The ubiquitin-proteasome system regulates mitochondrial intermembrane space proteins

Molecular and Cellular Biology

Volumn 33, Issue 11, 2013, Pages 2136-2148

  Bragoszewski, Piotr ^a   Gornicka, Agnieszka ^a   Sztolsztener, Malgorzata E ^a   Chacinska, Agnieszka ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MITOCHONDRIAL INTERMEMBRANE SPACE PROTEIN; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; CYTOSOL; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; UBIQUITINATION;

CATION TRANSPORT PROTEINS; CYTOSOL; INTRACELLULAR MEMBRANES; LEUPEPTINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MOLECULAR CHAPERONES; MULTIENZYME COMPLEXES; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITINATED PROTEINS;

EID: 84879001260     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01579-12     Document Type: Article

References (69)

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. 2003. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. U. S. A. 100:13207-13212.
2. Prokisch H, Scharfe C, Camp 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. doi:10.1371/journal.pbio.0020160.
3. Perocchi F, Jensen LJ, Gagneur J, Ahting U, von Mering C, Bork P, Prokisch H, Steinmetz LM. 2006. Assessing systems properties of yeast mitochondria through an interaction map of the organelle. PLoS Genet. 2:e170. doi:10.1371/journal.pgen.0020170.
4. Dolezal P, Likic V, Tachezy J, Lithgow T. 2006. Evolution of the molecular machines for protein import into mitochondria. Science 313:314-318.
5. Neupert W, Herrmann JM. 2007. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76:723-749.
6. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628-644.
7. Schmidt O, Pfanner N, Meisinger C. 2010. Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 11:655-667.
8. Wasilewski M, Scorrano L. 2009. The changing shape of mitochondrial apoptosis. Trends Endocrinol. Metab. 20:287-294.
9. Herrmann JM, Riemer J. 2010. The intermembrane space of mitochondria. Antioxid. Redox Signal. 13:1341-1358.
10. Martinou JC, Youle RJ. 2011. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev. Cell 21:92-101.
11. Nunnari J, Suomalainen A. 2012. Mitochondria: in sickness and in health. Cell 148:1145-1159.
12. Vögtle FN, Burkhart JM, Rao S, Gerbeth C, Hinrichs J, Martinou JC, Chacinska A, Sickmann A, Zahedi RP, Meisinger C. 2012. Intermembrane space proteome of yeast mitochondria. Mol. Cell. Proteomics 11:1840-1852.
13. Endo T, Yamano K, Kawano S. 2010. Structural basis for the disulfide relay system in the mitochondrial intermembrane space. Antioxid. Redox Signal. 13:1359-1373.
14. Sideris DP, Tokatlidis K. 2010. Oxidative protein folding in the mitochondrial intermembrane space. Antioxid. Redox Signal. 13:1189-1204.
15. Herrmann JM, Riemer J. 2012. Mitochondrial disulfide relay: redoxregulated protein import into the intermembrane space. J. Biol. Chem. 287:4426-4433.
16. Stojanovski D, Bragoszewski P, Chacinska A. 2012. The MIA pathway: a tight bond between protein transport and oxidative folding in mitochondria. Biochim. Biophys. Acta 1823:1142-1150.
17. Koehler CM. 2004. The small Tim proteins and the twin Cx3C motif. Trends Biochem. Sci. 29:1-4.
18. Gabriel K, Milenkovic D, Chacinska A, Müller J, Guiard B, Pfanner N, Meisinger C. 2007. Novel mitochondrial intermembrane space proteins as substrates of the MIA import pathway. J. Mol. Biol. 365:612-620.
19. Longen S, Bien M, Bihlmaier K, Kloeppel C, Kauff F, Hammermeister M, Westermann B, Herrmann JM, Riemer J. 2009. Systematic analysis of the twin cx(9)c protein family. J. Mol. Biol. 393:356-368.
20. 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.
21. 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.
22. Müller JM, Milenkovic D, Guiard B, Pfanner N, Chacinska A. 2008. Precursor oxidation by Mia40 and Erv1 promotes vectorial transport of proteins into the mitochondrial intermembrane space. Mol. Biol. Cell 19:226-236.
23. 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.
24. Tienson HL, Dabir DV, Neal SE, Loo R, Hasson SA, Boontheung P, Kim SK, Loo JA, Koehler CM. 2009. Reconstitution of the Mia40-Erv1 oxidative folding pathway for the small Tim proteins. Mol. Biol. Cell 20: 3481-3490.
25. Milenkovic D, Ramming T, Müller 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.
26. 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.
27. Banci L, Bertini I, Cefaro C, Cenacchi L, Ciofi-Baffoni S, Felli IC, Gallo A, Gonnelli L, Luchinat E, Sideris D, Tokatlidis K. 2010. Molecular chaperone function of Mia40 triggers consecutive induced folding steps of the substrate in mitochondrial protein import. Proc. Natl. Acad. Sci. U. S. A. 107:20190-20195.
28. 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.
29. 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.
30. 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. U. S. A. 108:4811-4816.
31. Stojanovski D, Milenkovic D, Müller JM, Gabriel K, Schulze-Specking A, Baker MJ, Ryan MT, Guiard B, Pfanner N, Chacinska A. 2008. Mitochondrial protein import: precursor oxidation in a ternary complex with disulfide carrier and sulfhydryl oxidase. J. Cell Biol. 183:195-202.
32. Böttinger L, Gornicka A, Czerwik T, Bragoszewski P, Loniewska-Lwowska A, Schulze-Specking A, Truscott KN, Guiard B, Milenkovic D, Chacinska A. 2012. In vivo evidence for cooperation of Mia40 and Erv1 in the oxidation of mitochondrial proteins. Mol. Biol. Cell 23:3957-3969.
