1932

Abstract

Together, the nuclear and mitochondrial genomes encode the oxidative phosphorylation (OXPHOS) complexes that reside in the mitochondrial inner membrane and enable aerobic life. Mitochondria maintain their own genome that is expressed and regulated by factors distinct from their nuclear counterparts. For optimal function, the cell must ensure proper stoichiometric production of OXPHOS subunits by coordinating two physically separated and evolutionarily distinct gene expression systems. Here, we review our current understanding of mitonuclear coregulation primarily at the levels of transcription and translation. Additionally, we discuss other levels of coregulation that may exist but remain largely unexplored, including mRNA modification and stability and posttranslational protein degradation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120417-031709
2018-11-23
2024-06-22
Loading full text...

Full text loading...

/deliver/fulltext/genet/52/1/annurev-genet-120417-031709.html?itemId=/content/journals/10.1146/annurev-genet-120417-031709&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Adams K 2003. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol. Phylogenet. Evol. 29:3380–95
    [Google Scholar]
  2. 2.  Allen JF 2015. Why chloroplasts and mitochondria retain their own genomes and genetic systems: colocation for redox regulation of gene expression. PNAS 112:3310231–38
    [Google Scholar]
  3. 3.  Amiott EA, Jaehning JA 2006. Mitochondrial transcription is regulated via an ATP “sensing” mechanism that couples RNA abundance to respiration. Mol. Cell 22:3329–38
    [Google Scholar]
  4. 4.  Amuthan G, Biswas G, Ananadatheerthavarada HK, Vijayasarathy C, Shephard HM, Avadhani NG 2002. Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells. Oncogene 21:517839–49
    [Google Scholar]
  5. 5.  Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR et al. 1981. Sequence and organization of the human mitochondrial genome. Nature 290:5806457–65
    [Google Scholar]
  6. 6.  Arnould T, Vankoningsloo S, Renard P, Houbion A, Ninane N et al. 2002. CREB activation induced by mitochondrial dysfunction is a new signaling pathway that impairs cell proliferation. EMBO J 21:1–253–63
    [Google Scholar]
  7. 7.  Baker MJ, Tatsuta T, Langer T 2011. Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol. 3:7a007559
    [Google Scholar]
  8. 8.  Barrell BG, Bankier AT, Drouin J 1979. A different genetic code in human mitochondria. Nature 282:5735189–94
    [Google Scholar]
  9. 9.  Barrientos A, Korr D, Tzagoloff A 2002. Shy1p is necessary for full expression of mitochondrial COX1 in the yeast model of Leigh's syndrome. EMBO J 21:1–243–52
    [Google Scholar]
  10. 10.  Barrientos A, Zambrano A, Tzagoloff A 2004. Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae. EMBO J 23:173472–82
    [Google Scholar]
  11. 11.  Baughman JM, Nilsson R, Gohil VM, Arlow DH, Gauhar Z, Mootha VK 2009. A computational screen for regulators of oxidative phosphorylation implicates SLIRP in mitochondrial RNA homeostasis. PLOS Genet 5:8e1000590
    [Google Scholar]
  12. 12.  Blesa JR, Prieto-Ruiz JA, Abraham BA, Harrison BL, Hegde AA, Hernández-Yago J 2008. NRF-1 is the major transcription factor regulating the expression of the human TOMM34 gene. Biochem. Cell Biol. 86:146–56
    [Google Scholar]
  13. 13.  Blumberg A, Rice EJ, Kundaje A, Danko CG, Mishmar D 2017. Initiation of mtDNA transcription is followed by pausing, and diverges across human cell types and during evolution. Genome Res 27:3362–73
    [Google Scholar]
  14. 14.  Blumberg A, Sri Sailaja B, Kundaje A, Levin L, Dadon S et al. 2014. Transcription factors bind negatively selected sites within human mtDNA genes. Genome Biol. Evol. 6:102634–46
    [Google Scholar]
  15. 15.  Bogenhagen DF, Ostermeyer-Fay AG, Haley JD, Garcia-Diaz M 2018. Kinetics and mechanism of mammalian mitochondrial ribosome assembly. Cell Rep 22:71935–44
    [Google Scholar]
  16. 16.  Bonitz SG, Berlani R, Coruzzi G, Li M, Macino G et al. 1980. Codon recognition rules in yeast mitochondria. PNAS 77:63167–70
