DOI QR코드

DOI QR Code

Mitochondrial noncoding RNA transport

  • Kim, Kyoung Mi (Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, National Institutes of Health) ;
  • Noh, Ji Heon (Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, National Institutes of Health) ;
  • Abdelmohsen, Kotb (Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, National Institutes of Health) ;
  • Gorospe, Myriam (Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, National Institutes of Health)
  • Received : 2017.01.19
  • Published : 2017.04.30

Abstract

Mitochondria are cytosolic organelles essential for generating energy and maintaining cell homeostasis. Despite their critical function, the handful of proteins expressed by the mitochondrial genome is insufficient to maintain mitochondrial structure or activity. Accordingly, mitochondrial metabolism is fully dependent on factors encoded by the nuclear DNA, including many proteins synthesized in the cytosol and imported into mitochondria via established mechanisms. However, there is growing evidence that mammalian mitochondria can also import cytosolic noncoding RNA via poorly understood processes. Here, we summarize our knowledge of mitochondrial RNA, discuss recent progress in understanding the molecular mechanisms and functional impact of RNA import into mitochondria, and identify rising challenges and opportunities in this rapidly evolving field.

Keywords

References

  1. Gray MW, Burger G and Lang BF (1999) Mitochondrial evolution. Science 283, 1476-1481 https://doi.org/10.1126/science.283.5407.1476
  2. Lane N and Martin W (2010) The energetics of genome complexity. Nature 467, 929-934 https://doi.org/10.1038/nature09486
  3. Neupert W and Herrmann JM (2007) Translocation of proteins into mitochondria. Annu Rev Biochem 76, 723-749 https://doi.org/10.1146/annurev.biochem.76.052705.163409
  4. Chacinska A, Koehler CM, Milenkovic D, Lithgow T and Pfanner N (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628-644 https://doi.org/10.1016/j.cell.2009.08.005
  5. Schmidt O, Pfanner N and Meisinger C (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat Rev Mol Cell Biol 11, 655-667 https://doi.org/10.1038/nrm2959
  6. Suyama Y (1967) The origins of mitochondrial ribonucleic acids in Tetrahymena pyriformis. Biochemistry 6, 2829-2839 https://doi.org/10.1021/bi00861a025
  7. Chang DD and Clayton DA (1989) Mouse RNAase MRP RNA is encoded by a nuclear gene and contains a decamer sequence complementary to a conserved region of mitochondrial RNA substrate. Cell 56, 131-139 https://doi.org/10.1016/0092-8674(89)90991-4
  8. Chang DD and Clayton DA (1987) A mammalian mitochondrial RNA processing activity contains nucleusencoded RNA. Science 235, 1178-1184 https://doi.org/10.1126/science.2434997
  9. Yoshionari S, Koike T, Yokogawa T et al (1994) Existence of nuclear-encoded 5S-rRNA in bovine mitochondria. FEBS Lett 338, 137-142 https://doi.org/10.1016/0014-5793(94)80351-X
  10. Kiss T and Filipowicz W (1992) Evidence against a mitochondrial location of the 7-2/MRP RNA in mammalian cells. Cell 70, 11-16 https://doi.org/10.1016/0092-8674(92)90528-K
  11. Magalhaes PJ, Andreu AL and Schon EA (1998) Evidence for the presence of 5S rRNA in mammalian mitochondria. Mol Biol Cell 9, 2375-2382 https://doi.org/10.1091/mbc.9.9.2375
  12. Puranam RS and Attardi G (2001) The RNase P associated with HeLa cell mitochondria contains an essential RNA component identical in sequence to that of the nuclear RNase P. Mol Cell Biol 21, 548-561 https://doi.org/10.1128/MCB.21.2.548-561.2001
