1932

Abstract

Mitochondria are essential organelles of endosymbiotic origin that are responsible for oxidative phosphorylation within eukaryotic cells. Independent evolution between species has generated mitochondrial genomes that are extremely diverse, with the composition of the vestigial genome determining their translational requirements. Typically, translation within mitochondria is restricted to a few key subunits of the oxidative phosphorylation complexes that are synthesized by dedicated ribosomes (mitoribosomes). The dramatically rearranged mitochondrial genomes, the limited set of transcripts, and the need for the synthesized proteins to coassemble with nuclear-encoded subunits have had substantial consequences for the translation machinery. Recent high-resolution cryo–electron microscopy has revealed the effect of coevolution on the mitoribosome with the mitochondrial genome. In this review, we place the new structural information in the context of the molecular mechanisms of mitochondrial translation and focus on the novel ways protein synthesis is organized and regulated in mitochondria.

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2016-06-02
2024-03-28
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Literature Cited

  1. Sagan L. 1.  1967. On the origin of mitosing cells. J. Theor. Biol 14:255–74 [Google Scholar]
  2. Christian BE, Spremulli LL. 2.  2012. Mechanism of protein biosynthesis in mammalian mitochondria. Biochim. Biophys. Acta 1819:1035–54 [Google Scholar]
  3. Gustafsson CM, Falkenberg M, Larsson NG. 3. 2016 Maintenance and expression of mammalian mitochondrial DNA. Annu. Rev. Biochem. 85:133–60 [Google Scholar]
  4. Van Haute L, Pearce SF, Powell CA, D'Souza AR, Nicholls TJ, Minczuk M. 4.  2015. Mitochondrial transcript maturation and its disorders. J. Inherit. Metab. Dis. 38:655–80 [Google Scholar]
  5. Powell CA, Nicholls TJ, Minczuk M. 5.  2015. Nuclear-encoded factors involved in post-transcriptional processing and modification of mitochondrial tRNAs in human disease. Front. Genet. 6:79 [Google Scholar]
  6. Hällberg BM, Larsson NG. 6.  2014. Making proteins in the powerhouse. Cell Metab. 20:226–40 [Google Scholar]
  7. Szczesny RJ, Borowski LS, Malecki M, Wojcik MA, Stepien PP, Golik P. 7.  2012. RNA degradation in yeast and human mitochondria. Biochim. Biophys. Acta 1819:1027–34 [Google Scholar]
  8. Salinas-Giege T, Giege R, Giege P. 8.  2015. tRNA biology in mitochondria. Int. J. Mol. Sci. 16:4518–59 [Google Scholar]
  9. De Silva D, Tu YT, Amunts A, Fontanesi F, Barrientos A. 9.  2015. Mitochondrial ribosome assembly in health and disease. Cell Cycle 14:2226–50 [Google Scholar]
  10. Johnston SA, Anziano PQ, Shark K, Sanford JC, Butow RA. 10.  1988. Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 240:1538–41 [Google Scholar]
  11. Fox TD, Sanford JC, McMullin TW. 11.  1988. Plasmids can stably transform yeast mitochondria lacking endogenous mtDNA. PNAS 85:7288–92 [Google Scholar]
  12. Burger G, Gray MW, Lang BF. 12.  2003. Mitochondrial genomes: Anything goes. Trends Genet. 19:709–16 [Google Scholar]
  13. Nierman WC, Feldblyum TV, Laub MT, Paulsen IT, Nelson KE. 13.  et al. 2001. Complete genome sequence of Caulobacter crescentus. PNAS 98:4136–41 [Google Scholar]
  14. Fu Q, Li H, Moorjani P, Jay F, Slepchenko SM. 14.  et al. 2014. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514:445–49 [Google Scholar]
  15. Rocha EP, Danchin A. 15.  2002. Base composition bias might result from competition for metabolic resources. Trends Genet. 18:291–94 [Google Scholar]
  16. Martin AP. 16.  1995. Metabolic rate and directional nucleotide substitution in animal mitochondrial DNA. Mol. Biol. Evol. 12:1124–31 [Google Scholar]
