinska A, Guiard B, &, Chacinska A, (2013) Disulfide bond formation: sulfhydryl oxidase ALR controls mitochondrial biogenesis of human MIA40. Traffic 14, 309-320.
27. Terziyska N, Grumbt B, Kozany C, &, Hell K, (2009) Structural and functional roles of the conserved cysteine residues of the redox-regulated import receptor Mia40 in the intermembrane space of mitochondria. J Biol Chem 284, 1353-1363.
28. Naoe M, Ohwa Y, Ishikawa D, Ohshima C, Nishikawa S, Yamamoto H, &, Endo T, (2004) Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J Biol Chem 279, 47815-47821.
29. Lionaki E, Aivaliotis M, Pozidis C, &, Tokatlidis K, (2010) The N-terminal shuttle domain of Erv1 determines the affinity for Mia40 and mediates electron transfer to the catalytic Erv1 core in yeast mitochondria. Antioxid Redox Signal 13, 1327-1339.
30. Allen S, Lu H, Thornton D, &, Tokatlidis K, (2003) Juxtaposition of the two distal CX3C motifs via intrachain disulfide bonding is essential for the folding of Tim10. J Biol Chem 278, 38505-38513.
31. Banci L, Bertini I, Cefaro C, Ciofi-Baffoni S, &, Gallo A, (2011) Functional role of two interhelical disulfide bonds in human Cox17 protein from a structural perspective. J Biol Chem 286, 34382-34390.
32. Kojer K, Bien M, Gangel H, Morgan B, Dick TP, &, Riemer J, (2012) Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state. EMBO J 31, 3169-3182.
33. van der Laan M, Bohnert M, Wiedemann N, &, Pfanner N, (2012) Role of MINOS in mitochondrial membrane architecture and biogenesis. Trends Cell Biol 22, 185-192.
34. von der Malsburg K, Muller JM, Bohnert M, Oeljeklaus S, Kwiatkowska P, Becker T, Loniewska-Lwowska A, Wiese S, Rao S, Milenkovic D, et al,. (2011) Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell 21, 694-707.
35. Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, &, Neupert W, (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 30, 4356-4370.
36. 'Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM, Lackner LL, Westermann B, Schuldiner M, Weissman JS, &, Nunnari J, (2011) A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J Cell Biol 195, 323-340.
37. Sideris DP, &, Tokatlidis K, (2007) Oxidative folding of small Tims is mediated by site-specific docking onto Mia40 in the mitochondrial intermembrane space. Mol Microbiol 65, 1360-1373.
38. Daum G, Bohni PC, &, Schatz G, (1982) Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 257, 13028-13033.