  13. Holzmann J, Frank P, Loffler E, Bennett KL, Gerner C and Rossmanith W (2008) RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135, 462-474 https://doi.org/10.1016/j.cell.2008.09.013
  14. Bandiera S, Ruberg S, Girard M et al (2011) Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 6, e20746 https://doi.org/10.1371/journal.pone.0020746
  15. Sripada L, Tomar D, Prajapati P, Singh R, Singh AK and Singh R (2012) Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 7, e44873 https://doi.org/10.1371/journal.pone.0044873
  16. Kamenski P, Kolesnikova O, Jubenot V et al (2007) Evidence for an adaptation mechanism of mitochondrial translation via tRNA import from the cytosol. Mol Cell 26, 625-637 https://doi.org/10.1016/j.molcel.2007.04.019
  17. Wang G, Chen HW, Oktay Y et al (2010) PNPASE regulates RNA import into mitochondria. Cell 142, 456-467 https://doi.org/10.1016/j.cell.2010.06.035
  18. Smirnov A, Entelis N, Martin RP and Tarassov I (2011) Biological significance of 5S rRNA import into human mitochondria: role of ribosomal protein MRP-L18. Genes Dev 25, 1289-1305 https://doi.org/10.1101/gad.624711
  19. Noh JH, Kim KM, Abdelmohsen K et al (2016) HuR and GRSF1 modulate the nuclear export and mitochondrial localization of the lncRNA RMRP. Genes Dev 30, 1224-1239
  20. O'Brien TW (2002) Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease. Gene 286, 73-79 https://doi.org/10.1016/S0378-1119(01)00808-3
  21. Ojala D, Montoya J and Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290, 470-474 https://doi.org/10.1038/290470a0
  22. Attardi G and Ojala D (1971) Mitochondrial ribssome in HeLa cells. Nat New Biol 229, 133-136
  23. Mercer TR, Neph S, Dinger ME et al (2011) The human mitochondrial transcriptome. Cell 146, 645-658 https://doi.org/10.1016/j.cell.2011.06.051
  24. Rackham O, Shearwood AM, Mercer TR, Davies SM, Mattick JS and Filipovska A (2011) Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA 17, 2085-2093 https://doi.org/10.1261/rna.029405.111
  25. Sanchez MI, Mercer TR, Davies SM et al (2011) RNA processing in human mitochondria. Cell Cycle 10, 2904-2916 https://doi.org/10.4161/cc.10.17.17060
  26. Villegas J, Burzio V, Villota C et al (2007) Expression of a novel non-coding mitochondrial RNA in human proliferating cells. Nucleic Acids Res 35, 7336-7347 https://doi.org/10.1093/nar/gkm863
  27. Villegas J, Zarraga AM, Muller I et al (2000) A novel chimeric mitochondrial RNA localized in the nucleus of mouse sperm. DNA Cell Biol 19, 579-588 https://doi.org/10.1089/104454900439809
  28. Burzio VA, Villota C, Villegas J et al (2009) Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells. Proc Natl Acad Sci U S A 106, 9430-9434 https://doi.org/10.1073/pnas.0903086106
  29. Landerer E, Villegas J, Burzio VA et al (2011) Nuclear localization of the mitochondrial ncRNAs in normal and cancer cells. Cell Oncol (Dordr) 34, 297-305 https://doi.org/10.1007/s13402-011-0018-8
  30. Bianchessi V, Badi I, Bertolotti M et al (2015) The mitochondrial lncRNA ASncmtRNA-2 is induced in aging and replicative senescence in Endothelial Cells. J Mol Cell Cardiol 81, 62-70 https://doi.org/10.1016/j.yjmcc.2015.01.012
  31. Kumarswamy R, Bauters C, Volkmann I et al (2014) Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ Res 114, 1569-1575 https://doi.org/10.1161/CIRCRESAHA.114.303915
  32. Entelis NS, Kolesnikova OA, Dogan S, Martin RP and Tarassov IA (2001) 5 S rRNA and tRNA import into human mitochondria. Comparison of in vitro requirements. J Biol Chem 276, 45642-45653 https://doi.org/10.1074/jbc.M103906200
  33. Li K, Smagula CS, Parsons WJ et al (1994) Subcellular partitioning of MRP RNA assessed by ultrastructural and biochemical analysis. J Cell Biol 124, 871-882 https://doi.org/10.1083/jcb.124.6.871