  17. von Heijne G. 17.  1986. Why mitochondria need a genome. FEBS Lett. 198:1–4 [Google Scholar]
  18. Claros MG, Perea J, Shu YM, Samatey FA, Popot JL, Jacq C. 18.  1995. Limitations to in vivo import of hydrophobic proteins into yeast mitochondria: the case of a cytoplasmically synthesized apocytochrome b. Eur. J. Biochem. 228:762–71 [Google Scholar]
  19. Allen JF. 19.  2003. Why chloroplasts and mitochondria contain genomes. Comp. Funct. Genomics 4:31–36 [Google Scholar]
  20. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R. 20.  et al. 2003. The proteome of Saccharomyces cerevisiae mitochondria. PNAS 100:13207–12 [Google Scholar]
  21. Andreoli C, Prokisch H, Hortnagel K, Mueller JC, Munsterkotter M. 21.  et al. 2004. MitoP2, an integrated database on mitochondrial proteins in yeast and man. Nucleic Acids Res. 32:D459–62 [Google Scholar]
  22. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. 22.  2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628–44 [Google Scholar]
  23. Neupert W. 23.  2015. A perspective on transport of proteins into mitochondria: a myriad of open questions. J. Mol. Biol. 427:1135–58 [Google Scholar]
  24. Barrell BG, Bankier AT, Drouin J. 24.  1979. A different genetic code in human mitochondria. Nature 282:189–94 [Google Scholar]
  25. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR. 25.  et al. 1981. Sequence and organization of the human mitochondrial genome. Nature 290:457–65 [Google Scholar]
  26. Hancock K, Hajduk SL. 26.  1990. The mitochondrial tRNAs of Trypanosoma brucei are nuclear encoded. J. Biol. Chem. 265:19208–15 [Google Scholar]
  27. Schneider A. 27.  2011. Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu. Rev. Biochem. 80:1033–53 [Google Scholar]
  28. Jühling F, Putz J, Florentz C, Stadler PF. 28.  2012. Armless mitochondrial tRNAs in Enoplea (Nematoda). RNA Biol. 9:1161–66 [Google Scholar]
  29. Wende S, Platzer EG, Jühling F, Putz J, Florentz C. 29.  et al. 2014. Biological evidence for the world's smallest tRNAs. Biochimie 100:151–58 [Google Scholar]
  30. Chimnaronk S, Gravers Jeppesen M, Suzuki T, Nyborg J, Watanabe K. 30.  2005. Dual-mode recognition of noncanonical tRNAsSer by seryl-tRNA synthetase in mammalian mitochondria. EMBO J. 24:3369–79 [Google Scholar]
  31. Brown A, Amunts A, Bai XC, Sugimoto Y, Edwards PC. 31.  et al. 2014. Structure of the large ribosomal subunit from human mitochondria. Science 346:718–22 [Google Scholar]
  32. Amunts A, Brown A, Toots J, Scheres SH, Ramakrishnan V. 32.  2015. The structure of the human mitochondrial ribosome. Science 348:95–98 [Google Scholar]
  33. Greber BJ, Bieri P, Leibundgut M, Leitner A, Aebersold R. 33.  et al. 2015. Ribosome. The complete structure of the 55S mammalian mitochondrial ribosome. Science 348:303–8 [Google Scholar]
  34. Amunts A, Brown A, Bai XC, Llacer JL, Hussain T. 34.  et al. 2014. Structure of the yeast mitochondrial large ribosomal subunit. Science 343:1485–89 [Google Scholar]
  35. Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK. 35.  2003. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115:97–108 [Google Scholar]
  36. van der Sluis EO, Bauerschmitt H, Becker T, Mielke T, Frauenfeld J. 36.  et al. 2015. Parallel structural evolution of mitochondrial ribosomes and OXPHOS complexes. Genome Biol. Evol. 7:1235–51 [Google Scholar]
  37. Sharma MR, Booth TM, Simpson L, Maslov DA, Agrawal RK. 37.  2009. Structure of a mitochondrial ribosome with minimal RNA. PNAS 106:9637–42 [Google Scholar]
  38. Leaver CJ, Harmey MA. 38.  1976. Higher-plant mitochondrial ribosomes contain a 5S ribosomal ribonucleic acid component. Biochem. J. 157:275–77 [Google Scholar]
  39. Dontsova OA, Dinman JD. 39.  2005. 5S rRNA: structure and function from head to toe. Int. J. Biomed. Sci. 1:2–7 [Google Scholar]
