Mechanisms of protein sorting in mitochondria

Cold Spring Harbor Perspectives in Biology

Volumn 4, Issue 10, 2012, Pages

  Stojanovski, Diana ^a   Bohnert, Maria ^b   Pfanner, Nikolaus ^b   van der Laan, Martin ^b  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PROTEIN; SIGNAL PEPTIDE;

ARTICLE; BIOLOGICAL MODEL; EUKARYOTIC CELL; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PHYSIOLOGY; PROTEIN TRANSPORT;

EUKARYOTIC CELLS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT;

EID: 84867599882     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a011320     Document Type: Article

References (160)

1. Abe Y, Shodai T, Muto T, Mihara K, Torii H, Nishikawa S, Endo T, Kohda D. 2000. Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100: 551-560.
2. Ahting U, Thun C, Hegerl R, Typke D, Nargang FE, NeupertW, Nussberger S. 1999. The TOMcore complex: The general protein import pore of the outer membrane of mitochondria. J Cell Biol 147: 959-968.
3. Albrecht R, Rehling P, Chacinska A, Brix J, Cadamuro SA, Volkmer R, Guiard B, Pfanner N, Zeth K. 2006. The Tim21 binding domain connects the preprotein translocases of both mitochondrial membranes. EMBO Rep 7: 1233-1238.
4. Alder NN, Jensen RE, Johnson AE. 2008. Fluorescence mapping of mitochondrial TIM23 complex reveals a waterfacing, substrate-interacting helix surface. Cell 134: 439-450.
5. Baker MJ, Webb CT, Stroud DA, Palmer CS, Frazier AE, Guiard B, Chacinska A, Gulbis JM, RyanMT. 2009. Structural and functional requirements for activity of the Tim9-Tim10 complex in mitochondrial protein import. Mol Biol Cell 20: 769-779.
6. 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.
7. 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 107: 20190-20195.
8. 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 108: 4811-4816.
9. Becker L, Bannwarth M, Meisinger C, Hill K, Model K, Krimmer T, Casadio R, Truscott KN, Schulz GE, Pfanner N, et al. 2005. Preprotein translocase of the outer mitochondrial membrane: Reconstituted Tom40 forms a characteristic TOM pore. J Mol Biol 353: 1011-1020.
10. Becker T, Pfannschmidt S, Guiard B, Stojanovski D, MilenkovicD, Kutik S, Pfanner N, Meisinger C, Wiedemann N. 2008. Biogenesis of the mitochondrial TOM complex: Mim1 promotes insertion and assembly of signal-anchored receptors. J Biol Chem 283: 120-127.
11. Becker T, Guiard B, Thornton N, Zufall N, Stroud DA, Wiedemann N, Pfanner N. 2010. Assembly of the mitochondrial protein import channel: Role of Tom5 in twostage interaction of Tom40 with the SAM complex. Mo Biol Cell 21: 3106-3113.
12. Becker T, Wenz LS, Thornton N, Stroud D, Meisinger C, Wiedemann N, Pfanner N. 2011a. Biogenesis of mitochondria: Dual role of Tom7 in modulating assembly of the preprotein translocase of the outer membrane. J Mol Biol 405: 113-124.
13. Becker T, Wenz LS, Krüger V, Lehmann W, Müller JM, Goroncy L, Zufall N, Lithgow T, Guiard B, Chacinsk A, et al. 2011b. The mitochondrial import protein Mim1 promotes biogenesis of multispanning outer membrane proteins. J Cell Biol 194: 387-395.
14. Bhangoo MK, Tzankov S, Fan AC, Dejgaard K, Thomas DY, Young JC. 2007. Multiple 40-kDa heat-shock protein chaperones function in Tom70-dependent mitochondrial import. Mol Biol Cell 18: 3414-3428.
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. Bihlmaier K, Mesecke N, Terziyska N, Bien M, Hell K, Herrmann JM. 2007. The disulfide relay system of mitochondria is connected to the respiratory chain. J Cell Biol 179: 389-395.
17. Bohnert M, Rehling P, Guiard B, Herrmann JM, Pfanner N, van der Laan M. 2010. Cooperation of stop-transfer and conservative sorting mechanisms in mitochondrial protein transport. Curr Biol 20: 1227-1232.
18. Boldogh IR, Nowakowski DW, Yang HC, Chung H, Karmon S, Royes P, Pon LA. 2003. A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery. Mol Biol Cell 14: 4618-4627.