  34. Martin RP, Schneller JM, Stahl AJ and Dirheimer G (1977) Study of yeast mitochondrial tRNAs by twodimensional polyacrylamide gel electrophoresis: characterization of isoaccepting species and search for imported cytoplasmic tRNAs. Nucleic Acids Res 4, 3497-3510 https://doi.org/10.1093/nar/4.10.3497
  35. Simpson AM, Suyama Y, Dewes H, Campbell DA and Simpson L (1989) Kinetoplastid mitochondria contain functional tRNAs which are encoded in nuclear DNA and also contain small minicircle and maxicircle transcripts of unknown function. Nucleic Acids Res 17, 5427-5445 https://doi.org/10.1093/nar/17.14.5427
  36. Hancock K and Hajduk SL (1990) The mitochondrial tRNAs of Trypanosoma brucei are nuclear encoded. J Biol Chem 265, 19208-19215
  37. Mottram JC, Bell SD, Nelson RG and Barry JD (1991) tRNAs of Trypanosoma brucei. Unusual gene organization and mitochondrial importation. J Biol Chem 266, 18313-18317
  38. Lye LF, Chen DH and Suyama Y (1993) Selective import of nuclear-encoded tRNAs into mitochondria of the protozoan Leishmania tarentolae. Mol Biochem Parasitol 58, 233-245 https://doi.org/10.1016/0166-6851(93)90045-Y
  39. Schneider A, Martin J and Agabian N (1994) A nuclear encoded tRNA of Trypanosoma brucei is imported into mitochondria. Mol Cell Biol 14, 2317-2322 https://doi.org/10.1128/MCB.14.4.2317
  40. Rusconi CP and Cech TR (1996) Mitochondrial import of only one of three nuclear-encoded glutamine tRNAs in Tetrahymena thermophila. EMBO J 15, 3286-3295
  41. Martin RP, Schneller JM, Stahl AJ and Dirheimer G (1979) Import of nuclear deoxyribonucleic acid coded lysine-accepting transfer ribonucleic acid (anticodon C-U-U) into yeast mitochondria. Biochemistry 18, 4600-4605 https://doi.org/10.1021/bi00588a021
  42. Tarassov IA and Martin RP (1996) Mechanisms of tRNA import into yeast mitochondria: an overview. Biochimie 78, 502-510 https://doi.org/10.1016/0300-9084(96)84756-0
  43. Marechal-Drouard L, Weil JH and Guillemaut P (1988) Import of several tRNAs from the cytoplasm into the mitochondria in bean Phaseolus vulgaris. Nucleic Acids Res 16, 4777-4788 https://doi.org/10.1093/nar/16.11.4777
  44. Dietrich A, Small I, Cosset A, Weil JH and Marechal-Drouard L (1996) Editing and import: strategies for providing plant mitochondria with a complete set of functional transfer RNAs. Biochimie 78, 518-529 https://doi.org/10.1016/0300-9084(96)84758-4
  45. Akashi K, Sakurai K, Hirayama J, Fukuzawa H and Ohyama K (1996) Occurrence of nuclear-encoded tRNAIle in mitochondria of the liverwort Marchantia polymorpha. Curr Genet 30, 181-185 https://doi.org/10.1007/s002940050118
  46. Chen HC, Viry-Moussaid M, Dietrich A and Wintz H (1997) Evolution of a mitochondrial tRNA PHE gene in A. thaliana: import of cytosolic tRNA PHE into mitochondria. Biochem Biophys Res Commun 237, 432-437 https://doi.org/10.1006/bbrc.1997.7138
  47. Glover KE, Spencer DF and Gray MW (2001) Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem 276, 639-648 https://doi.org/10.1074/jbc.M007708200
  48. Brubacher-Kauffmann S, Marechal-Drouard L, Cosset A, Dietrich A and Duchene AM (1999) Differential import of nuclear-encoded tRNAGly isoacceptors into solanum Tuberosum mitochondria. Nucleic Acids Res 27, 2037-2042 https://doi.org/10.1093/nar/27.9.2037
  49. Dorner M, Altmann M, Paabo S and Morl M (2001) Evidence for import of a lysyl-tRNA into marsupial mitochondria. Mol Biol Cell 12, 2688-2698 https://doi.org/10.1091/mbc.12.9.2688
  50. Schneider A (2011) Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu Rev Biochem 80, 1033-1053 https://doi.org/10.1146/annurev-biochem-060109-092838