    [Google Scholar]
  17. 17.  Bonnefoy N, Bsat N, Fox TD 2001. Mitochondrial translation of Saccharomyces cerevisiae COX2 mRNA is controlled by the nucleotide sequence specifying the pre-Cox2p leader peptide. Mol. Cell. Biol. 21:72359–72
    [Google Scholar]
  18. 18.  Borowski LS, Dziembowski A, Hejnowicz MS, Stepien PP, Szczesny RJ 2013. Human mitochondrial RNA decay mediated by PNPase–hSuv3 complex takes place in distinct foci. Nucleic Acids Res 41:21223–40
    [Google Scholar]
  19. 19.  Burger G, Gray MW, Lang BF 2003. Mitochondrial genomes: anything goes. Trends Genet 19:12709–16
    [Google Scholar]
  20. 20.  Cammarota M, Paratcha G, Bevilaqua LR, Levi de Stein M, Lopez M et al. 1999. Cyclic AMP-responsive element binding protein in brain mitochondria. J. Neurochem. 72:62272–77
    [Google Scholar]
  21. 21.  Casas F, Rochard P, Rodier A, Cassar-Malek I, Marchal-Victorion S et al. 1999. A variant form of the nuclear triiodothyronine receptor c-ErbAα1 plays a direct role in regulation of mitochondrial RNA synthesis. Mol. Cell. Biol. 19:127913–24
    [Google Scholar]
  22. 22.  Chatterjee A, Seyfferth J, Lucci J, Gilsbach R, Preissl S et al. 2016. MOF acetyl transferase regulates transcription and respiration in mitochondria. Cell 167:3722–38.e23
    [Google Scholar]
  23. 23.  Chen JQ, Delannoy M, Cooke C, Yager JD 2004. Mitochondrial localization of ERα and ERβ in human MCF7 cells. Am. J. Physiol. Endocrinol. Metab. 286:6E1011–22
    [Google Scholar]
  24. 24.  Chen JQ, Eshete M, Alworth WL, Yager JD 2004. Binding of MCF-7 cell mitochondrial proteins and recombinant human estrogen receptors α and β to human mitochondrial DNA estrogen response elements. J. Cell. Biochem. 93:2358–73
    [Google Scholar]
  25. 25.  Chujo T, Ohira T, Sakaguchi Y, Goshima N, Nomura N et al. 2012. LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria. Nucleic Acids Res 40:168033–47
    [Google Scholar]
  26. 26.  Claros MG, Perea J, Shu Y, Samatey FA, Popot J-L, Jacq C 1995. Limitations to in vivo import of hydrophobic proteins into yeast mitochondria. Eur. J. Biochem. 228:3762–71
    [Google Scholar]
  27. 27.  Cogswell PC, Kashatus DF, Keifer JA, Guttridge DC, Reuther JY et al. 2003. NF-κB and IκBα are found in the mitochondria. Evidence for regulation of mitochondrial gene expression by NF-κB. J. Biol. Chem. 278:52963–68
    [Google Scholar]
  28. 28.  Costanzo MC, Fox TD 1990. Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu. Rev. Genet. 24:91–113
    [Google Scholar]
  29. 29.  Costanzo MC, Fox TD 1993. Suppression of a defect in the 5′ untranslated leader of mitochondrial COX3 mRNA by a mutation affecting an mRNA-specific translational activator protein. Mol. Cell. Biol. 13:84806–13
    [Google Scholar]
  30. 30.  Costanzo MC, Seaver EC, Fox TD 1986. At least two nuclear gene products are specifically required for translation of a single yeast mitochondrial mRNA. EMBO J 5:133637–41
    [Google Scholar]
  31. 31.  Couvillion MT, Soto IC, Shipkovenska G, Churchman LS 2016. Synchronized mitochondrial and cytosolic translation programs. Nature 533:7604499–503
    [Google Scholar]
  32. 32.  De Rasmo D, Signorile A, Roca E, Papa S 2009. cAMP response element-binding protein (CREB) is imported into mitochondria and promotes protein synthesis. FEBS J 276:164325–33
    [Google Scholar]
  33. 33.  DeRisi JL, Iyer VR, Brown PO 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278:5338680–86
    [Google Scholar]
  34. 34.  Deshpande AP, Patel SS 2012. Mechanism of transcription initiation by the yeast mitochondrial RNA polymerase. Biochim. Biophys. Acta 1819:9–10930–38
    [Google Scholar]
  35. 35.  Dhar SS, Ongwijitwat S, Wong-Riley MTT 2008. Nuclear respiratory factor 1 regulates all ten nuclear-encoded subunits of cytochrome c oxidase in neurons. J. Biol. Chem. 283:63120–29
    [Google Scholar]
  36. 36.  Duborjal H, Beugnot R, Mousson de Camaret B, Issartel J-P 2002. Large functional range of steady-state levels of nuclear and mitochondrial transcripts coding for the subunits of the human mitochondrial OXPHOS system. Genome Res. 12:121901–9