19. Brandner K, Rehling P, Truscott KN. 2005. The carboxylterminal third of the dicarboxylate carrier is crucial for productive association with the inner membrane twinpore translocase. J Biol Chem 280: 6215-6221.
20. Brix J, Dietmeier K, Pfanner N. 1997. Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, an Tom70. J Biol Chem 272: 20730-20735.
21. 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 TOMTIM-preprotein supercomplex. EMBO J 22: 5370-5381.
22. 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.
23. Chacinska A, Lind M, Frazier AE, Dudek J, Meisinger C, Geissler A, Sickmann A, Meyer HE, Truscott KN, Guiard B, et al. 2005. Mitochondrial presequence translocase: Switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120: 817-829.
24. 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.
25. Chacinska A, van der Laan M, Mehnert CS, Guiard B, Mick DU, Hutu DP, Truscott KN, Wiedemann N, Meisinger C, Pfanner N, et al. 2010. Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting. Mol Cell Biol 30: 307-318.
26. Chan NC, Lithgow T. 2008. The peripheral membrane subunits of the SAM complex function codependently in mitochondrial outer membrane biogenesis. Mol Biol Cell 19: 126-136.
27. Curran SP, Leuenberger D, Oppliger W, Koehler CM. 2002. The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier. EMBO J 21: 942-953.
28. 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 fro Erv1. EMBO J 26: 4801-4811.
29. Davey KM, Parboosingh JS, McLeod DR, Chan A, Casey R, Ferreira P, Snyder FF, Bridge PJ, Bernier FP. 2006. Mutation of DNAJC19, a human homologue of yeast inner mitochondrial membrane co-chaperones, causes DCMAsyndrome, a novel autosomal recessive Barth syndrome-like condition. J Med Genet 43: 385-393.
30. Davis AJ, Alder NN, Jensen RE, Johnson AE. 2007. The Tim9p/10p and Tim8p/13p complexes bind to specific sites on Tim23p during mitochondrial protein import. Mol Biol Cell 18: 475-486.
31. Dekker PJ, Martin F, Maarse AC, Bömer U, Müller H, Guiard B, Meijer M, Rassow J, Pfanner N. 1997. The Tim core complex defines the number of mitochondrial translocation sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44. EMBO J 16: 5408-5419.
32. Dekker PJ, Ryan MT, Brix J, Müller H, Hönlinger A, Pfanner N. 1998. Preprotein translocase of the outer mitochondrial membrane: molecular dissection and assembly of the general import pore complex. Mol Cell Biol 18: 6515-6524.
33. Devaux F, Lelandais G, Garcia M, Goussard S, Jacq C. 2010. Posttranscriptional control of mitochondrial biogenesis: Spatio-temporal regulation of the protein import process. FEBS Lett 584: 4273-4279.
34. Dolezal P, Likic V, Tachezy J, Lithgow T. 2006. Evolution of the molecular machines for protein import into mitochondria. Science 313: 314-318.
35. D'Silva PD, Schilke B, WalterW, Andrew A, Craig EA. 2003. J protein cochaperone of the mitochondrial inner membrane required for protein import into the mitochondrial matrix. Proc Natl Acad Sci 100: 13839-13844.
36. D'Silva P, Liu Q, WalterW, Craig EA. 2004. Regulated interactions of mtHsp70 with Tim44 at the translocon in the mitochondrial inner membrane. Nat Struct Mol Biol 11: 1084-1091.
37. D'Silva PR, Schilke B, Hayashi M, Craig EA. 2008. Interaction of the J-protein heterodimer Pam18/Pam16 of the mitochondrial import motor with the translocon of the inner membrane. Mol Biol Cell 19: 424-432.
38. Dukanovic J, Dimmer KS, Bonnefoy N, Krumpe K, Rapaport D. 2009. Genetic and functional interactions between the mitochondrial outer membrane protein Tom6 and Sam37. Mol Cell Biol 29: 5975-5988.
39. Fontaine B, Davoine CS, Durr A, Paternotte C, Feki I, Weissenbach J, Hazan J, Brice A. 2000. A new locus for autosomal dominant pure spastic paraplegia, on chromosome 2q24-q34. Am J Hum Genet 66: 702-707.
40. Frazier AE, Dudek J, Guiard B, Voos W, Li Y, Lind M, Meisinger C, Geissler A, Sickmann A, Meyer HE, et al. 2004. Pam16 has an essential role in the mitochondrial protein import motor. Nat Struct Mol Biol 11: 226-233.
