1932

Abstract

Good fortune let me be an innocent child during World War II, a hopeful adolescent with encouraging parents during the years of German recovery, and a self-determined adult in a period of peace, freedom, and wealth. My luck continued as a scientist who could entirely follow his fancy. My mind was always set on understanding how things are made. At a certain point, I found myself confronted with the question of how mitochondria and organelles, which cannot be formed de novo, are put together. Intracellular transport of proteins, their translocation across the mitochondrial membranes, and their folding and assembly were the processes that fascinated me. Now, after some 30 years, we have wonderful insights, unimagined views of a complex and at the same time simple machinery and its workings. We have glimpses of how orderly processes are established in the cell to assemble from single molecules our beautiful mitochondria that every day make some 50 kg of ATP for each of us. At the same time, we have learned amazing lessons from the tinkering of evolution that developed mitochondria from bacteria.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-083109-171531
2012-07-07
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/biochem/81/1/annurev-biochem-083109-171531.html?itemId=/content/journals/10.1146/annurev-biochem-083109-171531&mimeType=html&fmt=ahah

Literature Cited

  1. Brosemer R, Vogell W, Bücher T. 1.  1963. Morphologische und enzymatische Muster bei der Entwicklung indirekter Flugmuskeln von Locusta migratoria. Biochem. Z. 338:854–910 [Google Scholar]
  2. Kleinow W, Neupert W, Miller F. 2.  1974. Electron microscope study of mitochondrial 60S and cytoplasmic 80S ribosomes from Locusta migratoria. J. Cell Biol. 62:860–75 [Google Scholar]
  3. Luck DJL. 3.  1963. Genesis of mitochondria in Neurospora crassa. Proc. Natl. Acad. Sci. USA 49:233–40 [Google Scholar]
  4. Aizawa Y, Xiang Q, Lambowitz AM, Pyle AM. 4.  2003. The pathway for DNA recognition and RNA integration by a group II intron retrotransposon. Mol. Cell 11:795–805 [Google Scholar]
  5. Sebald W, Machleidt W, Otto J. 5.  1973. Products of mitochondrial protein synthesis in Neurospora crassa. Determination of equimolar amounts of three products in cytochrome oxidase on the basis of amino-acid analysis. Eur. J. Biochem. 38:311–24 [Google Scholar]
  6. Weiss H, Ziganke B. 6.  1974. Cytochrome b in Neurospora crassa mitochondria. Site of translation of the heme protein. Eur. J. Biochem. 41:63–71 [Google Scholar]
  7. Kellems RE, Allison VF, Butow RA. 7.  1975. Cytoplasmic type 80S ribosomes associated with yeast mitochondria. J. Cell Biol. 65:1–14 [Google Scholar]
  8. Korb H, Neupert W. 8.  1978. Biogenesis of cytochrome c in Neurospora crassa. Synthesis of apocytochrome c, transfer to mitochondria and conversion to holocytochrome c. Eur. J. Biochem. 91:609–20 [Google Scholar]
  9. Hallermayer G, Zimmermann R, Neupert W. 9.  1977. Kinetic studies on the transport of cytoplasmically synthesized proteins into the mitochondria in intact cells of Neurospora crassa. Eur. J. Biochem. 81:523–32 [Google Scholar]
  10. Harmey MA, Hallermayer G, Korb H, Neupert W. 10.  1977. Transport of cytoplasmically synthesized proteins into the mitochondria in a cell free system from Neurospora crassa. Eur. J. Biochem. 81:533–44 [Google Scholar]
  11. Maccecchini ML, Rudin Y, Blobel G, Schatz G. 11.  1979. Import of proteins into mitochondria: precursor forms of the extramitochondrially made F1-ATPase subunits in yeast. Proc. Natl. Acad. Sci. USA 76:343–47 [Google Scholar]