  51. Tarassov I, Kamenski P, Kolesnikova O et al (2007) Import of nuclear DNA-encoded RNAs into mitochondria and mitochondrial translation. Cell Cycle 6, 2473-2477 https://doi.org/10.4161/cc.6.20.4783
  52. Kolesnikova OA, Entelis NS, Jacquin-Becker C et al (2004) Nuclear DNA-encoded tRNAs targeted into mitochondria can rescue a mitochondrial DNA mutation associated with the MERRF syndrome in cultured human cells. Hum Mol Genet 13, 2519-2534 https://doi.org/10.1093/hmg/ddh267
  53. Kolesnikova OA, Entelis NS, Mireau H, Fox TD, Martin RP and Tarassov IA (2000) Suppression of mutations in mitochondrial DNA by tRNAs imported from the cytoplasm. Science 289, 1931-1933 https://doi.org/10.1126/science.289.5486.1931
  54. Tarassov IA and Entelis NS (1992) Mitochondriallyimported cytoplasmic tRNA(Lys)(CUU) of Saccharomyces cerevisiae: in vivo and in vitro targetting systems. Nucleic Acids Res 20, 1277-1281 https://doi.org/10.1093/nar/20.6.1277
  55. Rubio MA, Rinehart JJ, Krett B et al (2008) Mammalian mitochondria have the innate ability to import tRNAs by a mechanism distinct from protein import. Proc Natl Acad Sci U S A 105, 9186-9191 https://doi.org/10.1073/pnas.0804283105
  56. Brandina I, Graham J, Lemaitre-Guillier C et al (2006) Enolase takes part in a macromolecular complex associated to mitochondria in yeast. Biochim Biophys Acta 1757, 1217-1228 https://doi.org/10.1016/j.bbabio.2006.07.001
  57. Entelis N, Brandina I, Kamenski P, Krasheninnikov IA, Martin RP and Tarassov I (2006) A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes Dev 20, 1609-1620 https://doi.org/10.1101/gad.385706
  58. Kamenski P, Smirnova E, Kolesnikova O 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, 284-293 https://doi.org/10.1016/j.mito.2010.01.002
  59. Tarassov I, Entelis N and Martin RP (1995) Mitochondrial import of a cytoplasmic lysine-tRNA in yeast is mediated by cooperation of cytoplasmic and mitochondrial lysyltRNA synthetases. EMBO J 14, 3461-3471
  60. Tarassov I, Entelis N and Martin RP (1995) An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA. J Mol Biol 245, 315-323 https://doi.org/10.1006/jmbi.1994.0026
  61. Kolesnikova O, Kazakova H, Comte C et al (2010) Selection of RNA aptamers imported into yeast and human mitochondria. RNA 16, 926-941 https://doi.org/10.1261/rna.1914110
  62. Gowher A, Smirnov A, Tarassov I and Entelis N (2013) Induced tRNA import into human mitochondria: implication of a host aminoacyl-tRNA-synthetase. PLoS One 8, e66228 https://doi.org/10.1371/journal.pone.0066228
  63. Eilers M and Schatz G (1986) Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322, 228-232 https://doi.org/10.1038/322228a0
  64. Entelis NS, Kieffer S, Kolesnikova OA, Martin RP and Tarassov IA (1998) Structural requirements of tRNALys for its import into yeast mitochondria. Proc Natl Acad Sci U S A 95, 2838-2843 https://doi.org/10.1073/pnas.95.6.2838
  65. Vestweber D and Schatz G (1989) DNA-protein conjugates can enter mitochondria via the protein import pathway. Nature 338, 170-172 https://doi.org/10.1038/338170a0
  66. Nierlich DP (1982) Fragmentary 5S rRNA gene in the human mitochondrial genome. Mol Cell Biol 2, 207-209 https://doi.org/10.1128/MCB.2.2.207
  67. Pelham HR and Brown DD (1980) A specific transcription factor that can bind either the 5S RNA gene or 5S RNA. Proc Natl Acad Sci U S A 77, 4170-4174 https://doi.org/10.1073/pnas.77.7.4170
  68. Guddat U, Bakken AH and Pieler T (1990) Proteinmediated nuclear export of RNA: 5S rRNA containing small RNPs in xenopus oocytes. Cell 60, 619-628 https://doi.org/10.1016/0092-8674(90)90665-2