    [Google Scholar]
  37. 37.  Dunstan HM, Green-Willms NS, Fox TD 1997. In vivo analysis of Saccharomyces cerevisiae COX2 mRNA 5′-untranslated leader functions in mitochondrial translation initiation and translational activation. Genetics 147:187–100
    [Google Scholar]
  38. 38.  Ebner E, Mennucci L, Schatz G 1973. Mitochondrial assembly in respiration-deficient mutants of Saccharomyces cerevisiae. I. Effect of nuclear mutations on mitochondrial protein synthesis. J. Biol. Chem. 248:155360–68
    [Google Scholar]
  39. 39.  Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M et al. 2004. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 13:9935–44
    [Google Scholar]
  40. 40.  Emdadul Haque M, Grasso D, Miller C, Spremulli LL, Saada A 2008. The effect of mutated mitochondrial ribosomal proteins S16 and S22 on the assembly of the small and large ribosomal subunits in human mitochondria. Mitochondrion 8:3254–61
    [Google Scholar]
  41. 41.  Enríquez JA, Fernández-Silva P, Garrido-Pérez N, López-Pérez MJ, Pérez-Martos A, Montoya J 1999. Direct regulation of mitochondrial RNA synthesis by thyroid hormone. Mol. Cell. Biol. 19:1657–70
    [Google Scholar]
  42. 42.  Faye G, Sor F 1977. Analysis of mitochondrial ribosomal proteins of Saccharomyces cerevisiae by two dimensional polyacrylamide gel electrophoresis. Mol. Gen. Genet. 155:127–34
    [Google Scholar]
  43. 43.  Fernández-Vizarra E, Enriquez JA, Pérez-Martos A, Montoya J, Fernández-Silva P 2008. Mitochondrial gene expression is regulated at multiple levels and differentially in the heart and liver by thyroid hormones. Curr. Genet. 54:113–22
    [Google Scholar]
  44. 44.  Finley LWS, Haigis MC 2009. The coordination of nuclear and mitochondrial communication during aging and calorie restriction. Ageing Res. Rev. 8:3173–88
    [Google Scholar]
  45. 45.  Foury F, Roganti T, Lecrenier N, Purnelle B 1998. The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett 440:3325–31
    [Google Scholar]
  46. 46.  Fox TD 2012. Mitochondrial protein synthesis, import, and assembly. Genetics 192:41203–34
    [Google Scholar]
  47. 47.  Frechin M, Enkler L, Tetaud E, Laporte D, Senger B et al. 2014. Expression of nuclear and mitochondrial genes encoding ATP synthase is synchronized by disassembly of a multisynthetase complex. Mol. Cell 56:6763–76
    [Google Scholar]
  48. 48.  Frechin M, Senger B, Brayé M, Kern D, Martin RP, Becker HD 2009. Yeast mitochondrial Gln-tRNAGln is generated by a GatFAB-mediated transamidation pathway involving Arc1p-controlled subcellular sorting of cytosolic GluRS. Genes Dev 23:91119–30
    [Google Scholar]
  49. 49.  Freyer C, Park CB, Ekstrand MI, Shi Y, Khvorostova J et al. 2010. Maintenance of respiratory chain function in mouse hearts with severely impaired mtDNA transcription. Nucleic Acids Res 38:196577–88
    [Google Scholar]
  50. 50.  Gao Y, Bai X, Zhang D, Han C, Yuan J et al. 2016. Mammalian elongation factor 4 regulates mitochondrial translation essential for spermatogenesis. Nat. Struct. Mol. Biol. 23:5441–49
    [Google Scholar]
  51. 51.  Gardner MJ, Hall N, Fung E, White O, Berriman M et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:6906498–511
    [Google Scholar]
  52. 52.  Gelfand R, Attardi G 1981. Synthesis and turnover of mitochondrial ribonucleic acid in HeLa cells: the mature ribosomal and messenger ribonucleic acid species are metabolically unstable. Mol. Cell. Biol. 1:6497–511
    [Google Scholar]
  53. 53.  Gilbert WV, Bell TA, Schaening C 2016. Messenger RNA modifications: form, distribution, and function. Science 352:62921408–12
    [Google Scholar]
  54. 54.  Gleyzer N, Vercauteren K, Scarpulla RC 2005. Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol. Cell. Biol. 25:41354–66
    [Google Scholar]
  55. 55.  Goldberg AL 2003. Protein degradation and protection against misfolded or damaged proteins. Nature 426:895–99
    [Google Scholar]
  56. 56.  Gomes AP, Price NL, Ling AJY, Moslehi JJ, Montgomery MK et al. 2013. Declining NAD+ induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155:71624–38