  12. Harmey MA, Neupert W. 12.  1979. Biosynthesis of mitochondrial citrate synthase in Neurospora crassa. FEBS Lett. 108:385–89 [Google Scholar]
  13. Zimmerman R, Paluch U, Sprinzl M, Neupert W. 13.  1979. Cell-free synthesis of the mitochondrial ADP/ATP carrier protein of Neurospora crassa. Eur. J. Biochem. 99:247–52 [Google Scholar]
  14. Zimmermann R, Hennig B, Neupert W. 14.  1981. Different transport pathways of individual precursor proteins in mitochondria. Eur. J. Biochem. 116:455–60 [Google Scholar]
  15. Freitag H, Neupert W, Benz R. 15.  1982. Purification and characterisation of a pore protein of the outer mitochondrial membrane from Neurospora crassa. Eur. J. Biochem. 123:629–36 [Google Scholar]
  16. Pfaller R, Freitag H, Harmey MA, Benz R, Neupert W. 16.  1985. A water-soluble form of Porin from the mitochondrial outer membrane of Neurospora crassa. Properties and relationship to the biosynthetic precursor form. J. Biol. Chem. 260:8188–93 [Google Scholar]
  17. Schleyer M, Neupert W. 17.  1985. Transport of proteins into mitochondria: translocational intermediates spanning contact sites between outer and inner membranes. Cell 43:339–50 [Google Scholar]
  18. Schwaiger M, Herzog V, Neupert W. 18.  1987. Characterization of translocation contact sites involved in the import of mitochondrial proteins. J. Cell Biol. 105:235–46 [Google Scholar]
  19. Eilers M, Hwang S, Schatz G. 19.  1988. Unfolding and refolding of a purified precursor protein during import into isolated mitochondria. EMBO J. 7:1139–45 [Google Scholar]
  20. Hawlitschek G, Schneider H, Schmidt B, Tropschug M, Hartl FU, Neupert W. 20.  1988. Mitochondrial protein import: identification of processing peptidase and of PEP, a processing enhancing protein. Cell 53:795–806 [Google Scholar]
  21. Witte C, Jensen RE, Yaffe MP, Schatz G. 21.  1988. MAS1, a gene essential for yeast mitochondrial assembly, encodes a subunit of the mitochondrial processing protease. EMBO J. 7:1439–47 [Google Scholar]
  22. Yang M, Jensen RE, Yaffe MP, Oppliger W, Schatz G. 22.  1988. Import of proteins into yeast mitochondria: The purified matrix processing protease contains two subunits which are encoded by the nuclear MAS1 and MAS2 genes. EMBO J. 7:3857–62 [Google Scholar]
  23. Schulte U, Arretz M, Schneider H, Tropschug M, Wachter E. 23.  et al. 1989. A family of mitochondrial proteins involved in bioenergetics and biogenesis. Nature 339:147–49 [Google Scholar]
  24. Bolhuis A, Koetje E, Dubois JY, Vehmaanpera J, Venema G. 24.  et al. 2000. Did the mitochondrial processing peptidase evolve from a eubacterial regulator of gene expression?. Mol. Biol. Evol. 17:198–201 [Google Scholar]
  25. Sollner T, Griffiths G, Pfaller R, Pfanner N, Neupert W. 25.  1989. MOM19, an import receptor for mitochondrial precursor proteins. Cell 59:1061–70 [Google Scholar]
  26. Sollner T, Pfaller R, Griffiths G, Pfanner N, Neupert W. 26.  1990. A mitochondrial import receptor for the ADP/ATP carrier. Cell 62:107–15 [Google Scholar]
  27. Kiebler M, Pfaller R, Sollner T, Griffiths G, Horstmann H. 27.  et al. 1990. Identification of a mitochondrial receptor complex required for recognition and membrane insertion of precursor proteins. Nature 348:610–16 [Google Scholar]
  28. Baker KP, Schaniel A, Vestweber D, Schatz G. 28.  1990. A yeast mitochondrial outer membrane protein essential for protein import and cell viability. Nature 348:605–9 [Google Scholar]