  40. Yoshionari S, Koike T, Yokogawa T, Nishikawa K, Ueda T. 40.  et al. 1994. Existence of nuclear-encoded 5S-rRNA in bovine mitochondria. FEBS Lett. 338:137–42 [Google Scholar]
  41. Greber BJ, Boehringer D, Leibundgut M, Bieri P, Leitner A. 41.  et al. 2014. The complete structure of the large subunit of the mammalian mitochondrial ribosome. Nature 515:283–86 [Google Scholar]
  42. Dowton M, Cameron SL, Dowavic JI, Austin AD, Whiting MF. 42.  2009. Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Mol. Biol. Evol. 26:1607–17 [Google Scholar]
  43. Foury F, Roganti T, Lecrenier N, Purnelle B. 43.  1998. The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 440:325–31 [Google Scholar]
  44. Denslow ND, Anders JC, O'Brien TW. 44.  1991. Bovine mitochondrial ribosomes possess a high affinity binding site for guanine nucleotides. J. Biol. Chem. 266:9586–90 [Google Scholar]
  45. Zhang L, Ging NC, Komoda T, Hanada T, Suzuki T, Watanabe K. 45.  2005. Antibiotic susceptibility of mammalian mitochondrial translation. FEBS Lett. 579:6423–27 [Google Scholar]
  46. Sohmen D, Chiba S, Shimokawa-Chiba N, Innis CA, Berninghausen O. 46.  et al. 2015. Structure of the Bacillus subtilis 70S ribosome reveals the basis for species-specific stalling. Nat. Commun. 6:6941 [Google Scholar]
  47. Nilsson OB, Hedman R, Marino J, Wickles S, Bischoff L. 47.  et al. 2015. Cotranslational protein folding inside the ribosome exit tunnel. Cell Rep. 12:1533–40 [Google Scholar]
  48. Shao S, Brown A, Santhanam B, Hegde RS. 48.  2015. Structure and assembly pathway of the ribosome quality control complex. Mol. Cell 57:433–44 [Google Scholar]
  49. Ott M, Herrmann JM. 49.  2010. Co-translational membrane insertion of mitochondrially encoded proteins. Biochim. Biophys. Acta 1803:767–75 [Google Scholar]
  50. Prestele M, Vogel F, Reichert AS, Herrmann JM, Ott M. 50.  2009. Mrpl36 is important for generation of assembly competent proteins during mitochondrial translation. Mol. Biol. Cell 20:2615–25 [Google Scholar]
  51. Ott M, Prestele M, Bauerschmitt H, Funes S, Bonnefoy N, Herrmann JM. 51.  2006. Mba1, a membrane-associated ribosome receptor in mitochondria. EMBO J. 25:1603–10 [Google Scholar]
  52. Liu M, Spremulli L. 52.  2000. Interaction of mammalian mitochondrial ribosomes with the inner membrane. J. Biol. Chem. 275:29400–6 [Google Scholar]
  53. Greber BJ, Boehringer D, Leitner A, Bieri P, Voigts-Hoffmann F. 53.  et al. 2014. Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature 505:515–19 [Google Scholar]
  54. Pfeffer S, Woellhaf MW, Herrmann JM, Forster F. 54.  2015. Organization of the mitochondrial translation machinery studied in situ by cryoelectron tomography. Nat. Commun. 6:6019 [Google Scholar]
  55. Pfeffer S, Dudek J, Gogala M, Schorr S, Linxweiler J. 55.  et al. 2014. Structure of the mammalian oligosaccharyl-transferase complex in the native ER protein translocon. Nat. Commun. 5:3072 [Google Scholar]
  56. Fiori A, Mason TL, Fox TD. 56.  2003. Evidence that synthesis of the Saccharomyces cerevisiae mitochondrially encoded ribosomal protein Var1p may be membrane localized. Eukaryot. Cell 2:651–53 [Google Scholar]
  57. Jia L, Dienhart M, Schramp M, McCauley M, Hell K, Stuart RA. 57.  2003. Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal hydrophilic region of Oxa1. EMBO J. 22:6438–47 [Google Scholar]
  58. Saller MJ, Wu ZC, de Keyzer J, Driessen AJ. 58.  2012. The YidC/Oxa1/Alb3 protein family: common principles and distinct features. Biol. Chem. 393:1279–90 [Google Scholar]
  59. Funes S, Kauff F, van der Sluis EO, Ott M, Herrmann JM. 59.  2011. Evolution of YidC/Oxa1/Alb3 insertases: three independent gene duplications followed by functional specialization in bacteria, mitochondria and chloroplasts. Biol. Chem. 392:13–19 [Google Scholar]