41. Garcia M, Darzacq X, Delaveau T, Jourdren L, Singer RH, Jacq C. 2007. Mitochondria-associated yeast mRNAs and the biogenesis of molecular complexes. Mol Biol Cell 18: 362-368.
42. Garcia-Rodriguez LJ, Gay AC, Pon LA. 2007. Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast. J Cell Biol 176: 197-207.
43. Gebert N, Chacinska A, Wagner K, Guiard B, Koehler CM, Rehling P, Pfanner N, Wiedemann N. 2008. Assembly of the three small Tim proteins precedes docking to the mitochondrial carrier translocase. EMBO Rep 9: 548-554.
44. Gebert N, Joshi AS, Kutik S, BeckerT, McKenzieM, GuanXL, Mooga VP, StroudDA, Kulkarni G, Wenk MR, et al. 2009. Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: Implications for Barth syndrome. Curr Biol 19: 2133-2139.
45. Gebert N, Ryan MT, Pfanner N, Wiedemann N, Stojanovsk D. 2011a. Mitochondrial protein import machineries and lipids: A functional connection. Biochim Biophy Acta 1808: 1002-1011.
46. Gebert N, Gebert M, Oeljeklaus S, von der Malsburg K, Stroud DA, Kulawiak B, Wirth C, Zahedi RP, Dolezal P, Wiese S, et al. 2011b. Dual function of Sdh3 in the respiratory chain and TIM22 protein translocase of the mitochondrial inner membrane. Mol Cell 44: 811-818.
47. Gentle I, Gabriel K, Beech P, Waller R, Lithgow T. 2004. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164: 19-24.
48. Gevorkyan-Airapetov L, Zohary K, Popov-Čeleketić D, Mapa K, Hell K, Neupert W, Azem A, Mokranjac D. 2009. Interaction of Tim23 with Tim50 is essential for protein translocation by the mitochondrial TIM23 complex. J Biol Chem 284: 4865-4872.
49. 2are sorted to the intermembrane space of yeast mitochondria by a stoptransfer mechanism. Cell 69: 809-822.
50. 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.
51. Hansen JJ, Durr A, Cournu-Rebeix I, Georgopoulos C, Ang D, Nielsen MN, Davoine CS, Brice A, Fontaine B, Gregersen N, et al. 2002. Hereditary spastic paraplegia SPG13 is associatedwith a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am J Hum Genet 70: 1328-1332.
52. Harner M, Körner C, Walther D, Mokranjac D, Kaesmache J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W. 2011. The mitochondrial contact site complex, a determinant of mitochondrial ultrastructure. EMBO J 30: 4356-4370.
53. Hill K, Model K, RyanMT, Dietmeier K, Martin F, Wagner R, Pfanner N. 1998. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 395: 516-521.
54. Hoppins SC, Nargang FE. 2004. The Tim8-Tim13 complex ofNeurospora crassa functions in the assembly of proteins into both mitochondrial membranes. J Biol Chem 279: 12396-12405.
55. 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.
56. Hulett JM, Lueder F, Chan NC, Perry AJ, Wolynec P, Likic VA, Gooley PR, Lithgow T. 2008. The transmembrane segment of Tom20 is recognized by Mim1 for docking to the mitochondrial TOM complex. J Mol Biol 376: 694-704.
57. Hutu DP, Guiard B, Chacinska A, Becker D, Pfanner N, Rehling P, van der Laan M. 2008. Mitochondrial protein import motor: Differential role of Tim44 in the recruitment of Pam17 and J-complex to the presequence translocase. Mol Biol Cell 19: 2642-2649.
58. Iacovino M, Granycome C, Sembongi H, Bokori-Brown M, Butow RA, Holt IJ, Bateman JM. 2009. The conserved translocase Tim17 prevents mitochondrial DNA loss. Hum Mol Genet 18: 65-74.
59. Ishikawa D, Yamamoto H, Tamura Y, Moritoh K, Endo T. 2004. Two novel proteins in the mitochondrial outer membrane mediate b-barrel protein assembly. J Cell Biol 166: 621-627.
60. Kawano S, Yamano K, Naoé 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 106: 14403-14407.
61. Kemper C, Habib SJ, Engl G, Heckmeyer P, Dimmer KS, Rapaport D. 2008. Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. J Cell Sci 121: 1990-1998.