  29. Kiebler M, Keil P, Schneider H, van der Klei IJ, Pfanner N, Neupert W. 29.  1993. The mitochondrial receptor complex: a central role of MOM22 in mediating preprotein transfer from receptors to the general insertion pore. Cell 74:483–92 [Google Scholar]
  30. Endo T, Yamano K, Kawano S. 30.  2011. Structural insight into the mitochondrial protein import system. Biochim. Biophys. Acta 1808:955–70 [Google Scholar]
  31. Mayer A, Lill R, Neupert W. 31.  1993. Translocation and insertion of precursor proteins into isolated outer membranes of mitochondria. J. Cell Biol. 121:1233–43 [Google Scholar]
  32. Mayer A, Neupert W, Lill R. 32.  1995. Mitochondrial protein import: Reversible binding of the presequence at the trans side of the outer membrane drives partial translocation and unfolding. Cell 80:127–37 [Google Scholar]
  33. Künkele KP, Heins S, Dembowski M, Nargang FE, Benz R. 33.  et al. 1998. The preprotein translocation channel of the outer membrane of mitochondria. Cell 93:1009–19 [Google Scholar]
  34. Künkele KP, Juin P, Pompa C, Nargang FE, Henry JP. 34.  et al. 1998. The isolated complex of the translocase of the outer membrane of mitochondria. Characterization of the cation-selective and voltage-gated preprotein-conducting pore. J. Biol. Chem. 273:31032–39 [Google Scholar]
  35. Stan T, Ahting U, Dembowski M, Künkele KP, Nussberger S. 35.  et al. 2000. Recognition of preproteins by the isolated TOM complex of mitochondria. EMBO J. 19:4895–902 [Google Scholar]
  36. Ahting U, Thieffry M, Engelhardt H, Hegerl R, Neupert W, Nussberger S. 36.  2001. Tom40, the pore-forming component of the protein-conducting TOM channel in the outer membrane of mitochondria. J. Cell Biol. 153:1151–60 [Google Scholar]
  37. Cheng MY, Hartl FU, Martin J, Pollock RA, Kalousek F. 37.  et al. 1989. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337:620–25 [Google Scholar]
  38. Ellis J. 38.  1987. Proteins as molecular chaperones. Nature 328:378–79 [Google Scholar]
  39. Anfinsen CB. 39.  1973. Principles that govern the folding of protein chains. Science 181:223–30 [Google Scholar]
  40. Ostermann J, Horwich AL, Neupert W, Hartl FU. 40.  1989. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature 341:125–30 [Google Scholar]
  41. Craig EA, Kramer J, Shilling J, Werner-Washburne M, Holmes S. 41.  et al. 1989. SSC1, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein. Mol. Cell. Biol. 9:3000–8 [Google Scholar]
  42. Kang PJ, Ostermann J, Shilling J, Neupert W, Craig EA, Pfanner N. 42.  1990. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348:137–43 [Google Scholar]
  43. Ungermann C, Neupert W, Cyr DM. 43.  1994. The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science 266:1250–53 [Google Scholar]
  44. Ungermann C, Guiard B, Neupert W, Cyr DM. 44.  1996. The delta psi- and Hsp70/MIM44-dependent reaction cycle driving early steps of protein import into mitochondria. EMBO J. 15:735–44 [Google Scholar]
  45. Yogev O, Pines O. 45.  2011. Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochim. Biophys. Acta 1808:1012–20 [Google Scholar]
  46. Rowley N, Prip-Buus C, Westermann B, Brown C, Schwarz E. 46.  et al. 1994. Mdj1p, a novel chaperone of the DnaJ family, is involved in mitochondrial biogenesis and protein folding. Cell 77:249–59 [Google Scholar]
  47. Maarse AC, Blom J, Grivell LA, Meijer M. 47.  1992. MPI1, an essential gene encoding a mitochondrial membrane protein, is possibly involved in protein import into yeast mitochondria. EMBO J. 11:3619–28 [Google Scholar]