33. 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, Rospert S, Rehling P, Meisinger C, Veenhuis M, Warscheid B, van der Klei IJ, Pfanner N, Chacinska A, van der Laan M. 2011. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 21:694-707.
34. Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuán 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.
35. Allen S, Balabanidou V, Sideris DP, Lisowsky T, Tokatlidis K. 2005. 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. 353:937-944.
36. 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.
37. Durigon R, Wang Q, Ceh Pavia E, Grant CM, Lu H. 2012. Cytosolic thioredoxin system facilitates the import of mitochondrial small Tim proteins. EMBO Rep. 13:916-922.
38. Chacinska A, Guiard B, Müller 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.
39. 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.
40. Morvan J, Froissard M, Haguenauer-Tsapis R, Urban-Grimal D. 2004. The ubiquitin ligase Rsp5p is required for modification and sorting of membrane proteins into multivesicular bodies. Traffic 5:383-392.
41. Stawiecka-Mirota M, Pokrzywa W, Morvan J, Zoladek T, Haguenauer-Tsapis R, Urban-Grimal D, Morsomme P. 2007. Targeting of Sna3p to the endosomal pathway depends on its interaction with Rsp5p and multivesicular body sorting on its ubiquitylation. Traffic 8:1280 -1296.
42. Liu C, Apodaca J, Davis LE, Rao H. 2007. Proteasome inhibition in wild-type yeast Saccharomyces cerevisiae cells. Biotechniques 42:158, 160, 162.
43. Meisinger C, Pfanner N, Truscott KN. 2006. Isolation of yeast mitochondria. Methods Mol. Biol. 313:33-39.
44. Ciechanover A. 2012. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Biochim. Biophys. Acta 1824:3-13.
45. Anand R, Langer T, Baker MJ. 2013. Proteolytic control of mitochondrial function and morphogenesis. Biochim. Biophys. Acta 1833:195-204.
46. Heinemeyer W, Gruhler A, Möhrle V, Mahé Y, Wolf DH. 1993. PRE2, highly homologous to the human major histocompatibility complexlinked RING10 gene, codes for a yeast proteasome subunit necessary for chymotryptic activity and degradation of ubiquitinated proteins. J. Biol. Chem. 268:5115-5120.
47. Velichutina I, Connerly PL, Arendt CS, Li X, Hochstrasser M. 2004. Plasticity in eucaryotic 20S proteasome ring assembly revealed by a subunit deletion in yeast. EMBO J. 23:500-510.
48. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I. 2008. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481-488.
49. Kusmierczyk AR, Kunjappu MJ, Funakoshi M, Hochstrasser M. 2008. A multimeric assembly factor controls the formation of alternative 20S proteasomes. Nat. Struct. Mol. Biol. 15:237-244.
50. Finley D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78:477-513.
51. Husnjak K, Dikic I. 2012. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81:291-322.
52. Hofmann S, Rothbauer U, Mühlenbein N, Baiker K, Hell K, Bauer MF. 2005. Functional and mutational characterization of human MIA40 acting during import into the mitochondrial intermembrane space. J. Mol. Biol. 353:517-528.
53. Chacinska A, van der Laan M, Mehnert CS, Guiard B, Mick DU, Hutu DP, Truscott KN, Wiedemann N, Meisinger C, Pfanner N, Rehling P. 2010. Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting. Mol. Cell. Biol. 30:307-318.
54. Goldberg AL. 2003. Protein degradation and protection against misfolded or damaged proteins. Nature 426:895-899.
55. Ye Y, Shibata Y, Yun C, Ron D, Rapoport TA. 2004. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429:841-847.
56. Nakatsukasa K, Huyer G, Michaelis S, Brodsky JL. 2008. Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 132:101-112.
57. Deshaies RJ, Joazeiro CA. 2009. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78:399-434.
58. Varshavsky A. 2011. The N-end rule pathway and regulation by proteolysis. Protein Sci. 20:1298-1345.
59. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086.
60. Escobar-Henriques M, Westermann B, Langer T. 2006. Regulation of mitochondrial fusion by the F-box protein Mdm30 involves proteasomeindependent turnover of Fzo1. J. Cell Biol. 173:645-650.
61. Margineantu DH, Emerson CB, Diaz D, Hockenbery DM. 2007. Hsp90 inhibition decreases mitochondrial protein turnover. PLoS One 2:e1066. doi:10.1371/journal.pone.0001066.
62. Cohen MM, Leboucher GP, Livnat-Levanon N, Glickman MH, Weissman AM. 2008. Ubiquitin-proteasome-dependent degradation of a mitofusin, a critical regulator of mitochondrial fusion. Mol. Biol. Cell 19:2457-2464.
63. Karbowski M, Youle RJ. 2011. Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation. Curr. Opin. Cell Biol. 23:476-482.
64. Pearce DA, Sherman F. 1997. Differential ubiquitin-dependent degradation of the yeast apo-cytochrome c isozymes. J. Biol. Chem. 272:31829-31836.
65. Radke S, Chander H, Schäfer P, Meiss G, Krüger R, Schulz JB, Germain D. 2008. Mitochondrial protein quality control by the proteasome involves ubiquitination and the protease Omi. J. Biol. Chem. 283:12681-12685.
66. Baker MJ, Mooga VP, Guiard B, Langer T, Ryan MT, Stojanovski D. 2012. Impaired folding of the mitochondrial small TIM chaperones induces clearance by the i-AAA protease. J. Mol. Biol. 424:227-239.
67. 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.
68. Komander D, Clague MJ, Urbé S. 2009. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10:550-563.
69. 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.