62. Kerscher O, Holder J, Srinivasan M, Leung RS, Jensen RE. 1997. The Tim54p-Tim22p complex mediates insertion of proteins into the mitochondrial inner membrane. J Cell Biol 139: 1663-1675.
63. Kerscher O, Sepuri NB, Jensen RE. 2000. Tim18p is a new component of the Tim54p-Tim22p translocon in the mitochondrial inner membrane. Mol Biol Cell 11: 103-116.
64. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR. 2009. Membrane protein architecture: the role of the BAM complex in outer membrane protein assembly. Nat Rev Microbiol 7: 206-214.
65. Koehler CM, Jarosch E, Tokatlidis K, Schmid K, Schweye RJ, Schatz G. 1998a. Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science 279: 369-373.
66. Koehler CM, Merchant S, OppligerW, Schmid K, Jarosch E, Dolfini L, Junne T, Schatz G, Tokatlidis K. 1998b. Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins. EMBO J 17: 6477-6486.
67. Koehler CM, Leuenberger D, Merchant S, Renold A, Junne T, Schatz G. 1999. Human deafness dystonia syndrome is a mitochondrial disease. Proc Natl Acad Sci 96: 2141-2146.
68. Koehler CM, Murphy MP, Bally NA, Leuenberger D, Oppliger W, Dolfini L, Junne T, Schatz G, Or E. 2000. Tim18p, a new subunit of the TIM22 complex that mediates insertion of imported proteins into the yeast mitochondrial inner membrane. Mol Cell Biol 20: 1187-1193.
69. Komiya T, Rospert S, Koehler C, Looser R, Schatz G, Mihara K. 1998. Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: Evidence for the "acid chain" hypothesis. EMBO J 17: 3886-3898.
70. Kornmann B, Walter P. 2010. ERMES-mediated ER-mitochondria contacts: Molecular hubs for the regulation of mitochondrial biology. J Cell Sci 123: 1389-1393.
71. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P. 2009. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325: 477-481.
72. Kornmann B, Osman C, Walter P. 2011. The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc Natl Acad Sci 108: 14151-14156.
73. Kozany C, Mokranjac D, Sichting M, Neupert W, Hell K. 2004. The J domain-related cochaperone Tim16 is a constituent of the mitochondrial TIM23 preprotein translocase. Nat Struct Mol Biol 11: 234-241.
74. Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278: 48520-48523.
75. Künkele KP, Heins S, Dembowski M, Nargang FE, Benz R, Thieffry M, Walz J, Lill R, Nussberger S, NeupertW. 1998. The preprotein translocation channel of the outer membrane of mitochondria. Cell 93: 1009-1019.
76. Kutik S, Stojanovski D, Becker L, Becker T, Meinecke M, Krüger V, Prinz C, Meisinger C, Guiard B, Wagner R, et al. 2008a. Dissecting membrane insertion of mitochondrial b-barrel proteins. Cell 132: 1011-1024.
77. Kutik S, Rissler M, Guan XL, Guiard B, Shui G, Gebert N, Heacock PN, Rehling P, Dowhan W, Wenk MR, et al. 2008b. The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis. J Cell Biol 183: 1213-1221.
78. Li Y, Dudek J, Guiard B, Pfanner N, Rehling P, VoosW. 2004. The presequence translocase-associated protein import motor of mitochondria. Pam16 functions in an antagonistic manner to Pam18. J Biol Chem 279: 38047-38054.
79. Luk E, Yang M, Jensen LT, Bourbonnais Y, Culotta VC. 2005. Manganese activation of superoxide dismutase 2 in the mitochondria of Saccharomyces cerevisiae. J Biol Chem 280: 22715-22720.
80. Mapa K, Sikor M, Kudryavtsev, Waegemann K, Kalinin S, Seidel CA, Neupert W, Lamb DC, Mokranjac D. 2010. The conformational dynamics of the mitochondrial Hsp70 chaperone. Mol Cell 38: 89-100.
81. Marc P, Margeot A, Devaux F, Blugeon C, Corral-Debrinsk M, Jacq C. 2002. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep 3: 159-164.
82. Marom M, Dayan D, Demishtein-Zohary K, Mokranjac D, Neupert W, Azem A. 2011. Direct interaction of mitochondrial targeting presequences with purified components of the TIM23 complex. J Biol Chem 286: 43809-43815.