  48. Emtage JLT, Jensen RE. 48.  1993. MAS6 encodes an essential inner membrane component of the yeast mitochondrial protein import pathway. J. Cell Biol. 122:1003–12 [Google Scholar]
  49. Ryan KR, Menold MM, Garrett S, Jensen RE. 49.  1994. SMS1, a high-copy suppressor of the yeast mas6 mutant, encodes an essential inner membrane protein required for mitochondrial protein import. Mol. Biol. Cell 5:529–38 [Google Scholar]
  50. Schneider HC, Berthold J, Bauer MF, Dietmeier K, Guiard B. 50.  et al. 1994. Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature 371:768–74 [Google Scholar]
  51. Berthold J, Bauer MF, Schneider HC, Klaus C, Dietmeier K. 51.  et al. 1995. The MIM complex mediates preprotein translocation across the mitochondrial inner membrane and couples it to the mt-Hsp70/ATP driving system. Cell 81:1085–93 [Google Scholar]
  52. Okamoto K, Brinker A, Paschen SA, Moarefi I, Hayer-Hartl M. 52.  et al. 2002. The protein import motor of mitochondria: a targeted molecular ratchet driving unfolding and translocation. EMBO J. 21:3659–71 [Google Scholar]
  53. Neupert W, Brunner M. 52a.  2002. The protein import motor of mitochondria. Nat. Rev. Mol. Cell Biol. 3:555–65 [Google Scholar]
  54. Yamano K, Kuroyanagi-Hasegawa M, Esaki M, Yokota M, Endo T. 53.  2008. Step-size analyses of the mitochondrial Hsp70 import motor reveal the Brownian ratchet in operation. J. Biol. Chem. 283:27325–32 [Google Scholar]
  55. Bauer MF, Sirrenberg C, Neupert W, Brunner M. 54.  1996. Role of Tim23 as voltage sensor and presequence receptor in protein import into mitochondria. Cell 87:33–41 [Google Scholar]
  56. Alder NN, Jensen RE, Johnson AE. 55.  2008. Fluorescence mapping of mitochondrial TIM23 complex reveals a water-facing, substrate-interacting helix surface. Cell 134:439–50 [Google Scholar]
  57. Geissler A, Chacinska A, Truscott KN, Wiedemann N, Brandner K. 56.  et al. 2002. The mitochondrial presequence translocase: an essential role of Tim50 in directing preproteins to the import channel. Cell 111:507–18 [Google Scholar]
  58. Yamamoto H, Esaki M, Kanamori T, Tamura Y, Nishikawa S, Endo T. 57.  2002. Tim50 is a subunit of the TIM23 complex that links protein translocation across the outer and inner mitochondrial membranes. Cell 111:519–28 [Google Scholar]
  59. Mokranjac D, Paschen SA, Kozany C, Prokisch H, Hoppins SC. 58.  et al. 2003. Tim50, a novel component of the TIM23 preprotein translocase of mitochondria. EMBO J. 22:816–25 [Google Scholar]
  60. van der Laan M, Chacinska A, Lind M, Perschil I, Sickmann A. 59.  et al. 2005. Pam17 is required for architecture and translocation activity of the mitochondrial protein import motor. Mol. Cell. Biol. 25:7449–58 [Google Scholar]
  61. Chacinska A, Lind M, Frazier AE, Dudek J, Meisinger C. 60.  et al. 2005. Mitochondrial presequence translocase: Switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120:817–29 [Google Scholar]
  62. Mokranjac D, Popov-Celeketic D, Hell K, Neupert W. 61.  2005. Role of Tim21 in mitochondrial translocation contact sites. J. Biol. Chem. 280:23437–40 [Google Scholar]
  63. Westermann B, Prip-Buus C, Neupert W, Schwarz E. 62.  1995. The role of the GrpE homologue, Mge1p, in mediating protein import and protein folding in mitochondria. EMBO J. 14:3452–60 [Google Scholar]
  64. Mokranjac D, Sichting M, Neupert W, Hell K. 63.  2003. Tim14, a novel key component of the import motor of the TIM23 protein translocase of mitochondria. EMBO J. 22:4945–56 [Google Scholar]