  69. Chan YL, Lin A, McNally J and Wool IG (1987) The primary structure of rat ribosomal protein L5. A comparison of the sequence of amino acids in the proteins that interact with 5 S rRNA. J Biol Chem 262, 12879-12886
  70. Steitz JA, Berg C, Hendrick JP et al (1988) A 5S rRNA/L5 complex is a precursor to ribosome assembly in mammalian cells. J Cell Biol 106, 545-556 https://doi.org/10.1083/jcb.106.3.545
  71. Rudt F and Pieler T (1996) Cytoplasmic retention and nuclear import of 5S ribosomal RNA containing RNPs. EMBO J 15, 1383-1391
  72. Smirnov A, Tarassov I, Mager-Heckel AM et al (2008) Two distinct structural elements of 5S rRNA are needed for its import into human mitochondria. RNA 14, 749-759 https://doi.org/10.1261/rna.952208
  73. Smirnov A, Comte C, Mager-Heckel AM et al (2010) Mitochondrial enzyme rhodanese is essential for 5 S ribosomal RNA import into human mitochondria. J Biol Chem 285, 30792-30803 https://doi.org/10.1074/jbc.M110.151183
  74. Ridanpaa M, van Eenennaam H, Pelin K et al (2001) Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia. Cell 104, 195-203 https://doi.org/10.1016/S0092-8674(01)00205-7
  75. Hermanns P, Bertuch AA, Bertin TK et al (2005) Consequences of mutations in the non-coding RMRP RNA in cartilage-hair hypoplasia. Hum Mol Genet 14, 3723-3740 https://doi.org/10.1093/hmg/ddi403
  76. Chu S, Archer RH, Zengel JM and Lindahl L (1994) The RNA of RNase MRP is required for normal processing of ribosomal RNA. Proc Natl Acad Sci U S A 91, 659-663 https://doi.org/10.1073/pnas.91.2.659
  77. Schmitt ME and Clayton DA (1993) Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Mol Cell Biol 13, 7935-7941 https://doi.org/10.1128/MCB.13.12.7935
  78. Gill T, Cai T, Aulds J, Wierzbicki S and Schmitt ME (2004) RNase MRP cleaves the CLB2 mRNA to promote cell cycle progression: novel method of mRNA degradation. Mol Cell Biol 24, 945-953 https://doi.org/10.1128/MCB.24.3.945-953.2004
  79. Maida Y, Yasukawa M, Furuuchi M et al (2009) An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA. Nature 461, 230-235 https://doi.org/10.1038/nature08283
  80. Chen HW, Rainey RN, Balatoni CE et al (2006) Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis. Mol Cell Biol 26, 8475-8487 https://doi.org/10.1128/MCB.01002-06
  81. Chen HW, Koehler CM and Teitell MA (2007) Human polynucleotide phosphorylase: location matters. Trends Cell Biol 17, 600-608 https://doi.org/10.1016/j.tcb.2007.09.006
  82. Rainey RN, Glavin JD, Chen HW, French SW, Teitell MA and Koehler CM (2006) A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space. Mol Cell Biol 26, 8488-8497 https://doi.org/10.1128/MCB.01006-06
  83. Guerrier-Takada C, Gardiner K, Marsh T, Pace N and Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35, 849-857 https://doi.org/10.1016/0092-8674(83)90117-4
  84. Pannucci JA, Haas ES, Hall TA, Harris JK and Brown JW (1999) RNase P RNAs from some Archaea are catalytically active. Proc Natl Acad Sci U S A 96, 7803-7808 https://doi.org/10.1073/pnas.96.14.7803
  85. Kikovska E, Svard SG and Kirsebom LA (2007) Eukaryotic RNase P RNA mediates cleavage in the absence of protein. Proc Natl Acad Sci U S A 104, 2062-2067 https://doi.org/10.1073/pnas.0607326104
  86. Doersen CJ, Guerrier-Takada C, Altman S and Attardi G (1985) Characterization of an RNase P activity from HeLa cell mitochondria. Comparison with the cytosol RNase P activity. J Biol Chem 260, 5942-5949
  87. Rossmanith W and Karwan RM (1998) Characterization of human mitochondrial RNase P: novel aspects in tRNA processing. Biochem Biophys Res Commun 247, 234-241 https://doi.org/10.1006/bbrc.1998.8766
