Mitochondrial protein homeostasis

IUBMB Life

Volumn 65, Issue 3, 2013, Pages 191-201

  Varabyova, Aksana ^a   Stojanovski, Diana ^b   Chacinska, Agnieszka ^a  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

mitochondria; protein assembly; protein degradation; protein import; protein processing

Indexed keywords

ABC TRANSPORTER; ADENINE NUCLEOTIDE TRANSLOCASE; CARRIER PROTEIN; CASEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTATHIONE; MEMBRANE PROTEIN; MESSENGER RNA; MITOCHONDRIAL PROTEIN; PROTEASOME; PROTEIN; PROTEIN PRECURSOR; UBIQUITIN PROTEIN LIGASE E3;

AMINO TERMINAL SEQUENCE; APOPTOSIS; BINDING SITE; BIOGENESIS; BIOLOGICAL FUNCTIONS; CELL FUNCTION; CELL MEMBRANE; CELL SURVIVAL; CYTOSOL; EUKARYOTIC CELL; HUMAN; LIPID COMPOSITION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL GENOME; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MITOPHAGY; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; PROTEIN PROCESSING; PROTEIN QUALITY; PROTEIN TRANSPORT; RESPIRATORY CHAIN; REVIEW; RIBOSOME;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN PRECURSORS; PROTEOLYSIS;

EID: 84874462435     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1122     Document Type: Review

References (120)

1. Sickmann, A., Reinders, J., Wagner, Y., Joppich, C., Zahedi, R., et al. (2003) The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. USA 100, 13207-13212.
2. Dolezal, P., Likic, V., Tachezy, J., and, Lithgow, T., (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313, 314-318.
3. Pagliarini, D. J., Calvo, S. E., Chang, B., Sheth, S. A., Vafai, S. B., et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123.
4. Neupert, W., and, Herrmann, J. M., (2007) Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749.
5. Chacinska, A., Koehler, C. M., Milenkovic, D., Lithgow, T., and, Pfanner, N., (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628-644.
6. Schmidt, O., Pfanner, N., and, Meisinger, C., (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 11, 655-667.
7. Becker, T., Böttinger, L., and, Pfanner, N., (2012) Mitochondrial protein import: from transport pathways to an integrated network. Trends Biochem. Sci. 37, 85-91.
8. Schmidt, O., Harbauer, A. B., Rao, S., Eyrich, B., Zahedi, R. P., et al. (2011) Regulation of mitochondrial protein import by cytosolic kinases. Cell 144, 227-239.
9. Rao, S., Schmidt, O., Harbauer, A. B., Schönfisch, B., Guiard, B., et al. (2012) Biogenesis of the preprotein translocase of the outer mitochondrial membrane: protein kinase A phosphorylates the precursor of Tom40 and impairs its import. Mol. Biol. Cell 23, 1618-1627.
10. Young, J. C., Hoogenraad, N. J., and, Hartl, F.U., (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112, 41-50.
11. Zara, V., Ferramosca, A., Robitaille-Foucher, P., Palmieri, F., and, Young, J. C., (2009) Mitochondrial carrier protein biogenesis: role of the chaperones Hsc70 and Hsp90. Biochem. J. 419, 369-375.
12. Kellems, R. E., Allison, V. F., and, Butow, R. A., (1975) Cytoplasmic type 80S ribosomes associated with yeast mitochondria. IV. Attachment of ribosomes to the outer membrane of isolated mitochondria. J. Cell Biol. 65, 1-14.
13. Suissa, M., and, Schatz, G., (1982) Import of proteins into mitochondria. Translatable mRNAs for imported mitochondrial proteins are present in free as well as mitochondria-bound cytoplasmic polysomes. J. Biol. Chem. 257, 13048-13055.
14. Marc, P., Margeot, A., Devaux, F., Blugeon, C., Corral-Debrinski, M., et al. (2002) Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3, 159-164.
15. Garcia, M., Darzacq, X., Devaux, F., Singer, R.H., and, Jacq, C., (2007) Yeast mitochondrial transcriptomics. Methods Mol. Biol. 372, 505-528.
16. Saint-Georges, Y., Garcia, M., Delaveau, T., Jourdren, L., Le Crom, S., et al. (2008) Yeast mitochondrial biogenesis: a role for the PUF RNA-binding protein Puf3p in mRNA localization. PLoS One 3, e2293.