  65. Truscott KN, Voos W, Frazier AE, Lind M, Li Y. 64.  et al. 2003. A J-protein is an essential subunit of the presequence translocase-associated protein import motor of mitochondria. J. Cell Biol. 163:707–13 [Google Scholar]
  66. D'Silva PD, Schilke B, Walter W, Andrew A, Craig EA. 65.  2003. J protein cochaperone of the mitochondrial inner membrane required for protein import into the mitochondrial matrix. Proc. Natl. Acad. Sci. USA 100:13839–44 [Google Scholar]
  67. Kozany C, Mokranjac D, Sichting M, Neupert W, Hell K. 66.  2004. The J domain–related cochaperone Tim16 is a constituent of the mitochondrial TIM23 preprotein translocase. Nat. Struct. Mol. Biol. 11:234–41 [Google Scholar]
  68. Mokranjac D, Berg A, Adam A, Neupert W, Hell K. 67.  2007. Association of the Tim14•Tim16 subcomplex with the TIM23 translocase is crucial for function of the mitochondrial protein import motor. J. Biol. Chem. 282:18037–45 [Google Scholar]
  69. Mokranjac D, Bourenkov G, Hell K, Neupert W, Groll M. 68.  2006. Structure and function of Tim14 and Tim16, the J and J-like components of the mitochondrial protein import motor. EMBO J. 25:4675–85 [Google Scholar]
  70. Popov-Celeketic D, Mapa K, Neupert W, Mokranjac D. 69.  2008. Active remodelling of the TIM23 complex during translocation of preproteins into mitochondria. EMBO J. 27:1469–80 [Google Scholar]
  71. Wiedemann N, van der Laan M, Hutu DP, Rehling P, Pfanner N. 70.  2007. Sorting switch of mitochondrial presequence translocase involves coupling of motor module to respiratory chain. J. Cell Biol. 179:1115–22 [Google Scholar]
  72. Popov-Celeketic D, Waegemann K, Mapa K, Neupert W, Mokranjac D. 71.  2011. Role of the import motor in insertion of transmembrane segments by the mitochondrial TIM23 complex. EMBO Rep. 12:542–48 [Google Scholar]
  73. Nobrega FG, Nobrega MP, Tzagoloff A. 72.  1992. BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae. EMBO J. 11:3821–29 [Google Scholar]
  74. Folsch H, Guiard B, Neupert W, Stuart RA. 73.  1996. Internal targeting signal of the BCS1 protein: a novel mechanism of import into mitochondria. EMBO J. 15:479–87 [Google Scholar]
  75. Herlan M, Vogel F, Bornhovd C, Neupert W, Reichert AS. 74.  2003. Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J. Biol. Chem. 278:27781–88 [Google Scholar]
  76. Herlan M, Bornhovd C, Hell K, Neupert W, Reichert AS. 75.  2004. Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J. Cell Biol. 165:167–73 [Google Scholar]
  77. Ishihara N, Fujita Y, Oka T, Mihara K. 76.  2006. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25:2966–77 [Google Scholar]
  78. Duvezin-Caubet S, Koppen M, Wagener J, Zick M, Israel L. 77.  et al. 2007. OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA protease in mitochondria. Mol. Biol. Cell 18:3582–90 [Google Scholar]
  79. Donzeau M, Kaldi K, Adam A, Paschen S, Wanner G. 78.  et al. 2000. Tim23 links the inner and outer mitochondrial membranes. Cell 101:401–12 [Google Scholar]
  80. Sirrenberg C, Bauer MF, Guiard B, Neupert W, Brunner M. 79.  1996. Import of carrier proteins into the mitochondrial inner membrane mediated by Tim22. Nature 384:582–85 [Google Scholar]
  81. Kerscher O, Holder J, Srinivasan M, Leung RS, Jensen RE. 80.  1997. The Tim54p-Tim22p complex mediates insertion of proteins into the mitochondrial inner membrane. J. Cell Biol. 139:1663–75 [Google Scholar]
  82. Kerscher O, Sepuri NB, Jensen RE. 81.  2000. Tim18p is a new component of the Tim54p-Tim22p translocon in the mitochondrial inner membrane. Mol. Biol. Cell 11:103–16 [Google Scholar]