    [Google Scholar]
  57. 57.  Gray MW 2012. Mitochondrial evolution. Cold Spring Harb. Perspect. Biol. 4:9a011403
    [Google Scholar]
  58. 58.  Green-Willms NS, Butler CA, Dunstan HM, Fox TD 2001. Pet111p, an inner membrane-bound translational activator that limits expression of the Saccharomyces cerevisiae mitochondrial gene COX2. J. Biol. Chem. 276:96392–97
    [Google Scholar]
  59. 59.  Grohmann K, Amairic F, Crews S, Attardi G 1978. Failure to detect “cap” structures in mitochondrial DNA-coded poly(A)-containing RNA from HeLa cells. Nucleic Acids Res 5:3637–51
    [Google Scholar]
  60. 60.  Guseva NV, Taghiyev AF, Sturm MT, Rokhlin OW, Cohen MB 2004. Tumor necrosis factor–related apoptosis-inducing ligand–mediated activation of mitochondria-associated nuclear factor-κB in prostatic carcinoma cell lines. Mol. Cancer Res. 2:10574–84
    [Google Scholar]
  61. 61.  Hazkani-Covo E, Sorek R, Graur D 2003. Evolutionary dynamics of large numts in the human genome: rarity of independent insertions and abundance of post-insertion duplications. J. Mol. Evol. 56:169–74
    [Google Scholar]
  62. 62.  Hell K, Neupert W, Stuart RA 2001. Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J 20:61281–88
    [Google Scholar]
  63. 63.  Herrmann JM, Woellhaf MW, Bonnefoy N 2013. Control of protein synthesis in yeast mitochondria: the concept of translational activators. Biochim. Biophys. Acta 1833:2286–94
    [Google Scholar]
  64. 64.  Hibbs MA, Hess DC, Myers CL, Huttenhower C, Li K, Troyanskaya OG 2007. Exploring the functional landscape of gene expression: directed search of large microarray compendia. Bioinformatics 23:202692–99
    [Google Scholar]
  65. 65.  Hornig-Do H-T, Tatsuta T, Buckermann A, Bust M, Kollberg G et al. 2012. Nonsense mutations in the COX1 subunit impair the stability of respiratory chain complexes rather than their assembly. EMBO J 31:51293–307
    [Google Scholar]
  66. 66.  Houtkooper RH, Mouchiroud L, Ryu D, Moullan N, Katsyuba E et al. 2013. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497:7450451–57
    [Google Scholar]
  67. 67.  Huttenhower C, Haley EM, Hibbs MA, Dumeaux V, Barrett DR et al. 2009. Exploring the human genome with functional maps. Genome Res 19:61093–106
    [Google Scholar]
  68. 68.  Ikeda M, Ide T, Fujino T, Arai S, Saku K et al. 2015. Overexpression of TFAM or twinkle increases mtDNA copy number and facilitates cardioprotection associated with limited mitochondrial oxidative stress. PLOS ONE 10:3e0119687
    [Google Scholar]
  69. 69.  Jazwinski SM 2013. The retrograde response: when mitochondrial quality control is not enough. Biochim. Biophys. Acta 1833:2400–9
    [Google Scholar]
  70. 70.  Jiao X, Doamekpor SK, Bird JG, Nickels BE, Tong L et al. 2017. 5′ end nicotinamide adenine dinucleotide cap in human cells promotes RNA decay through DXO-mediated deNADding. Cell 168:61015–27.e10
    [Google Scholar]
  71. 71.  Johnson RF, Witzel I-I, Perkins ND 2011. p53-dependent regulation of mitochondrial energy production by the RelA subunit of NF-κB. Cancer Res 71:165588–97
    [Google Scholar]
  72. 72.  Juszkiewicz S, Hedge RS 2018. Quality control of orphaned proteins. Mol. Cell 71:3443–57
    [Google Scholar]
  73. 73.  Kamenski P, Kolesnikova O, Jubenot V, Entelis N, Krasheninnikov IA et al. 2007. Evidence for an adaptation mechanism of mitochondrial translation via tRNA import from the cytosol. Mol. Cell 26:5625–37
    [Google Scholar]
  74. 74.  Kamenski P, Smirnova E, Kolesnikova O, Krasheninnikov IA, Martin RP et al. 2010. tRNA mitochondrial import in yeast: mapping of the import determinants in the carrier protein, the precursor of mitochondrial lysyl-tRNA synthetase. Mitochondrion 10:3284–93
    [Google Scholar]
  75. 75.  Kaufman BA, Durisic N, Mativetsky JM, Costantino S, Hancock MA et al. 2007. The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Mol. Biol. Cell 18:93225–36
    [Google Scholar]
  76. 76.  Kelly JL, Lehman IR 1986. Yeast mitochondrial RNA polymerase. Purification and properties of the catalytic subunit. J. Biol. Chem. 261:2210340–47