17. Eliyahu, E., Pnueli, L., Melamed, D., Scherrer, T., Gerber, A. P., et al. (2010) Tom20 mediates localization of mRNAs to mitochondria in a translation-dependent manner. Mol. Cell. Biol. 30, 284-294.
18. Quenault, T., Lithgow, T., and, Traven, A., (2011) PUF proteins: repression, activation and mRNA localization. Trends Cell Biol. 21, 104-112.
19. Yogev, O., Karniely, S., and, Pines, O., (2007) Translation-coupled translocation of yeast fumarase into mitochondria in vivo. J. Biol. Chem. 282, 29222-29229.
20. Luk, E., Yang, M., Jensen, L. T., Bourbonnais, Y., and, Culotta, V. C., (2005) Manganese activation of superoxide dismutase 2 in the mitochondria of Saccharomyces cerevisiae. J. Biol. Chem. 280, 22715-22720.
21. Fünfschilling, U., and, Rospert, S., (1999) Nascent polypeptide-associated complex stimulates protein import into yeast mitochondria. Mol. Biol. Cell 10, 3289-3299.
22. Isken, O., and, Maquat, L. E., (2007) Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21, 1833-1856.
23. Izawa, T., Tsuboi, T., Kuroha, K., Inada, T., Nishikawa, S., et al. (2012) Roles of dom34:hbs1 in nonstop protein clearance from translocators for normal organelle protein influx. Cell Rep. 2, 447-453.
24. Dudek, J., Rehling, P., and, van der Laan, M., Mitochondrial protein import: common principles and physiological networks. Biochim. Biophys. Acta, DOI:10.1016/j.bbamcr.2012.05.028.
25. Mokranjac, D., and, Neupert, W., (2010) The many faces of the mitochondrial TIM23 complex. Biochim. Biophys. Acta 1797, 1045-1054.
26. Mokranjac, D., Sichting, M., Popov-Celeketic̈, D., Mapa, K., Gevorkyan-Airapetov, L., et al. (2009) Role of Tim50 in the transfer of precursor proteins from the outer to the inner membrane of mitochondria. Mol. Biol. Cell 20, 1400-1407.
27. Marom, M., Dayan, D., Demishtein-Zohary, K., Mokranjac, D., Neupert, W., et al. (2011) Direct interaction of mitochondrial targeting presequences with purified components of the TIM23 protein complex. J. Biol. Chem. 286, 43809-43815.
28. Schulz, C., Lytovchenko, O., Melin, J., Chacinska, A., Guiard, B., et al. (2011) Tim50′s presequence receptor domain is essential for signal driven transport across the TIM23 complex. J. Cell Biol. 195, 643-656.
29. Qian, X., Gebert, M., Höpker, J., Yan, M., Li, J., et al. (2011) Structural basis for the function of Tim50 in the mitochondrial presequence translocase. J. Mol. Biol. 411, 513-519.
30. Chacinska, A., Lind, M., Frazier, A. E., Dudek, J., Meisinger, C., et al. (2005) Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120, 817-829.
31. van der Laan, M., Meinecke, M., Dudek, J., Hutu, D.P., Lind, M., et al. (2007) Motor-free mitochondrial presequence translocase drives membrane integration of preproteins. Nat. Cell Biol. 9, 1152-1159.
32. Chacinska, A., van der Laan, M., Mehnert, C. S., Guiard, B., Mick, D. U., et al. (2010) Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting. Mol. Cell. Biol. 30, 307-318.
33. Gebert, M., Schrempp, S. G., Mehnert, C. S., Heißwolf, A. K., Oeljeklaus, S., et al. (2012). Mgr2 promotes coupling of the mitochondrial presequence translocase to partner complexes. J. Cell Biol. 197, 595-604.
34. van der Laan, M., Wiedemann, N., Mick, D. U., Guiard, B., Rehling, P., et al. (2006) A role for Tim21 in membrane-potential-dependent preprotein sorting in mitochondria. Curr. Biol. 16, 2271-2276.
35. Rehling, P., Model, K., Brandner, K., Kovermann, P., Sickmann, A., et al. (2003) Protein insertion into the mitochondrial inner membrane by a twin-pore translocase. Science 299, 1747-1751.