  60. Hell K, Herrmann J, Pratje E, Neupert W, Stuart RA. 60.  1997. Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett. 418:367–70 [Google Scholar]
  61. He S, Fox TD. 61.  1997. Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p. Mol. Biol. Cell 8:1449–60 [Google Scholar]
  62. van der Laan M, Bechtluft P, Kol S, Nouwen N, Driessen AJ. 62.  2004. F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J. Cell Biol. 165:213–22 [Google Scholar]
  63. van der Laan M, Nouwen NP, Driessen AJ. 63.  2005. YidC—an evolutionary conserved device for the assembly of energy-transducing membrane protein complexes. Curr. Opin. Microbiol. 8:182–87 [Google Scholar]
  64. van der Laan M, Houben EN, Nouwen N, Luirink J, Driessen AJ. 64.  2001. Reconstitution of Sec-dependent membrane protein insertion: Nascent FtsQ interacts with YidC in a SecYEG-dependent manner. EMBO Rep. 2:519–23 [Google Scholar]
  65. Hell K, Neupert W, Stuart RA. 65.  2001. Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J. 20:1281–88 [Google Scholar]
  66. Szyrach G, Ott M, Bonnefoy N, Neupert W, Herrmann JM. 66.  2003. Ribosome binding to the Oxa1 complex facilitates cotranslational protein insertion in mitochondria. EMBO J. 22:6448–57 [Google Scholar]
  67. Saint-Georges Y, Hamel P, Lemaire C, Dujardin G. 67.  2001. Role of positively charged transmembrane segments in the insertion and assembly of mitochondrial inner-membrane proteins. PNAS 98:13814–19 [Google Scholar]
  68. Fox TD. 68.  2012. Mitochondrial protein synthesis, import, and assembly. Genetics 192:1203–34 [Google Scholar]
  69. Christian BE, Spremulli LL. 69.  2010. Preferential selection of the 5′-terminal start codon on leaderless mRNAs by mammalian mitochondrial ribosomes. J. Biol. Chem. 285:28379–86 [Google Scholar]
  70. Jones CN, Wilkinson KA, Hung KT, Weeks KM, Spremulli LL. 70.  2008. Lack of secondary structure characterizes the 5′ ends of mammalian mitochondrial mRNAs. RNA 14:862–71 [Google Scholar]
  71. Liao HX, Spremulli LL. 71.  1990. Identification and initial characterization of translational initiation factor 2 from bovine mitochondria. J. Biol. Chem. 265:13618–22 [Google Scholar]
  72. Koc EC, Spremulli LL. 72.  2002. Identification of mammalian mitochondrial translational initiation factor 3 and examination of its role in initiation complex formation with natural mRNAs. J. Biol. Chem. 277:35541–49 [Google Scholar]
  73. Cummings HS, Hershey JW. 73.  1994. Translation initiation factor IF1 is essential for cell viability in Escherichia coli. J. Bacteriol. 176:198–205 [Google Scholar]
  74. Gaur R, Grasso D, Datta PP, Krishna PD, Das G. 74.  et al. 2008. A single mammalian mitochondrial translation initiation factor functionally replaces two bacterial factors. Mol. Cell 29:180–90 [Google Scholar]
  75. Atkinson GC, Kuzmenko A, Kamenski P, Vysokikh MY, Lakunina V. 75.  et al. 2012. Evolutionary and genetic analyses of mitochondrial translation initiation factors identify the missing mitochondrial IF3 in S. cerevisiae. Nucleic Acids Res. 40:6122–34 [Google Scholar]
  76. Miller JL, Koc H, Koc EC. 76.  2008. Identification of phosphorylation sites in mammalian mitochondrial ribosomal protein DAP3. Protein Sci. 17:251–60 [Google Scholar]
  77. Williams EH, Butler CA, Bonnefoy N, Fox TD. 77.  2007. Translation initiation in Saccharomyces cerevisiae mitochondria: functional interactions among mitochondrial ribosomal protein Rsm28p, initiation factor 2, methionyl-tRNA-formyltransferase and novel protein Rmd9p. Genetics 175:1117–26 [Google Scholar]