    [Google Scholar]
  77. 77.  Khalimonchuk O, Bestwick M, Meunier B, Watts TC, Winge DR 2010. Formation of the redox cofactor centers during Cox1 maturation in yeast cytochrome oxidase. Mol. Cell. Biol. 30:41004–17
    [Google Scholar]
  78. 78.  Khalimonchuk O, Bird A, Winge DR 2007. Evidence for a pro-oxidant intermediate in the assembly of cytochrome oxidase. J. Biol. Chem. 282:2417442–49
    [Google Scholar]
  79. 79.  Kolesnikova OA, Entelis NS, Mireau H, Fox TD, Martin RP, Tarassov IA 2000. Suppression of mutations in mitochondrial DNA by tRNAs imported from the cytoplasm. Science 289:54861931–33
    [Google Scholar]
  80. 80.  Koufali M-M, Moutsatsou P, Sekeris CE, Breen KC 2003. The dynamic localization of the glucocorticoid receptor in rat C6 glioma cell mitochondria. Mol. Cell. Endocrinol. 209:1–251–60
    [Google Scholar]
  81. 81.  Krause K, Dieckmann CL 2004. Analysis of transcription asymmetries along the tRNAE-COB operon: evidence for transcription attenuation and rapid RNA degradation between coding sequences. Nucleic Acids Res 32:216276–83
    [Google Scholar]
  82. 82.  Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K et al. 2005. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309:5733481–84
    [Google Scholar]
  83. 83.  Kukat C, Larsson N-G 2013. mtDNA makes a U-turn for the mitochondrial nucleoid. Trends Cell Biol. 23:9457–63
    [Google Scholar]
  84. 84.  Lagouge M, Mourier A, Lee HJ, Spåhr H, Wai T et al. 2015. SLIRP regulates the rate of mitochondrial protein synthesis and protects LRPPRC from degradation. PLOS Genet 11:8e1005423
    [Google Scholar]
  85. 85.  Lake NJ, Webb BD, Stroud DA, Richman TR, Ruzzenente B et al. 2017. Biallelic mutations in MRPS34 lead to instability of the small mitoribosomal subunit and Leigh syndrome. Am. J. Hum. Genet. 101:2239–54
    [Google Scholar]
  86. 86.  Lam YW, Lamond AI, Mann M, Andersen JS 2007. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 17:9749–60
    [Google Scholar]
  87. 87.  Lee HK, Hsu AK, Sajdak J, Qin J, Pavlidis P 2004. Coexpression analysis of human genes across many microarray data sets. Genome Res 14:61085–94
    [Google Scholar]
  88. 88.  Lee J, Kim C-H, Simon DK, Aminova LR, Andreyev AY et al. 2005. Mitochondrial cyclic AMP response element-binding protein (CREB) mediates mitochondrial gene expression and neuronal survival. J. Biol. Chem. 280:4940398–401
    [Google Scholar]
  89. 89.  Li G-W, Burkhardt D, Gross C, Weissman JS 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:3624–35
    [Google Scholar]
  90. 90.  Liao X, Butow RA 1993. RTG1 and RTG2: two yeast genes required for a novel path of communication from mitochondria to the nucleus. Cell 72:61–71
    [Google Scholar]
  91. 91.  Liu Z, Sekito T, Epstein CB, Butow RA 2001. RTG-dependent mitochondria to nucleus signaling is negatively regulated by the seven WD-repeat protein Lst8p. EMBO J 20:247209–19
    [Google Scholar]
  92. 92.  Liu Z, Sekito T, Spírek M, Thornton J, Butow RA 2003. Retrograde signaling is regulated by the dynamic interaction between Rtg2p and Mks1p. Mol. Cell 12:2401–11
    [Google Scholar]
  93. 93.  Luo Y, Bond JD, Ingram VM 1997. Compromised mitochondrial function leads to increased cytosolic calcium and to activation of MAP kinases. PNAS 94:189705–10
    [Google Scholar]
  94. 94.  Maleszka R, Skelly PJ, Clark-Walker GD 1991. Rolling circle replication of DNA in yeast mitochondria. EMBO J 10:123923–29
    [Google Scholar]
  95. 95.  Marinov GK, Wang YE, Chan D, Wold BJ 2014. Evidence for site-specific occupancy of the mitochondrial genome by nuclear transcription factors. PLOS ONE 9:1e84713
    [Google Scholar]
  96. 96.  Marsh JA, Hernández H, Hall Z, Ahnert SE, Perica T et al. 2013. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 153:2461–70
    [Google Scholar]
  97. 97.  Marykwas DL, Fox TD 1989. Control of the Saccharomyces cerevisiae regulatory gene PET494: transcriptional repression by glucose and translational induction by oxygen. Mol. Cell. Biol. 9:2484–91