  88. Bartkiewicz M, Gold H and Altman S (1989) Identification and characterization of an RNA molecule that copurifies with RNase P activity from HeLa cells. Genes Dev 3, 488-499 https://doi.org/10.1101/gad.3.4.488
  89. Huntzinger E and Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12, 99-110 https://doi.org/10.1038/nrg2936
  90. Filipowicz W, Bhattacharyya SN and Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9, 102-114 https://doi.org/10.1038/nrg2290
  91. Fabian MR, Sonenberg N and Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79, 351-379 https://doi.org/10.1146/annurev-biochem-060308-103103
  92. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 https://doi.org/10.1016/j.cell.2009.01.002
  93. Kim VN, Han J and Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10, 126-139
  94. Newman MA and Hammond SM (2010) Emerging paradigms of regulated microRNA processing. Genes Dev 24, 1086-1092 https://doi.org/10.1101/gad.1919710
  95. Kloosterman WP and Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11, 441-450 https://doi.org/10.1016/j.devcel.2006.09.009
  96. Lingor P (2010) Regulation of Cell Death and Survival by RNA Interference - The Roles of miRNA and siRNA; in Apoptosome: An up-and-coming therapeutical tool, Cecconi F and D'Amelio M (eds.), 95-117, Springer Netherlands, Dordrecht
  97. Catalanotto C, Cogoni C and Zardo G (2016) MicroRNA in Control of Gene Expression: An Overview of Nuclear Functions. Int J Mol Sci 17
  98. Yao S (2016) MicroRNA biogenesis and their functions in regulating stem cell potency and differentiation. Biol Proced Online 18, 8 https://doi.org/10.1186/s12575-016-0037-y
  99. Bushati N and Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23, 175-205 https://doi.org/10.1146/annurev.cellbio.23.090506.123406
  100. Abdelmohsen K and Gorospe M (2015) Noncoding RNA control of cellular senescence. Wiley Interdiscip Rev RNA 6, 615-629 https://doi.org/10.1002/wrna.1297
  101. Rottiers V and Naar AM (2012) MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 13, 239-250 https://doi.org/10.1038/nrm3313
  102. Shah MY, Ferrajoli A, Sood AK, Lopez-Berestein G and Calin GA (2016) microRNA Therapeutics in Cancer - An Emerging Concept. EBioMedicine 12, 34-42 https://doi.org/10.1016/j.ebiom.2016.09.017
  103. Saeidimehr S, Ebrahimi A, Saki N, Goodarzi P and Rahim F (2016) MicroRNA-Based Linkage between Aging and Cancer: from Epigenetics View Point. Cell J 18, 117-126
  104. Das S, Ferlito M, Kent OA et al (2012) Nuclear miRNA regulates the mitochondrial genome in the heart. Circ Res 110, 1596-1603 https://doi.org/10.1161/CIRCRESAHA.112.267732
  105. Sripada L, Tomar D and Singh R (2012) Mitochondria: one of the destinations of miRNAs. Mitochondrion 12, 593-599 https://doi.org/10.1016/j.mito.2012.10.009
  106. Bienertova-Vasku J, Sana J and Slaby O (2013) The role of microRNAs in mitochondria in cancer. Cancer Lett 336, 1-7 https://doi.org/10.1016/j.canlet.2013.05.001
  107. Barrey E, Saint-Auret G, Bonnamy B, Damas D, Boyer O and Gidrol X (2011) Pre-microRNA and mature microRNA in human mitochondria. PLoS One 6, e20220 https://doi.org/10.1371/journal.pone.0020220
  108. Srinivasan H and Das S (2015) Mitochondrial miRNA (MitomiR): a new player in cardiovascular health. Can J Physiol Pharmacol 93, 855-861 https://doi.org/10.1139/cjpp-2014-0500
  109. Zhang X, Zuo X, Yang B et al (2014) MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 158, 607-619 https://doi.org/10.1016/j.cell.2014.05.047
  110. Bandiera S, Mategot R, Girard M, Demongeot J and Henrion-Caude A (2013) MitomiRs delineating the intracellular localization of microRNAs at mitochondria. Free Radic Biol Med 64, 12-19 https://doi.org/10.1016/j.freeradbiomed.2013.06.013