83. Meier S, Neupert W, Herrmann JM. 2005. Conserved Nterminal negative charges in the Tim17 subunit of the TIM23 translocase play a critical role in the import of preproteins into mitochondria. J Biol Chem 280: 7777-7785.
84. Meinecke M, Wagner R, Kovermann P, Guiard B, Mick DU, Hutu DP, VoosW, Truscott KN, Chacinska A, Pfanner N, et al. 2006. Tim50 maintains the permeability barrier of the mitochondrial inner membrane. Science 312: 1523-1526.
85. Meisinger C, Rissler M, Chacinska A, Sanjuán Szklarz LK, Milenkovic D, Kozjak V, Schönfisch B, Lohaus C, Meyer HE, Yaffe MP, et al. 2004. The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane. Dev Cell 7: 61-71.
86. Meisinger C, Wiedemann N, Rissler M, Strub A, Milenkovi D, Schönfisch B, Müller H, Kozjak V, Pfanner N. 2006. Mitochondrial protein sorting: Differentiation of b-barrel assembly by Tom7-mediated segregation o Mdm10. J Biol Chem 281: 22819-22826.
87. Meisinger C, Pfannschmidt S, Rissler M, Milenkovic D, Becker T, Stojanovski D, Youngman MJ, Jensen RE, Chacinska A, Guiard B, et al. 2007. The morphology proteinsMdm12/Mmm1 function in the major b-barrel assembly pathway of mitochondria. EMBO J 26: 2229-2239.
88. Mesecke N, Terziyska N, Kozany C, Baumann F, NeupertW, Hell K, Herrmann JM. 2005. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121: 1059-1069.
89. Milenkovic D, Kozjak V, Wiedemann N, Lohaus C, Meyer HE, Guiard B, Pfanner N, Meisinger C. 2004. Sam35 of the mitochondrial protein sorting and assembly machinery is a peripheral outer membrane protein essential for cell viability. J Biol Chem 279: 22781-22785.
90. Milenkovic D, Gabriel K, Guiard B, Schulze-Specking A, Pfanner N, Chacinska A. 2007. Biogenesis of the essential Tim9-Tim10 chaperone complex of mitochondria: Sitespecific recognition of cysteine residues by the intermembrane space receptor Mia40. J Biol Chem 282: 22472-22480.
91. Milenkovic D, Ramming T, Müller JM, Wenz LS, Gebert N, Schulze-Specking A, StojanovskiD, Rospert S, Chacinsk A. 2009. Identification of the signal directing Tim9 and Tim10 into the intermembrane space of mitochondria. Mol Biol Cell 20: 2530-2539.
92. Moczko M, Bömer U, Kübrich M, Zufall N, Hönlinger A, Pfanner N. 1997. The intermembrane space domain of mitchondrial Tom22 functions as a trans binding site for preproteins with N-terminal targeting sequences. Mo Cell Biol 17: 6574-6584.
93. Model K, Meisinger C, Prinz T, Wiedemann N, Truscott KN, Pfanner N, Ryan MT. 2001. Multistep assembly of the protein import channel of the mitochondrial outer membrane. Nat Struct Biol 8: 361-370.
94. Mokranjac D, Sichting M, NeupertW, Hell K. 2003. Tim14, a novel key component of the import motor of the TIM23 protein translocase of mitochondria. EMBO J 22: 4945-4956.
95. Mokranjac D, Bourenkov G, Hell K, Neupert W, Groll M. 2006. Structure and function of Tim14 and Tim16, the J and J-like components of the mitochondrial protein import motor. EMBO J 25: 4675-4685.
96. Mokranjac D, Sichting M, Popov-Čeleketić D, Mapa K, Gevorkyan-Airapetov L, Zohary K, Hell K, Azem A, Neupert W. 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.
97. Naamati A, Regey-Rudzki N, Galperin S, Lill R, Pines O. 2009. Dual targeting of Nfs1 and discovery of its novel processing enzyme, Icp55. J Biol Chem 284: 30200-30208.
98. Naoé 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.
99. Neupert W, Herrmann JM. 2007. Translocation of proteins into mitochondria. Annu Rev Biochem 76: 723-749.
100. Nunnari J, FoxTD, Walter P. 1993. A mitochondrial protease with two catalytic subunits of nonoverlapping specificities. Science 262: 1997-2004.
101. Otera H, Taira Y, Horie C, Suzuki Y, Suzuki H, Setoguchi K, Kato H, Oka T, Mihara K. 2007. A novel insertion pathway of mitochondrial outer membrane proteins with multiple transmembrane segments. J Cell Biol 179: 1355-1363.
102. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, et al. 2008. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134: 112-123.
103. Pais JE, Schilke B, Craig EA. 2011. Re-evaluation of the role of the Pam18:Pam16 interaction in translocation of proteins by the mitochondrial Hsp70-based import motor. Mol Biol Cell 22: 4740-4749.
104. Papic D, Krumpe K, Dukanovic J, Dimmer KS, Rapaport D. 2011. Multispan mitochondrial outer membrane protein Ugo1 follows a unique Mim1-dependent import pathway. J Cell Biol 194: 397-405.
105. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, NeupertW. 2003. Evolutionary conservation of biogenesis of b-barrel membrane proteins. Nature 426: 862-866.
106. Popov-Čeleketić J, Waizenegger T, Rapaport D. 2008a. Mim1 functions in an oligomeric form to facilitate the integration of Tom20 into the mitochondrial outer membrane. J Mol Biol 376: 671-680.
107. Popov-Čeleketić D, Mapa K, Neupert W, Mokranjac D. 2008b. Active remodelling of the TIM23 complex during translocation of preproteins into mitochondria. EMBO J 27: 1469-1480.
108. Prokisch H, Scharfe C, Camp DG 2nd, Xiao W, David L, Andreoli C, Monroe ME, Moore RJ, Gritsenko MA, Kozany C, et al. 2004. Integrative analysis of the mitochondrial proteome in yeast. PLoS Biol 2: e160.
109. Qian X, Gebert M, Höpker J, Yan M, Li J, Wiedemann N, van der Laan M, Pfanner N, Sha B. 2011. Structural basis for the function of Tim50 in the mitochondrial presequence translocase. J Mol Biol 411: 513-519.
110. Rehling P, Model K, Brandner K, Kovermann P, Sickmann A, Meyer HE, Kühlbrandt W, Wagner R, Truscott KN, Pfanner N. 2003. Protein insertion into the mitochondrial inner membrane by a twin-pore translocase. Science 299: 1747-1751.
111. Reinders J, Zahedi RP, Pfanner N, Meisinger C, Sickmann A. 2006. Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J Proteome Res 5: 1543-1554.
112. 1-cytochrome oxidase supercomplex and its association with the TIM23 machinery. J Biol Chem 282: 6677-6686.
113. Saint-Georges Y, Garcia M, Delaveau T, Jourdren L, L Crom S, Lemoine S, Tanty V, Devaux F, Jacq C. 2008. Yeast mitochondrial biogenesis: A role for the PUF RNA-binding protein Puf3p in mRNA localization. PLoS ONE 4: e2293.
114. Saitoh T, Igura M, Obita T, Ose T, Kojima R, Maenaka K, Endo T, KohdaD. 2007. Tom20 recognizes mitochondrial presequences through dynamic equilibriumamong multiple bound states. EMBO J 26: 4777-4787.
115. Salhab M, Patani N, Jiang W, Mokbel K. 2010. High TIMM17A expression is associated with adverse pathological and clinical outcomes in human breast cancer. Breast Cancer 19: 153-160.
116. Schiller D, Cheng YC, Liu Q, Walter W, Craig EA. 2008. Residues of Tim44 involved in both association with the translocon of the inner mitochondrial membrane and regulation of mitochondrial Hsp70 tethering. Mo Cell Biol 28: 4424-4433.
117. Schmidt O, Harbauer AB, Rao S, Eyrich B, Zahedi RP, Stojanovski D, Schönfisch B, Guiard B, Sickmann A, Pfanner N, et al. 2011. Regulation of mitochondrial protein import by cytosolic kinases. Cell 144: 227-239.
118. Schulz C, Lytovchenko O, Melin J, Chacinska A, Guiard B, Neumann P, Ficner R, JahnO, Schmidt B, Rehling P. 2011. Tim50's presequence receptor domain is essential for signal driven transport across the TIM23 complex. J Cell Biol 195: 643-656.
119. Setoguchi K, Otera H, Mihara K. 2006. Cytosolic factorand TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J 25: 5635-5647.
120. Shiota T, Mabuchi H, Tanaka-Yamano S, Yamano K, End T. 2011. In vivo protein-interaction mapping of a mitochondrial translocator protein Tom22 at work. Pro Natl Acad Sci 108: 15179-15183.
121. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schönfisch B, Perschil I, Chacinska A, Guiard B, et al. 2003. The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci 100: 13207-13212.