    [Google Scholar]
  98. 98.  Masters BS, Stohl LL, Clayton DA 1987. Yeast mitochondrial RNA polymerase is homologous to those encoded by bacteriophages T3 and T7. Cell 51:189–99
    [Google Scholar]
  99. 99.  Matalon O, Horovitz A, Levy ED 2014. Different subunits belonging to the same protein complex often exhibit discordant expression levels and evolutionary properties. Curr. Opin. Struct. Biol. 26:113–20
    [Google Scholar]
  100. 100.  Matsushima Y, Goto Y-I, Kaguni LS 2010. Mitochondrial Lon protease regulates mitochondrial DNA copy number and transcription by selective degradation of mitochondrial transcription factor A (TFAM). PNAS 107:4318410–15
    [Google Scholar]
  101. 101.  McShane E, Sin C, Zauber H, Wells JN, Donnelly N et al. 2016. Kinetic analysis of protein stability reveals age-dependent degradation. Cell 167:3803–15.e21
    [Google Scholar]
  102. 102.  Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA et al. 2011. The human mitochondrial transcriptome. Cell 146:4645–58
    [Google Scholar]
  103. 103.  Mick DU, Wagner K, van der Laan M, Frazier AE, Perschil I et al. 2007. Shy1 couples Cox1 translational regulation to cytochrome c oxidase assembly. EMBO J 26:204347–58
    [Google Scholar]
  104. 104.  Minami Y, Weissman AM, Samelson LE, Klausner RD 1987. Building a multichain receptor: synthesis, degradation, and assembly of the T-cell antigen receptor. PNAS 84:92688–92
    [Google Scholar]
  105. 105.  Montoya J, Ojala D, Attardi G Distinctive features of the 5′-terminal sequences of the human mitochondrial mRNAs. Nature 290:465–70
    [Google Scholar]
  106. 106.  Mootha VK, Bunkenborg J, Olsen JV, Hjerrild M, Wisniewski JR et al. 2003. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115:5629–40
    [Google Scholar]
  107. 107.  Mootha VK, Lepage P, Miller K, Bunkenborg J, Reich M et al. 2003. Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. PNAS 100:2605–10
    [Google Scholar]
  108. 108.  Moyer AL, Wagner KR 2015. Mammalian Mss51 is a skeletal muscle-specific gene modulating cellular metabolism. J. Neuromuscul. Dis. 2:4371–85
    [Google Scholar]
  109. 109.  Münch C, Harper JW 2016. Mitochondrial unfolded protein response controls matrix pre-RNA processing and translation. Nature 534:7609710–13
    [Google Scholar]
  110. 110.  Nagaike T, Suzuki T, Katoh T, Ueda T 2005. Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochondria-specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem. 280:2019721–27
    [Google Scholar]
  111. 111.  Nakai T, Yasuhara T, Fujiki Y, Ohashi A 1995. Multiple genes, including a member of the AAA family, are essential for degradation of unassembled subunit 2 of cytochrome c oxidase in yeast mitochondria. Mol. Cell. Biol. 15:84441–52
    [Google Scholar]
  112. 112.  Nargund AM, Fiorese CJ, Pellegrino MW, Deng P, Haynes CM 2015. Mitochondrial and nuclear accumulation of the transcription factor ATFS-1 promotes OXPHOS recovery during the UPRmt. Mol. Cell 58:1123–33
    [Google Scholar]
  113. 113.  Nunnari J, Suomalainen A 2012. Mitochondria: in sickness and in health. Cell 148:61145–59
    [Google Scholar]
  114. 114.  Ojala D, Montoya J, Attardi G 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470
    [Google Scholar]
  115. 115.  Pearce DA, Sherman F 1995. Degradation of cytochrome oxidase subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1. J. Biol. Chem. 270:3620879–82
    [Google Scholar]
  116. 116.  Perez-Martinez X, Broadley SA, Fox TD 2003. Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. EMBO J 22:215951–61
    [Google Scholar]
  117. 117.  Pesole G, Allen JF, Lane N, Martin W, Rand DM et al. 2012. The neglected genome. EMBO Rep 13:6473–74
    [Google Scholar]
  118. 118.  Pláteník J, Balcar VJ, Yoneda Y, Mioduszewska B, Buchal R et al. 2005. Apparent presence of Ser133-phosphorylated cyclic AMP response element binding protein (pCREB) in brain mitochondria is due to cross-reactivity of pCREB antibodies with pyruvate dehydrogenase. J. Neurochem. 95:51446–60
    [Google Scholar]