  111. Duarte FV, Palmeira CM and Rolo AP (2014) The Role of microRNAs in Mitochondria: Small Players Acting Wide. Genes (Basel) 5, 865-886 https://doi.org/10.3390/genes5040865
  112. Das S, Bedja D, Campbell N et al (2014) miR-181c regulates the mitochondrial genome, bioenergetics, and propensity for heart failure in vivo. PLoS One 9, e96820 https://doi.org/10.1371/journal.pone.0096820
  113. Dasgupta N, Peng Y, Tan Z, Ciraolo G, Wang D and Li R (2015) miRNAs in mtDNA-less cell mitochondria. Cell Death Discov 1, 15004
  114. Bukeirat M, Sarkar SN, Hu H, Quintana DD, Simpkins JW and Ren X (2016) MiR-34a regulates blood-brain barrier permeability and mitochondrial function by targeting cytochrome c. J Cereb Blood Flow Metab 36, 387-392 https://doi.org/10.1177/0271678X15606147
  115. Jagannathan R, Thapa D, Nichols CE et al (2015) Translational Regulation of the Mitochondrial Genome Following Redistribution of Mitochondrial MicroRNA in the Diabetic Heart. Circ Cardiovasc Genet 8, 785-802 https://doi.org/10.1161/CIRCGENETICS.115.001067
  116. Guttman M and Rinn JL (2012) Modular regulatory principles of large non-coding RNAs. Nature 482, 339-346 https://doi.org/10.1038/nature10887
  117. Kretz M, Siprashvili Z, Chu C et al (2013) Control of somatic tissue differentiation by the long non-coding RNA TINCR. Nature 493, 231-235
  118. Guttman M, Amit I, Garber M et al (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223-227 https://doi.org/10.1038/nature07672
  119. Khalil AM, Guttman M, Huarte M et al (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 106, 11667-11672 https://doi.org/10.1073/pnas.0904715106
  120. Rinn JL, Kertesz M, Wang JK et al (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323 https://doi.org/10.1016/j.cell.2007.05.022
  121. Mattick JS and Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15 Spec No 1, R17-29 https://doi.org/10.1093/hmg/ddl046
  122. Carpenter S, Aiello D, Atianand MK et al (2013) A long noncoding RNA mediates both activation and repression of immune response genes. Science 341, 789-792 https://doi.org/10.1126/science.1240925
  123. Huarte M, Guttman M, Feldser D et al (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409-419 https://doi.org/10.1016/j.cell.2010.06.040
  124. Salinas T, Duchene AM, Delage L et al (2006) The voltage-dependent anion channel, a major component of the tRNA import machinery in plant mitochondria. Proc Natl Acad Sci U S A 103, 18362-18367 https://doi.org/10.1073/pnas.0606449103
  125. O'Brien TW (1971) The general occurrence of 55 S ribosomes in mammalian liver mitochondria. J Biol Chem 246, 3409-3417
  126. Grivell LA, Reijnders L and Borst P (1971) Isolation of yeast mitochondrial ribosomes highly active in protein synthesis. Biochim Biophys Acta 247, 91-103 https://doi.org/10.1016/0005-2787(71)90811-2
  127. Sharma MR, Booth TM, Simpson L, Maslov DA and Agrawal RK (2009) Structure of a mitochondrial ribosome with minimal RNA. Proc Natl Acad Sci U S A 106, 9637-9642 https://doi.org/10.1073/pnas.0901631106
  128. Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL and Agrawal RK (2003) Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115, 97-108 https://doi.org/10.1016/S0092-8674(03)00762-1
  129. Smits P, Smeitink JA, van den Heuvel LP, Huynen MA and Ettema TJ (2007) Reconstructing the evolution of the mitochondrial ribosomal proteome. Nucleic Acids Res 35, 4686-4703 https://doi.org/10.1093/nar/gkm441
  130. Mears JA, Sharma MR, Gutell RR et al (2006) A structural model for the large subunit of the mammalian mitochondrial ribosome. J Mol Biol 358, 193-212 https://doi.org/10.1016/j.jmb.2006.01.094