36. Gebert, N., Gebert, M., Oeljeklaus, S., von der Malsburg, K., Stroud, D. A., et al. (2011). Dual function of Sdh3 in the respiratory chain and TIM22 protein translocase of the mitochondrial inner membrane. Mol. Cell 44, 811-818.
37. Dukanovic, J., and, Rapaport, D., (2011) Multiple pathways in the integration of proteins into the mitochondrial outer membrane. Biochim. Biophys. Acta 1808, 971-980.
38. Paschen, S. A., Waizenegger, T., Stan, T., Preuss, M., Cyrklaff, M., et al. (2003) Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426, 862-866.
39. Wiedemann, N., Kozjak, V., Chacinska, A., Schönfisch, B., Rospert, S., et al. (2003) Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424, 565-571.
40. Kutik, S., Stojanovski, D., Becker, L., Becker, T., Meinecke, M., et al. (2008) Dissecting membrane insertion of mitochondrial beta-barrel proteins. Cell 132, 1011-1024.
41. Meisinger, C., Rissler, M., Chacinska, A., Szklarz, L. K., Milenkovic, D., et al. (2004) The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane. Dev. Cell 7, 61-71.
42. Kornmann, B., Currie, E., Collins, S. R., Schuldiner, M., Nunnari, J., et al. (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481.
43. Thornton, N., Stroud, D. A., Milenkovic, D., Guiard, B., Pfanner, N., et al. (2010) Two modular forms of the mitochondrial sorting and assembly machinery are involved in biogenesis of alpha-helical outer membrane proteins. J. Mol. Biol. 396, 540-549.
44. Sideris, D. P., and, Tokatlidis, K., (2010) Oxidative protein folding in the mitochondrial intermembrane space. Antioxid. Redox. Signal. 13, 1189-1204.
45. Stojanovski, D., Bragoszewski, P., and, Chacinska, A., (2012) The MIA pathway: a tight bond between protein transport and oxidative folding in mitochondria. Biochim. Biophys. Acta 1823, 1142-1150.
46. Herrmann, J. M., and, Riemer, J., (2012). Mitochondrial disulfide relay: redox-regulated protein import into the intermembrane space. J. Biol. Chem. 287, 4426-4433.
47. Chacinska, A., Pfannschmidt, S., Wiedemann, N., Kozjak, V., Sanjuán Szklarz, L. K., et al. (2004) Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J. 23, 3735-3746.
48. Mesecke, N., Terziyska, N., Kozany, C., Baumann, F., Neupert, W., et al. (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121, 1059-1069.
49. Banci, L., Bertini, I., Cefaro, C., Ciofi-Baffoni, S., Gallo, A., et al. (2009) MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat. Struct. Mol. Biol. 16, 198-206.
50. Stojanovski, D., Milenkovic, D., Müller, J. M., Gabriel, K., Schulze-Specking, A., et al. (2008) Mitochondrial protein import: precursor oxidation in a ternary complex with disulfide carrier and sulfhydryl oxidase. J. Cell Biol. 183, 195-202.
51. Bien, M., Longen, S., Wagener, N., Chwalla, I., Herrmann, J. M., et al. (2010) Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione. Mol. Cell 37, 516-528.
52. Böttinger, L., Gornicka, A., Czerwik, T., Bragoszewski, P., Loniewska-Lwowska, A., et al. (2012) In vivo evidence for cooperation of Mia40 and Erv1 in the oxidation of mitochondrial proteins. Mol. Biol. Cell 23, 3957-3969.
53. Kojer, K., Bien, M., Gangel, H., Morgan, B., Dick, T. P., et al. (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.
54. Milenkovic, D., Ramming, T., Müller, J. M., Wenz, L. S., Gebert, N., et al. (2009) Identification of the signal directing Tim9 and Tim10 into the intermembrane space of mitochondria. Mol. Biol. Cell 20, 2530-2539.
55. Sideris, D. P., Petrakis, N., Katrakili, N., Mikropoulou, D., Gallo, A., et al. (2009) A novel intermembrane space-targeting signal docks cysteines onto Mia40 during mitochondrial oxidative folding. J. Cell Biol. 187, 1007-1022.