122. 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.
123. Sideris DP, Petrakis N, Katrakili N, MikropoulouD, 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.
124. SinhaD, Joshi N, Chittoor B, Samji P, D'Silva P. 2010. Role of magmas in protein transport and human mitochondria biogenesis. Hum Mol Genet 19: 1248-1262.
125. Sirrenberg C, Bauer MF, Guiard B, Neupert W, Brunner M. 1996. Import of carrier proteins into the mitochondrial inner membrane mediated by Tim22. Nature 384: 582-585.
126. Sirrenberg C, Endres M, Folsch H, Stuart RA, Neupert W, Brunner M. 1998. Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/ Mrs11 and Tim12/Mrs5. Nature 391: 912-915.
127. Slutsky-Leiderman O, Marom M, Iosefson O, Levy R, Maoz S, Azem A. 2007. The interplay between components of the mitochondrial protein translocation motor studied using purified components. J Biol Chem 282: 33935-33942.
128. Stojanovski D, Guiard B, Kozjak-Pavlovic V, Pfanner N, Meisinger C. 2007. Alternative function for the mitochondrial SAM complex in biogenesis of a-helical TOM proteins. J Cell Biol 179: 881-893.
129. 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.
130. Stroud DA, Becker T, Qiu J, Stojanovski D, Pfannschmidt S, Wirth C, Hunte C, Guiard B, Meisinger C, Pfanner N, et al. 2011a. Biogenesis of mitochondrial b-barrel proteins: The POTRA domain is involved in precursor release from the SAM complex. Mol Biol Cell 22: 2823-2833.
131. Stroud DA, Oeljeklaus S, Wiese S, Bohnert M, Lewandrowski U, Sickmann A, Guiard B, van der Laan M, Warscheid B, Wiedemann N. 2011b. Composition and topology of the endoplasmic reticulum-mitochondria encounter structure. J Mol Biol 413: 743-750.
132. Tamura Y, Harada Y, Shiota T, Yamano K, Watanabe K, Yokota M, Yamamoto H, Sesaki H, Endo T. 2009a. Tim23-Tim50 pair coordinates functions of translocators and motor proteins in mitochondrial protein import. J Cell Biol 184: 129-141.
133. Tamura Y, Endo T, Iijima M, Sesaki H. 2009b. Ups1p and Ups2p antagonistically regulare cardiolipin metabolism in mitochondria. J Cell Biol 185: 1029-1045.
134. Taylor AB, Smith BS, Kitada S, Kojima K, Miyaura H, Otwinowski Z, Ito A, Deisenhofer J. 2001. Crystal structures of mitochondrial processing peptidase reveal the mode for specific cleavage of import signal sequences. Structure 9: 615-625.
135. Thornton N, Stroud DA, Milenkovic D, Guiard B, Pfanner N, Becker T. 2010. Two modular forms of the mitochondrial sorting and assembly machinery are involved in biogenesis of a-helical outer membrane proteins. J Mol Biol 396: 540-549.
136. Truscott KN, Voos W, Frazier AE, Lind M, Li Y, Geissler A, Dudek J, Müller H, Sickmann A, Meyer HE, et al. 2003. A J-protein is an essential subunit of the presequence translocase-associated protein import motor of mitochondria. J Cell Biol 163: 707-713.
137. van der Laan M, Chacinska A, Lind M, Perschil I, Sickmann A, Meyer HE, Guiard B, Meisinger C, Pfanner N, Rehling P. 2005. Pam17 is required for architecture and translocation activity of the mitochondrial protein import motor. Mol Cell Biol 25: 7449-7458.
138. van der Laan M, Wiedemann N, Mick DU, Guiard B, Rehling P, Pfanner N. 2006. A role for Tim21 in membrane-potential-dependent preprotein sorting in mitochondria. Curr Biol 16: 2271-2276.
139. van der Laan M, Meinecke M, Dudek J, Hutu DP, Lind M, Perschil I, Guiard B, Wagner R, Pfanner N, Rehling P. 2007. Motor-free mitochondrial presequence translocase drives membrane integration of preproteins. Nat Cell Biol 9: 1152-1159.
140. van Wilpe S, Ryan MT, Hill K, Maarse AC, Meisinger C, Brix J, Dekker PJ, Moczko M, Wagner R, Meijer M, et al. 1999. Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature 401: 485-489.