  119. 119.  Popot JL, de Vitry C 1990. On the microassembly of integral membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 19:369–403
    [Google Scholar]
  120. 120.  Quirós PM, Mottis A, Auwerx J 2016. Mitonuclear communication in homeostasis and stress. Nat. Rev. Mol. Cell Biol. 17:4213–26
    [Google Scholar]
  121. 121.  Rak M, McStay GP, Fujikawa M, Yoshida M, Manfredi G, Tzagoloff A 2011. Turnover of ATP synthase subunits in F1-depleted HeLa and yeast cells. FEBS Lett 585:162582–86
    [Google Scholar]
  122. 122.  Rak M, Su CH, Xu JT, Azpiroz R, Singh AM, Tzagoloff A 2016. Regulation of mitochondrial translation of the ATP8/ATP6 mRNA by Smt1p. Mol. Biol. Cell 27:6919–29
    [Google Scholar]
  123. 123.  Richman TR, Ermer JA, Davies SMK, Perks KL, Viola HM et al. 2015. Mutation in MRPS34 compromises protein synthesis and causes mitochondrial dysfunction. PLOS Genet 11:3e1005089
    [Google Scholar]
  124. 124.  Richter U, Lahtinen T, Marttinen P, Suomi F, Battersby BJ 2015. Quality control of mitochondrial protein synthesis is required for membrane integrity and cell fitness. J. Cell Biol. 211:2373–89
    [Google Scholar]
  125. 125.  Richter-Dennerlein R, Oeljeklaus S, Lorenzi I, Ronsör C, Bareth B et al. 2016. Mitochondrial protein synthesis adapts to influx of nuclear-encoded protein. Cell 167:2471–83.e10
    [Google Scholar]
  126. 126.  Rinehart J, Krett B, Rubio MAT, Alfonzo JD, Söll D 2005. Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev 19:5583–92
    [Google Scholar]
  127. 127.  Rooijers K, Loayza-Puch F, Nijtmans LG, Agami R 2013. Ribosome profiling reveals features of normal and disease-associated mitochondrial translation. Nat. Commun. 4:2886
    [Google Scholar]
  128. 128.  Ruan L, Zhou C, Jin E, Kucharavy A, Zhang Y et al. 2017. Cytosolic proteostasis through importing of misfolded proteins into mitochondria. Nature 543:7645443–46
    [Google Scholar]
  129. 129.  Rubio MAT, Rinehart JJ, Krett B, Duvezin-Caubet S, Reichert AS et al. 2008. Mammalian mitochondria have the innate ability to import tRNAs by a mechanism distinct from protein import. PNAS 105:279186–91
    [Google Scholar]
  130. 130.  Ryan MT, Hoogenraad NJ 2007. Mitochondrial-nuclear communications. Annu. Rev. Biochem. 76:701–22
    [Google Scholar]
  131. 131.  Safra M, Sas-Chen A, Nir R, Winkler R, Nachshon A et al. 2017. The m1A landscape on cytosolic and mitochondrial mRNA at single-base resolution. Nature 551:251–55
    [Google Scholar]
  132. 132.  Sasarman F, Brunel-Guitton C, Antonicka H, Wai T, Shoubridge EA et al. 2010. LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol. Biol. Cell 21:81315–23
    [Google Scholar]
  133. 133.  Schieber M, Chandel NS 2014. ROS function in redox signaling and oxidative stress. Curr. Biol. 24:10R453–62
    [Google Scholar]
  134. 134.  Schneider A 2011. Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu. Rev. Biochem. 80:1033–53
    [Google Scholar]
  135. 135.  Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J et al. 2011. Global quantification of mammalian gene expression control. Nature 473:7347337–42
    [Google Scholar]
  136. 136.  Shadel GS, Horvath TL 2015. Mitochondrial ROS signaling in organismal homeostasis. Cell 163:3560–69
    [Google Scholar]
  137. 137.  Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK 2003. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115:197–108
    [Google Scholar]
  138. 138.  She H, Yang Q, Shepherd K, Smith Y, Miller G et al. 2011. Direct regulation of complex I by mitochondrial MEF2D is disrupted in a mouse model of Parkinson disease and in human patients. J. Clin. Investig. 121:3930–40
    [Google Scholar]
  139. 139.  Shemorry A, Hwang C-S, Varshavsky A 2013. Control of protein quality and stoichiometries by N-terminal acetylation and the N-end rule pathway. Mol. Cell 50:4540–51
    [Google Scholar]
  140. 140.  Shingu-Vazquez M, Camacho-Villasana Y, Sandoval-Romero L, Butler CA, Fox TD, Perez-Martinez X 2010. The carboxyl-terminal end of Cox1 is required for feedback assembly regulation of Cox1 synthesis in Saccharomyces cerevisiae mitochondria. J. Biol. Chem. 285:4534382–89