56. von der Malsburg, K., Müller, J. M., Bohnert, M., Oeljeklaus, S., Kwiatkowska, P., et al. (2011) Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 21, 694-707.
57. Hoppins, S., Collins, S. R., Cassidy-Stone, A., Hummel, E., Devay, R. M., et al. (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.
58. Harner, M., Körner, C., Walther, D., Mokranjac, D., Kaesmacher, J., et al. (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 30, 4356-4370.
59. Alkhaja, A. K., Jans, D. C., Nikolov, M., Vukotic, M., Lytovchenko, O., et al. (2012) MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol. Biol. Cell 23, 247-257.
60. Harner, M., Neupert, W., and, Deponte, M., (2011) Lateral release of proteins from the TOM complex into the outer membrane of mitochondria. EMBO J. 30, 3232-3241.
61. Becker, T., Pfannschmidt, S., Guiard, B., Stojanovski, D., Milenkovic, D., et al. (2008) Biogenesis of the mitochondrial TOM complex: Mim1 promotes insertion and assembly of signal-anchored receptors. J. Biol. Chem. 283, 120-127.
62. Hulett, J. M., Lueder, F., Chan, N. C., Perry, A. J., Wolynec, P., et al. (2008) The transmembrane segment of Tom20 is recognized by Mim1 for docking to the mitochondrial TOM complex. J. Mol. Biol. 376, 694-704.
63. Popov-Celeketic̈, J., Waizenegger, T., and, Rapaport, D., (2008) Mim1 functions in an oligomeric form to facilitate the integration of Tom20 into the mitochondrial outer membrane. J. Mol. Biol. 376, 671-680.
64. Setoguchi, K., Otera, H., and, Mihara, K., (2006) Cytosolic factor- and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J. 25, 5635-5647.
65. Kemper, C., Habib, S. J., Engl, G., Heckmeyer, P., Dimmer, K. S., et al. (2008) Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. J. Cell Sci. 121, 1990-1998.
66. Krumpe, K., Frumkin, I., Herzig, Y., Rimon, N., Ozbalci, C., et al. (2012) Ergosterol content specifies targeting of tail-anchored proteins to mitochondrial outer membranes. Mol. Biol. Cell 23, 3927-3935.
67. Stojanovski, D., Guiard, B., Kozjak-Pavlovic, V., Pfanner, N., and, Meisinger, C., (2007) Alternative function for the mitochondrial SAM complex in biogenesis of alpha-helical TOM proteins. J. Cell Biol. 179, 881-893.
68. Hegde, R. S., and, Keenan, R. J., (2011) Tail-anchored membrane protein insertion into the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 12, 787-798.
69. Diekert, K., Kispal, G., Guiard, B., and, Lill, R., (1999) An internal targeting signal directing proteins into the mitochondrial intermembrane space. Proc. Natl. Acad. Sci. USA 96, 11752-11757.
70. Potting, C., Wilmes, C., Engmann, T., Osman, C., and, Langer, T., (2010) Regulation of mitochondrial phospholipids by Ups1/PRELI-like proteins depends on proteolysis and Mdm35. EMBO J. 29, 2888-2898.
71. Mick, D. U., Fox, T. D., and, Rehling, P., (2011) Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nat. Rev. Mol. Cell Biol. 12, 14-20.
72. Ott, M., and, Herrmann, J. M., (2010) Co-translational membrane insertion of mitochondrially encoded proteins. Biochim. Biophys. Acta 1803, 767-775.
73. Gruschke, S., Kehrein, K., Römpler, K., Gröne, K., Israel, L., et al. (2011) Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J. Cell. Biol. 193, 1101-1114.
74. Keil, M., Bareth, B., Woellhaf, M. W., Peleh, V., Prestele, M., et al. (2012) Oxa1-ribosome complexes coordinate the assembly of cytochrome C oxidase in mitochondria. J. Biol. Chem. 287, 34484-34493.
75. Krüger, V., Deckers, M., Hildenbeutel, M., van der Laan, M., Hellmers, M., et al. (2012) The mitochondrial oxidase assembly protein1 (oxa1) insertase forms a membrane pore in lipid bilayers. J. Biol. Chem. 287, 33314-33326.