  78. Bonnefoy N, Fox TD. 78.  2000. In vivo analysis of mutated initiation codons in the mitochondrial COX2 gene of Saccharomyces cerevisiae fused to the reporter gene ARG8m reveals lack of downstream reinitiation. Mol. Gen. Genet. 262:1036–46 [Google Scholar]
  79. Budkevich TV, Giesebrecht J, Behrmann E, Loerke J, Ramrath DJ. 79.  et al. 2014. Regulation of the mammalian elongation cycle by subunit rolling: a eukaryotic-specific ribosome rearrangement. Cell 158:121–31 [Google Scholar]
  80. Schwartzbach CJ, Spremulli LL. 80.  1989. Bovine mitochondrial protein synthesis elongation factors: identification and initial characterization of an elongation factor Tu-elongation factor Ts complex. J. Biol. Chem. 264:19125–31 [Google Scholar]
  81. Bhargava K, Templeton P, Spremulli LL. 81.  2004. Expression and characterization of isoform 1 of human mitochondrial elongation factor G. Protein Expr. Purif. 37:368–76 [Google Scholar]
  82. Coenen MJ, Antonicka H, Ugalde C, Sasarman F, Rossi R. 82.  et al. 2004. Mutant mitochondrial elongation factor G1 and combined oxidative phosphorylation deficiency. N. Engl. J. Med. 351:2080–86 [Google Scholar]
  83. Antonicka H, Sasarman F, Kennaway NG, Shoubridge EA. 83.  2006. The molecular basis for tissue specificity of the oxidative phosphorylation deficiencies in patients with mutations in the mitochondrial translation factor EFG1. Hum. Mol. Genet. 15:1835–46 [Google Scholar]
  84. Smeitink JA, Elpeleg O, Antonicka H, Diepstra H, Saada A. 84.  et al. 2006. Distinct clinical phenotypes associated with a mutation in the mitochondrial translation elongation factor EFTs. Am. J. Hum. Genet. 79:869–77 [Google Scholar]
  85. Valente L, Shigi N, Suzuki T, Zeviani M. 85.  2009. The R336Q mutation in human mitochondrial EFTu prevents the formation of an active mt-EFTu·GTP·aa-tRNA ternary complex. Biochim. Biophys. Acta 1792:791–95 [Google Scholar]
  86. Watanabe Y, Suematsu T, Ohtsuki T. 86.  2014. Losing the stem-loop structure from metazoan mitochondrial tRNAs and co-evolution of interacting factors. Front. Genet. 5:109 [Google Scholar]
  87. Eberly SL, Locklear V, Spremulli LL. 87.  1985. Bovine mitochondrial ribosomes. Elongation factor specificity. J. Biol. Chem. 260:8721–25 [Google Scholar]
  88. Jeppesen MG, Navratil T, Spremulli LL, Nyborg J. 88.  2005. Crystal structure of the bovine mitochondrial elongation factor Tu·Ts complex. J. Biol. Chem. 280:5071–81 [Google Scholar]
  89. Woriax VL, Bullard JM, Ma L, Yokogawa T, Spremulli LL. 89.  1997. Mechanistic studies of the translational elongation cycle in mammalian mitochondria. Biochim. Biophys. Acta 1352:91–101 [Google Scholar]
  90. Cai YC, Bullard JM, Thompson NL, Spremulli LL. 90.  2000. Interaction of mitochondrial elongation factor Tu with aminoacyl-tRNA and elongation factor Ts. J. Biol. Chem. 275:20308–14 [Google Scholar]
  91. Scolnick E, Tompkins R, Caskey T, Nirenberg M. 91.  1968. Release factors differing in specificity for terminator codons. PNAS 61:768–74 [Google Scholar]
  92. Fox TD. 92.  1979. Five TGA “stop” codons occur within the translated sequence of the yeast mitochondrial gene for cytochrome c oxidase subunit II. PNAS 76:6534–38 [Google Scholar]
  93. Lee CC, Timms KM, Trotman CN, Tate WP. 93.  1987. Isolation of a rat mitochondrial release factor. Accommodation of the changed genetic code for termination. J. Biol. Chem. 262:3548–52 [Google Scholar]
  94. Duarte I, Nabuurs SB, Magno R, Huynen M. 94.  2012. Evolution and diversification of the organellar release factor family. Mol. Biol. Evol. 29:3497–512 [Google Scholar]
  95. Temperley R, Richter R, Dennerlein S, Lightowlers RN, Chrzanowska-Lightowlers ZM. 95.  2010. Hungry codons promote frameshifting in human mitochondrial ribosomes. Science 327:301 [Google Scholar]
  96. Richter R, Rorbach J, Pajak A, Smith PM, Wessels HJ. 96.  et al. 2010. A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosome. EMBO J. 29:1116–25 [Google Scholar]