  83. Koehler CM, Murphy MP, Bally NA, Leuenberger D, Oppliger W. 82.  et al. 2000. Tim18p, a new subunit of the TIM22 complex that mediates insertion of imported proteins into the yeast mitochondrial inner membrane. Mol. Cell. Biol. 20:1187–93 [Google Scholar]
  84. Sirrenberg C, Endres M, Folsch H, Stuart RA, Neupert W, Brunner M. 83.  1998. Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature 391:912–15 [Google Scholar]
  85. Koehler CM, Jarosch E, Tokatlidis K, Schmid K, Schweyen RJ, Schatz G. 84.  1998. Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science 279:369–73 [Google Scholar]
  86. Koehler CM, Merchant S, Oppliger W, Schmid K, Jarosch E. 85.  et al. 1998. Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins. EMBO J. 17:6477–86 [Google Scholar]
  87. Adam A, Endres M, Sirrenberg C, Lottspeich F, Neupert W, Brunner M. 86.  1999. Tim9, a new component of the TIM22•54 translocase in mitochondria. EMBO J. 18:313–19 [Google Scholar]
  88. Lutz T, Neupert W, Herrmann JM. 87.  2003. Import of small Tim proteins into the mitochondrial intermembrane space. EMBO J. 22:4400–8 [Google Scholar]
  89. Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuan Szklarz LK. 88.  et al. 2004. Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J. 23:3735–46 [Google Scholar]
  90. Naoe M, Ohwa Y, Ishikawa D, Ohshima C, Nishikawa S. 89.  et al. 2004. Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J. Biol. Chem. 279:47815–21 [Google Scholar]
  91. Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N. 90.  et al. 2005. Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett. 579:179–84 [Google Scholar]
  92. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W. 91.  et al. 2005. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121:1059–69 [Google Scholar]
  93. Sideris DP, Tokatlidis K. 92.  2007. Oxidative folding of small Tims is mediated by site-specific docking onto Mia40 in the mitochondrial intermembrane space. Mol. Microbiol. 65:1360–73 [Google Scholar]
  94. Koehler CM, Tienson HL. 93.  2009. Redox regulation of protein folding in the mitochondrial intermembrane space. Biochim. Biophys. Acta 1793:139–45 [Google Scholar]
  95. Hell K. 94.  2008. The Erv1-Mia40 disulfide relay system in the intermembrane space of mitochondria. Biochim. Biophys. Acta 1783:601–9 [Google Scholar]
  96. Bonnefoy N, Chalvet F, Hamel P, Slonimski PP, Dujardin G. 95.  1994. OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J. Mol. Biol. 239:201–12 [Google Scholar]
  97. Bauer M, Behrens M, Esser K, Michaelis G, Pratje E. 96.  1994. PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast. Mol. Gen. Genet. 245:272–78 [Google Scholar]
  98. Hell K, Herrmann JM, Pratje E, Neupert W, Stuart RA. 97.  1998. Oxa1p, an essential component of the N-tail protein export machinery in mitochondria. Proc. Natl. Acad. Sci. USA 95:2250–55 [Google Scholar]
  99. Bonnefoy N, Fiumera HL, Dujardin G, Fox TD. 98.  2009. Roles of Oxa1-related inner-membrane translocases in assembly of respiratory chain complexes. Biochim. Biophys. Acta 1793:60–70 [Google Scholar]
  100. Herrmann JM, Neupert W, Stuart RA. 99.  1997. Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p. EMBO J. 16:2217–26 [Google Scholar]
  101. Szyrach G, Ott M, Bonnefoy N, Neupert W, Herrmann JM. 100.  2003. Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria. EMBO J. 22:6448–57 [Google Scholar]
  102. Preuss M, Ott M, Funes S, Luirink J, Herrmann JM. 101.  2005. Evolution of mitochondrial Oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery. J. Biol. Chem. 280:13004–11 [Google Scholar]