76. Bohnert, M., Rehling, P., Guiard, B., Herrmann, J. M., Pfanner, N., et al. (2010) Cooperation of stop-transfer and conservative sorting mechanisms in mitochondrial protein transport. Curr. Biol. 20, 1227-1232.
77. Wagener, N., Ackermann, M., Funes, S., and, Neupert, W., (2011) A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol. Cell 44, 191-202.
78. Mossmann, D., Meisinger, C., and, Vögtle, F. N., (2012) Processing of mitochondrial presequences. Biochim. Biophys. Acta 1819, 1098-1106.
79. Anand, R., Langer, T., and, Baker, M. J., Proteolytic control of mitochondrial function and morphogenesis. Biochim. Biophys. Acta, DOI:10.1016/j.bbamcr.2012.06.025.
80. Vögtle, F. N., Wortelkamp, S., Zahedi, R. P., Becker, D., Leidhold, C., et al. (2009) Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 139, 428-439.
81. Vögtle, F. N., Prinz, C., Kellermann, J., Lottspeich, F., Pfanner, N., et al. (2011) Mitochondrial protein turnover: role of the precursor intermediate peptidase Oct1 in protein stabilization. Mol. Biol. Cell 22, 2135-2143.
82. Varshavsky, A., The N-end rule pathway and regulation by proteolysis. Protein Sci., DOI:10.1002/pro.666.
83. Glick, B. S., Brandt, A., Cunningham, K., Müller, S., Hallberg, R. L., et al. (1992) Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell 69, 809-822.
84. Rugarli, E. I., and, Langer, T., (2012) Mitochondrial quality control: a matter of life and death for neurons. EMBO J. 31, 1336-1349.
85. Nolden, M., Ehses, S., Koppen, M., Bernacchia, A., Rugarli, E. I., et al. (2005) The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Cell 123, 277-289.
86. Bonn, F., Tatsuta, T., Petrungaro, C., Riemer, J., and, Langer, T., (2011) Presequence-dependent folding ensures MrpL32 processing by the m-AAA protease in mitochondria. EMBO J. 30, 2545-2556.
87. Craig, E. A., Huang, P., Aron, R., and, Andrew, A., (2006) The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. Rev. Physiol. Biochem. Pharmacol. 156, 1-21.
88. Voos, W., Chaperone-protease networks in mitochondrial protein homeostasis. Biochim. Biophys. Acta, DOI:10.1016/j.bbamcr.2012.06.005.
89. Schilke, B., Williams, B., Knieszner, H., Pukszta, S., D'Silva, P., et al. (2006) Evolution of mitochondrial chaperones utilized in Fe-S cluster biogenesis. Curr. Biol. 16, 1660-1665.
90. Lill, R., Hoffmann, B., Molik, S., Pierik, A. J., Rietzschel, N., et al. (2012) The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim. Biophys. Acta 1823, 1491-1508.
91. Weckbecker, D., Longen, S., Riemer, J., and, Herrmann, J. M., (2012). Atp23 biogenesis reveals a chaperone-like folding activity of Mia40 in the IMS of mitochondria. EMBO J. 31: 4348-4358.
92. Schreiner, B., Westerburg, H., Forné, I., Imhof, A., Neupert, W., et al. (2012). Role of the AAA protease Yme1 in folding of proteins in the intermembrane space of mitochondria. Mol. Biol. Cell 23: 4335-4346.
93. Wittig, I., and, Schägger, H., (2009). Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes. Biochim. Biophys. Acta 1787, 672-680.
94. Davies, K. M., Anselmi, C., Wittig, I., Faraldo-Gõmez, J. D., and, Kühlbrandt, W., (2012). Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. USA 109, 13602-13607.
95. Frey, T. G., and, Mannella, C.A., (2000). The internal structure of mitochondria. Trends Biochem. Sci. 25, 319-324.
96. Frezza, C., Cipolat, S., Martins de Brito, O., Micaroni, M., Beznoussenko, G. V., et al. (2006). OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126, 177-189.
97. Rabl, R., Soubannier, V., Scholz, R., Vogel, F., Mendl, N., et al. (2009) Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell Biol. 185, 1047-1063.
98. Wurm, C. A., and, Jakobs, S., (2006) Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast. FEBS Lett. 580, 5628-5634.