  97. Akabane S, Ueda T, Nierhaus KH, Takeuchi N. 97.  2014. Ribosome rescue and translation termination at non-standard stop codons by ICT1 in mammalian mitochondria. PLOS Genet. 10:e1004616 [Google Scholar]
  98. Gagnon MG, Seetharaman SV, Bulkley D, Steitz TA. 98.  2012. Structural basis for the rescue of stalled ribosomes: structure of YaeJ bound to the ribosome. Science 335:1370–72 [Google Scholar]
  99. Temperley RJ, Wydro M, Lightowlers RN, Chrzanowska-Lightowlers ZM. 99.  2010. Human mitochondrial mRNAs-like members of all families, similar but different. Biochim. Biophys. Acta 1797:1081–85 [Google Scholar]
  100. Huynen MA, Duarte I, Chrzanowska-Lightowlers ZM, Nabuurs SB. 100.  2012. Structure based hypothesis of a mitochondrial ribosome rescue mechanism. Biol. Direct. 7:14 [Google Scholar]
  101. Soleimanpour-Lichaei HR, Kühl I, Gaisne M, Passos JF, Wydro M. 101.  et al. 2007. mtRF1a is a human mitochondrial translation release factor decoding the major termination codons UAA and UAG. Mol. Cell 27:745–57 [Google Scholar]
  102. Tsuboi M, Morita H, Nozaki Y, Akama K, Ueda T. 102.  et al. 2009. EF-G2mt is an exclusive recycling factor in mammalian mitochondrial protein synthesis. Mol. Cell 35:502–10 [Google Scholar]
  103. Christian BE, Spremulli LL. 103.  2009. Evidence for an active role of IF3mt in the initiation of translation in mammalian mitochondria. Biochemistry 48:3269–78 [Google Scholar]
  104. Khalimonchuk O, Bird A, Winge DR. 104.  2007. Evidence for a pro-oxidant intermediate in the assembly of cytochrome oxidase. J. Biol. Chem. 282:17442–49 [Google Scholar]
  105. Williams CC, Jan CH, Weissman JS. 105.  2014. Targeting and plasticity of mitochondrial proteins revealed by proximity-specific ribosome profiling. Science 346:748–51 [Google Scholar]
  106. Cabral F, Schatz G. 106.  1978. Identification of cytochrome c oxidase subunits in nuclear yeast mutants lacking the functional enzyme. J. Biol. Chem. 253:4396–401 [Google Scholar]
  107. Ebner E, Mennucci L, Schatz G. 107.  1973. Mitochondrial assembly in respiration-deficient mutants of Saccharomyces cerevisiae. I. Effect of nuclear mutations on mitochondrial protein synthesis. J. Biol. Chem. 248:5360–68 [Google Scholar]
  108. Weraarpachai W, Antonicka H, Sasarman F, Seeger J, Schrank B. 108.  et al. 2009. Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat. Genet. 41:833–37 [Google Scholar]
  109. Herbert CJ, Golik P, Bonnefoy N. 109.  2013. Yeast PPR proteins, watchdogs of mitochondrial gene expression. RNA Biol. 10:1477–94 [Google Scholar]
  110. Barkan A, Small I. 110.  2014. Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65:415–42 [Google Scholar]
  111. Green-Willms NS, Fox TD, Costanzo MC. 111.  1998. Functional interactions between yeast mitochondrial ribosomes and mRNA 5′ untranslated leaders. Mol. Cell. Biol. 18:1826–34 [Google Scholar]
  112. Haffter P, McMullin TW, Fox TD. 112.  1991. Functional interactions among two yeast mitochondrial ribosomal proteins and an mRNA-specific translational activator. Genetics 127:319–26 [Google Scholar]
  113. Kehrein K, Schilling R, Möller-Hergt BV, Wurm CA, Jakobs S. 113.  et al. 2015. Organization of mitochondrial gene expression in two distinct ribosome-containing assemblies. Cell Rep. 10:843–53 [Google Scholar]
  114. Bauerschmitt H, Mick DU, Deckers M, Vollmer C, Funes S. 114.  et al. 2010. Ribosome-binding proteins Mdm38 and Mba1 display overlapping functions for regulation of mitochondrial translation. Mol. Biol. Cell 21:1937–44 [Google Scholar]
  115. Marykwas DL, Fox TD. 115.  1989. Control of the Saccharomyces cerevisiae regulatory gene PET494: transcriptional repression by glucose and translational induction by oxygen. Mol. Cell. Biol. 9:484–91 [Google Scholar]