    [Google Scholar]
  141. 141.  Shyamsundar R, Kim YH, Higgins JP, Montgomery K, Jorden M et al. 2005. A DNA microarray survey of gene expression in normal human tissues. Genome Biol. 6:3R22
    [Google Scholar]
  142. 142.  Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE et al. 2012. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLOS Biol. 10:1e1001241
    [Google Scholar]
  143. 143.  Srinivasan S, Guha M, Dong DW, Whelan KA, Ruthel G et al. 2016. Disruption of cytochrome c oxidase function induces the Warburg effect and metabolic reprogramming. Oncogene 35:121585–95
    [Google Scholar]
  144. 144.  Steele DF, Butler CA, Fox TD 1996. Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. PNAS 93:115253–57
    [Google Scholar]
  145. 145.  Stiburek L, Cesnekova J, Kostkova O, Fornuskova D, Vinsova K et al. 2012. YME1L controls the accumulation of respiratory chain subunits and is required for apoptotic resistance, cristae morphogenesis, and cell proliferation. Mol. Biol. Cell 23:61010–23
    [Google Scholar]
  146. 146.  Stroud DA, Surgenor EE, Formosa LE, Reljic B, Frazier AE et al. 2016. Accessory subunits are integral for assembly and function of human mitochondrial complex I. Nature 538:7623123–26
    [Google Scholar]
  147. 147.  Suomalainen A, Battersby BJ 2017. Mitochondrial diseases: the contribution of organelle stress responses to pathology. Nat. Rev. Mol. Cell Biol. 19:77–79
    [Google Scholar]
  148. 148.  Szczesny RJ, Borowski LS, Malecki M, Wojcik MA, Stepien PP, Golik P 2012. RNA degradation in yeast and human mitochondria. Biochim. Biophys. Acta 1819:9–101027–34
    [Google Scholar]
  149. 149.  Temperley RJ, Wydro M, Lightowlers RN, Chrzanowska-Lightowlers ZM 2010. Human mitochondrial mRNAs—like members of all families, similar but different. Biochim. Biophys. Acta 1797:6–71081–85
    [Google Scholar]
  150. 150.  Toyama BH, Savas JN, Park SK, Harris MS, Ingolia NT et al. 2013. Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154:5971–82
    [Google Scholar]
  151. 151.  Tyynismaa H, Sembongi H, Bokori-Brown M, Granycome C, Ashley N et al. 2004. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum. Mol. Genet. 13:243219–27
    [Google Scholar]
  152. 152.  van Waveren C, Moraes CT 2008. Transcriptional co-expression and co-regulation of genes coding for components of the oxidative phosphorylation system. BMC Genom 9:18
    [Google Scholar]
  153. 153.  Veltri KL, Espiritu M, Singh G 1990. Distinct genomic copy number in mitochondria of different mammalian organs. J. Cell. Physiol. 143:1160–64
    [Google Scholar]
  154. 154.  Vendramin R, Marine J-C, Leucci E 2017. Non-coding RNAs: the dark side of nuclear–mitochondrial communication. EMBO J 36:91123–33
    [Google Scholar]
  155. 155.  Virbasius JV, Scarpulla RC 1994. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. PNAS 91:41309–13
    [Google Scholar]
  156. 156.  von Heijne G 1986. Why mitochondria need a genome. FEBS Lett 198:11–4
    [Google Scholar]
  157. 157.  Walters RW, Matheny T, Mizoue LS, Rao BS, Muhlrad D, Parker R 2017. Identification of NAD+ capped mRNAs in Saccharomyces cerevisiae. PNAS 114:3480–85
    [Google Scholar]
  158. 158.  Weraarpachai W, Antonicka H, Sasarman F, Seeger J, Schrank B 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. 41:7833–37
    [Google Scholar]
  159. 159.  Williams RS 1986. Mitochondrial gene expression in mammalian striated muscle. Evidence that variation in gene dosage is the major regulatory event. J. Biol. Chem. 261:2612390–94
    [Google Scholar]
  160. 160.  Zhang X, Zuo X, Yang B, Li Z, Xue Y et al. 2014. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 158:3607–19
    [Google Scholar]
  161. 161.  Zurita Rendón O, Shoubridge EA 2012. Early complex I assembly defects result in rapid turnover of the ND1 subunit. Hum. Mol. Genet. 21:173815–24
    [Google Scholar]
/content/journals/10.1146/annurev-genet-120417-031709
Loading
/content/journals/10.1146/annurev-genet-120417-031709
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