99. Vogel, F., Bornhövd, C., Neupert, W., and, Reichert, A. S., (2006) Dynamic subcompartmentalization of the mitochondrial inner membrane. J. Cell Biol. 175, 237-247.
100. Stoldt, S., Wenzel, D., Hildenbeutel, M., Wurm, C. A., Herrmann, J. M., et al. (2012) The inner-mitochondrial distribution of Oxa1 depends on the growth conditions and on the availability of substrates. Mol. Biol. Cell 23, 2292-2301.
101. Zerbes, R. M., van der Klei, I. J., Veenhuis, M., Pfanner, N., van der Laan, M., et al. (2012) Mitofilin complexes: conserved organizers of mitochondrial membrane architecture. Biol. Chem. 393, 1247-1261.
102. Tatsuta, T., and, Langer, T., (2008) Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J. 27, 306-314.
103. Fischer, F., Hamann, A., and, Osiewacz, H. D., (2012) Mitochondrial quality control: an integrated network of pathways. Trends Biochem. Sci. 37, 284-292.
104. Baker, M. J., Mooga, V. P., Guiard, B., Langer, T., Ryan, M. T., et al. (2012). Impaired folding of the mitochondrial small TIM chaperones induces clearance by the i-AAA protease. J. Mol. Biol. 424: 227-239.
105. Livnat-Levanon, N., and, Glickman, M. H., (2011) Ubiquitin-proteasome system and mitochondria-reciprocity. Biochim. Biophys. Acta 1809, 80-87.
106. Escobar-Henriques, M., Westermann, B., and, Langer, T., (2006) Regulation of mitochondrial fusion by the F-box protein Mdm30 involves proteasome-independent turnover of Fzo1. J. Cell Biol. 173, 645-650.
107. Cohen, M. M., Leboucher, G. P., Livnat-Levanon, N., Glickman, M. H., and, Weissman, A. M., (2008) Ubiquitin-proteasome-dependent degradation of a mitofusin, a critical regulator of mitochondrial fusion. Mol. Biol. Cell 19, 2457-2464.
108. Heo, J. M., Livnat-Levanon, N., Taylor, E. B., Jones, K. T., Dephoure, N., et al. (2010). A stress-responsive system for mitochondrial protein degradation. Mol. Cell 40, 465-480.
109. Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D. F., Gautier, C. A., et al. (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298.
110. Benard, G., Neutzner, A., Peng, G., Wang, C., Livak, F., et al. (2010) IBRDC2, an IBR-type E3 ubiquitin ligase, is a regulatory factor for Bax and apoptosis activation. EMBO J. 29, 1458-1471.
111. Moberg, P., Ståhl, A., Bhushan, S., Wright, S. J., Eriksson, A., et al. (2003) Characterization of a novel zinc metalloprotease involved in degrading targeting peptides in mitochondria and chloroplasts. Plant J. 36, 616-628.
112. Glaser, E., and, Alikhani, N., (2010) The organellar peptidasome, PreP: a journey from Arabidopsis to Alzheimer's disease. Biochim. Biophys. Acta 1797, 1076-1080.
113. Alikhani, N., Berglund, A. K., Engmann, T., Spånning, E., Vögtle, F. N., et al. (2011) Targeting capacity and conservation of PreP homologues localization in mitochondria of different species. J. Mol. Biol. 410, 400-410.
114. Young, L., Leonhard, K., Tatsuta, T., Trowsdale, J., and, Langer, T., (2001) Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science 291, 2135-2138.
115. Haynes, C. M., and, Ron, D., (2010) The mitochondrial UPR-protecting organelle protein homeostasis. J. Cell Sci. 123, 3849-3855.
116. Haynes, C. M., Yang, Y., Blais, S. P., Neubert, T. A., and, Ron, D., (2010) The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol. Cell 37, 529-540.
117. Kanki, T., Wang, K., Cao, Y., Baba, M., and, Klionsky, D. J., (2009) Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17, 98-109.
118. Okamoto, K., Kondo-Okamoto, N., and, Ohsumi, Y., (2009) Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17, 87-97.
119. Novak, I., Kirkin, V., McEwan, D. G., Zhang, J., Wild, P., et al. (2010) Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11, 45-51.
120. Matsuda, N., Sato, S., Shiba, K., Okatsu, K., Saisho, K., et al. (2010) PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol. 189, 211-221.