  116. Rak M, Tzagoloff A. 116.  2009. F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase. PNAS 106:18509–14 [Google Scholar]
  117. Gruschke S, Römpler K, Hildenbeutel M, Kehrein K, Kühl I. 117.  et al. 2012. The Cbp3-Cbp6 complex coordinates cytochrome b synthesis with bc1 complex assembly in yeast mitochondria. J. Cell Biol. 199:137–50 [Google Scholar]
  118. Perez-Martinez X, Broadley SA, Fox TD. 118.  2003. Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. EMBO J. 22:5951–61 [Google Scholar]
  119. Barrientos A, Zambrano A, Tzagoloff A. 119.  2004. Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae. EMBO J. 23:3472–82 [Google Scholar]
  120. Choquet Y, Wostrikoff K, Rimbault B, Zito F, Girard-Bascou J. 120.  et al. 2001. Assembly-controlled regulation of chloroplast gene translation. Biochem. Soc. Trans. 29:421–26 [Google Scholar]
  121. Decoster E, Simon M, Hatat D, Faye G. 121.  1990. The MSS51 gene product is required for the translation of the COX1 mRNA in yeast mitochondria. Mol. Gen. Genet. 224:111–18 [Google Scholar]
  122. Roloff GA, Henry MF. 122.  2015. Mam33 promotes cytochrome c oxidase subunit I translation in Saccharomyces cerevisiae mitochondria. Mol. Biol. Cell 26:2885–94 [Google Scholar]
  123. Manthey GM, McEwen JE. 123.  1995. The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 14:4031–43 [Google Scholar]
  124. Tavares-Carreon F, Camacho-Villasana Y, Zamudio-Ochoa A, Shingu-Vazquez M, Torres-Larios A, Perez-Martinez X. 124.  2008. The pentatricopeptide repeats present in Pet309 are necessary for translation but not for stability of the mitochondrial COX1 mRNA in yeast. J. Biol. Chem. 283:1472–79 [Google Scholar]
  125. Zamudio-Ochoa A, Camacho-Villasana Y, Garcia-Guerrero AE, Perez-Martinez X. 125.  2014. The Pet309 pentatricopeptide repeat motifs mediate efficient binding to the mitochondrial COX1 transcript in yeast. RNA Biol. 11:953–67 [Google Scholar]
  126. Perez-Martinez X, Butler CA, Shingu-Vazquez M, Fox TD. 126.  2009. Dual functions of Mss51 couple synthesis of Cox1 to assembly of cytochrome c oxidase in Saccharomyces cerevisiae mitochondria. Mol. Biol. Cell 20:4371–80 [Google Scholar]
  127. Mick DU, Fox TD, Rehling P. 127.  2011. Inventory control: Cytochrome c oxidase assembly regulates mitochondrial translation. Nat. Rev. Mol. Cell Biol. 12:14–20 [Google Scholar]
  128. Mick DU, Vukotic M, Piechura H, Meyer HE, Warscheid B. 128.  et al. 2010. Coa3 and Cox14 are essential for negative feedback regulation of COX1 translation in mitochondria. J. Cell Biol. 191:141–54 [Google Scholar]
  129. Pierrel F, Bestwick ML, Cobine PA, Khalimonchuk O, Cricco JA, Winge DR. 129.  2007. Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly. EMBO J. 26:4335–46 [Google Scholar]
  130. Fontanesi F, Soto IC, Horn D, Barrientos A. 130.  2010. Mss51 and Ssc1 facilitate translational regulation of cytochrome c oxidase biogenesis. Mol. Cell. Biol. 30:245–59 [Google Scholar]
  131. Soto IC, Fontanesi F, Myers RS, Hamel P, Barrientos A. 131.  2012. A heme-sensing mechanism in the translational regulation of mitochondrial cytochrome c oxidase biogenesis. Cell Metab. 16:801–13 [Google Scholar]
  132. Ruzzenente B, Metodiev MD, Wredenberg A, Bratic A, Park CB. 132.  et al. 2012. LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J. 31:443–56 [Google Scholar]
  133. Sasarman F, Brunel-Guitton C, Antonicka H, Wai T, Shoubridge EA. 133.  2010. LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol. Biol. Cell 21:1315–23 [Google Scholar]
  134. Mick DU, Dennerlein S, Wiese H, Reinhold R, Pacheu-Grau D. 134.  et al. 2012. MITRAC links mitochondrial protein translocation to respiratory-chain assembly and translational regulation. Cell 151:1528–41 [Google Scholar]