  103. Meier S, Neupert W, Herrmann JM. 102.  2005. Proline residues of transmembrane domains determine the sorting of inner membrane proteins in mitochondria. J. Cell Biol. 170:881–88 [Google Scholar]
  104. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M. 103.  et al. 2003. Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426:862–66 [Google Scholar]
  105. Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE. 104.  et al. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J. Biol. Chem. 278:48520–23 [Google Scholar]
  106. Endo T, Yamano K. 105.  2010. Transport of proteins across or into the mitochondrial outer membrane. Biochim. Biophys. Acta 1803:706–14 [Google Scholar]
  107. Wagener N, Ackermann M, Funes S, Neupert W. 105a.  2011. A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol. Cell 44:191–202 [Google Scholar]
  108. Wagner I, Arlt H, van Dyck L, Langer T, Neupert W. 106.  1994. Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J. 13:5135–45 [Google Scholar]
  109. Arlt H, Tauer R, Feldmann H, Neupert W, Langer T. 107.  1996. The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell 85:875–85 [Google Scholar]
  110. Leonhard K, Herrmann JM, Stuart RA, Mannhaupt G, Neupert W, Langer T. 108.  1996. AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J. 15:4218–29 [Google Scholar]
  111. Ito K, Akiyama Y. 109.  2005. Cellular functions, mechanism of action, and regulation of FtsH protease. Annu. Rev. Microbiol. 59:211–31 [Google Scholar]
  112. Casari G, De Fusco M, Ciarmatori S, Zeviani M, Mora M. 110.  et al. 1998. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 93:973–83 [Google Scholar]
  113. Tatsuta T, Langer T. 111.  2009. AAA proteases in mitochondria: diverse functions of membrane-bound proteolytic machines. Res. Microbiol. 160:711–17 [Google Scholar]
  114. Tatsuta T, Augustin S, Nolden M, Friedrichs B, Langer T. 112.  2007. m-AAA protease-driven membrane dislocation allows intramembrane cleavage by rhomboid in mitochondria. EMBO J. 26:325–35 [Google Scholar]
  115. Hackenbrock CR. 113.  1966. Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J. Cell Biol. 30:269–97 [Google Scholar]
  116. Rabl R, Soubannier V, Scholz R, Vogel F, Mendl N. 113a.  et al. 2009. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell. Biol. 185:1047–63 [Google Scholar]
  117. Harner M, Körner C, Walther D, Mokranjac, Kaesmacher J. 113b.  et al. 2011. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 30:4356–70 [Google Scholar]
  118. Neupert W, Herrmann JM. 114.  2007. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76:723–49 [Google Scholar]
  119. Neupert W. 115.  1997. Protein import into mitochondria. Annu. Rev. Biochem. 66:863–917 [Google Scholar]
  120. Mokranjac D, Neupert W. 116.  2010. The many faces of the mitochondrial TIM23 complex. Biochim. Biophys. Acta 1797:1045–54 [Google Scholar]
  121. Lithgow T, Schneider A. 117.  2010. Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos. Trans. R. Soc. Lond. Ser. B 365:799–817 [Google Scholar]
  122. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. 118.  2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628–44 [Google Scholar]
  123. Harmey MA, Neupert W. 119.  1985. Synthesis and intracellular transport of mitochondrial proteins. The Enzymes of Biological Membranes A Martonosi 4431–64 New York: Plenum [Google Scholar]
/content/journals/10.1146/annurev-biochem-083109-171531
Loading
/content/journals/10.1146/annurev-biochem-083109-171531
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error