141. Vergnolle MA, Baud C, Golovanov AP, Alcock F, Luciano P, Lian LY, Tokatlidis K. 2005. Distinct domains of small Tims involved in subunit interaction and substrate recognition. J Mol Biol 351: 839-849.
142. Vögtle FN, Wortelkamp S, Zahedi RP, Becker D, Leidhold C, Gevaert K, Kellermann J, Voos W, Sickmann A, Pfanner N, et al. 2009. Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 139: 428-439.
143. Vögtle FN, Prinz C, Kellermann J, Lottspeich F, Pfanner N, Meisinger C. 2011. Mitochondrial protein turnover: Role of the precursor intermediate peptidase Oct1 in protein stabilization. Mol Biol Cell 22: 2135-2143.
144. von der Malsburg K, Müller 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.
145. Wagner K, Gebert N, Guiard B, Brandner K, Truscott KN, Wiedemann N, Pfanner N, Rehling P. 2008. The assembly pathway of the mitochondrial carrier translocase involves four preprotein translocases. Mol Cell Biol 28: 4251-4260.
146. Waizenegger T, Habib SJ, Lech M, MokranjacD, Paschen SA, Hell K, Neupert W, Rapaport D. 2004. Tob38, a novel essential component in the biogenesis of b-barrel proteins of mitochondria. EMBO Rep 5: 704-709.
147. Waizenegger T, Schmitt S, Zivkovic J, Neupert W, Rapapor D. 2005. Mim1, a protein required for the assembly of the TOM complex of mitochondria. EMBO Rep 6: 57-62.
148. Walther DM, Papic D, Bos MP, Tommassen J, Rapaport D. 2009. Signals in bacterial b-barrel proteins are functional in eukaryotic cells for targeting to and assembly in mitochondria. Proc Natl Acad Sci 106: 2531-2536.
149. Webb CT, Gorman MA, Lazarou M, Ryan MT, Gulbis JM. 2006. Crystal structure of the mitochondrial chaperone TIM9.10 reveals a six-bladed a-propeller. Mol Cell 21: 123-133.
150. Wideman JG, Go NE, Klein A, Redmond E, Lackey SW, Tao T, Kalbacher H, Rapaport D, Neupert W, Nargan FE. 2010. Roles of the Mdm10, Tom7, Mdm12, and Mmm1 proteins in the assembly of mitochondrial outer membrane proteins in Neurospora crassa. Mol Biol Cell 21: 1725-1736.
151. Wiedemann N, Pfanner N, Ryan MT. 2001. The three modules of ADP/ATP carrier cooperate in receptor recruitment and translocation into mitochondria. EMBO J 20: 951-960.
152. Wiedemann N, Kozjak V, Chacinska A, Schönfisch B, Rospert S, Ryan MT, Pfanner N, Meisinger C. 2003. Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424: 565-571.
153. Wiedemann N, Truscott KN, Pfannschmidt S, Guiard B, Meisinger C, Pfanner N. 2004. Biogenesis of the protein import channel Tom40 of the mitochondrial outer membrane: Intermembrane space components are involved in an early stage of the assembly pathway. J Biol Chem 279: 18188-18194.
154. Wiedemann N, van der Laan M, Hutu DP, Rehling P, Pfanner N. 2007. Sorting switch of mitochondrial presequence translocase involves coupling of motor module to respiratory chain. J Cell Biol 179: 1115-1122.
155. Wu Y, Sha B. 2006. Crystal structure of yeast mitochondrial outer membrane translocon member Tom70p. Nat Struct Mol Biol 13: 589-593.
156. Yamano K, Tanaka-Yamano S, Endo T. 2010. Tom7 regulates Mdm10-mediated assembly of the mitochondrial import channel protein Tom40. J Biol Chem 285: 41222-41231.
157. Yano M, Terada K, Mori M. 2003. AIP is a mitochondrial import mediator that binds to both import receptor Tom20 and preproteins. J Cell Biol 163: 45-56.
158. Yogev O, Karniely S, Pines O. 2007. Translation-coupled translocation of yeast fumarase into mitochondria in vivo. J Biol Chem 282: 29222-29229.
159. Young JC, Hoogenraad NJ, Hartl FU. 2003. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112: 41-50.
160. Zara V, Ferramosca A, Robitaille-Foucher P, Palmieri F, Young JC. 2009. Mitochondrial carrier protein biogenesis: role of the chaperones Hsc70 and Hsp90. Biochem J 419: 369-375.