  135. Weraarpachai W, Sasarman F, Nishimura T, Antonicka H, Aure K. 135.  et al. 2012. Mutations in C12orf62, a factor that couples COX I synthesis with cytochrome c oxidase assembly, cause fatal neonatal lactic acidosis. Am. J. Hum. Genet. 90:142–51 [Google Scholar]
  136. Bourens M, Boulet A, Leary SC, Barrientos A. 136.  2014. Human COX20 cooperates with SCO1 and SCO2 to mature COX2 and promote the assembly of cytochrome c oxidase. Hum. Mol. Genet. 23:2901–13 [Google Scholar]
  137. Dieckmann CL, Staples RR. 137.  1994. Regulation of mitochondrial gene expression in Saccharomyces cerevisiae. Int. Rev. Cytol. 152:145–81 [Google Scholar]
  138. Chen W, Dieckmann CL. 138.  1994. Cbp1p is required for message stability following 5′-processing of COB mRNA. J. Biol. Chem. 269:16574–78 [Google Scholar]
  139. Mittelmeier TM, Dieckmann CL. 139.  1993. In vivo analysis of sequences necessary for CBP1-dependent accumulation of cytochrome b transcripts in yeast mitochondria. Mol. Cell. Biol. 13:4203–13 [Google Scholar]
  140. Rödel G. 140.  1986. Two yeast nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5′-untranslated COB leader. Curr. Genet. 11:41–45 [Google Scholar]
  141. Gruschke S, Kehrein K, Römpler K, Gröne K, Israel L. 141.  et al. 2011. Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J. Cell Biol. 193:1101–14 [Google Scholar]
  142. Hildenbeutel M, Hegg EL, Stephan K, Gruschke S, Meunier B, Ott M. 142.  2014. Assembly factors monitor sequential hemylation of cytochrome b to regulate mitochondrial translation. J. Cell Biol. 205:511–24 [Google Scholar]
  143. Tucker EJ, Wanschers BF, Szklarczyk R, Mountford HS, Wijeyeratne XW. 143.  et al. 2013. Mutations in the UQCC1-interacting protein, UQCC2, cause human complex III deficiency associated with perturbed cytochrome b protein expression. PLOS Genet. 9:e1004034 [Google Scholar]
  144. Antonicka H, Sasarman F, Nishimura T, Paupe V, Shoubridge EA. 144.  2013. The mitochondrial RNA-binding protein GRSF1 localizes to RNA granules and is required for posttranscriptional mitochondrial gene expression. Cell Metab. 17:386–98 [Google Scholar]
  145. Jourdain AA, Koppen M, Wydro M, Rodley CD, Lightowlers RN. 145.  et al. 2013. GRSF1 regulates RNA processing in mitochondrial RNA granules. Cell Metab. 17:399–410 [Google Scholar]
  146. Brandt F, Carlson LA, Hartl FU, Baumeister W, Grunewald K. 146.  2010. The three-dimensional organization of polyribosomes in intact human cells. Mol. Cell 39:560–69 [Google Scholar]
  147. McMullin TW, Fox TD. 147.  1993. COX3 mRNA-specific translational activator proteins are associated with the inner mitochondrial membrane in Saccharomyces cerevisiae. J. Biol. Chem. 268:11737–41 [Google Scholar]
  148. Gruschke S, Ott M. 148.  2010. The polypeptide tunnel exit of the mitochondrial ribosome is tailored to meet the specific requirements of the organelle. BioEssays 32:1050–57 [Google Scholar]
  149. Sanchirico ME, Fox TD, Mason TL. 149.  1998. Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs. EMBO J. 17:5796–804 [Google Scholar]
  150. Naithani S, Saracco SA, Butler CA, Fox TD. 150.  2003. Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol. Biol. Cell 14:324–33 [Google Scholar]
  151. Carignani G, Groudinsky O, Frezza D, Schiavon E, Bergantino E, Slonimski PP. 151.  1983. An mRNA maturase is encoded by the first intron of the mitochondrial gene for the subunit I of cytochrome oxidase in S. cerevisiae. Cell 35:733–42 [Google Scholar]
  152. Zhang X, Zuo X, Yang B, Li Z, Xue Y. 152.  et al. 2014. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 158:607–19 [Google Scholar]
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