  131. Agrawal RK and Sharma MR (2012) Structural aspects of mitochondrial translational apparatus. Curr Opin Struct Biol 22, 797-803 https://doi.org/10.1016/j.sbi.2012.08.003
  132. Cha MY, Han SH, Son SM et al (2012) Mitochondriaspecific accumulation of amyloid beta induces mitochondrial dysfunction leading to apoptotic cell death. PLoS One 7, e34929 https://doi.org/10.1371/journal.pone.0034929
  133. Reddy PH (2009) Amyloid beta, mitochondrial structural and functional dynamics in Alzheimer's disease. Exp Neurol 218, 286-292 https://doi.org/10.1016/j.expneurol.2009.03.042
  134. Canugovi C, Shamanna RA, Croteau DL and Bohr VA (2014) Base excision DNA repair levels in mitochondrial lysates of Alzheimer's disease. Neurobiol Aging 35, 1293-1300 https://doi.org/10.1016/j.neurobiolaging.2014.01.004
  135. Marongiu R, Spencer B, Crews L et al (2009) Mutant Pink1 induces mitochondrial dysfunction in a neuronal cell model of Parkinson's disease by disturbing calcium flux. J Neurochem 108, 1561-1574 https://doi.org/10.1111/j.1471-4159.2009.05932.x
  136. Mortiboys H, Thomas KJ, Koopman WJ et al (2008) Mitochondrial function and morphology are impaired in parkin-mutant fibroblasts. Ann Neurol 64, 555-565 https://doi.org/10.1002/ana.21492
  137. Canet-Aviles RM, Wilson MA, Miller DW et al (2004) The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci U S A 101, 9103-9108 https://doi.org/10.1073/pnas.0402959101
  138. Devi L, Raghavendran V, Prabhu BM, Avadhani NG and Anandatheerthavarada HK (2008) Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J Biol Chem 283, 9089-9100 https://doi.org/10.1074/jbc.M710012200
  139. Ide T, Tsutsui H, Hayashidani S et al (2001) Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 88, 529-535 https://doi.org/10.1161/01.RES.88.5.529
  140. Ballinger SW, Patterson C, Knight-Lozano CA et al (2002) Mitochondrial integrity and function in atherogenesis. Circulation 106, 544-549 https://doi.org/10.1161/01.CIR.0000023921.93743.89
  141. Romanello V, Guadagnin E, Gomes L et al (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29, 1774-1785 https://doi.org/10.1038/emboj.2010.60
  142. Crescenzo R, Bianco F, Mazzoli A, Giacco A, Liverini G and Iossa S (2014) Mitochondrial efficiency and insulin resistance. Front Physiol 5, 512
  143. Mathur S, Brooks D and Carvalho CR (2014) Structural alterations of skeletal muscle in copd. Front Physiol 5, 104
  144. Antunes F, Corazzari M, Pereira G, Fimia GM, Piacentini M and Smaili S (2016) Fasting boosts sensitivity of human skin melanoma to cisplatin-induced cell death. Biochem Biophys Res Commun [Epub ahead of print]
  145. Katsetos CD, Anni H and Draber P (2013) Mitochondrial dysfunction in gliomas. Semin Pediatr Neurol 20, 216-227 https://doi.org/10.1016/j.spen.2013.09.003
  146. Trifunovic A, Wredenberg A, Falkenberg M et al (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423 https://doi.org/10.1038/nature02517
  147. Sastre J, Pallardo FV, Garcia de la Asuncion J and Vina J (2000) Mitochondria, oxidative stress and aging. Free Radic Res 32, 189-198 https://doi.org/10.1080/10715760000300201
  148. Smirnov AV, Entelis NS, Krasheninnikov IA, Martin R and Tarassov IA (2008) Specific features of 5S rRNA structure - its interactions with macromolecules and possible functions. Biochemistry (Mosc) 73, 1418-1437 https://doi.org/10.1134/S000629790813004X
  149. Tonin Y, Heckel AM, Vysokikh M et al (2014) Modeling of antigenomic therapy of mitochondrial diseases by mitochondrially addressed RNA targeting a pathogenic point mutation in mitochondrial DNA. J Biol Chem 289, 13323-13334 https://doi.org/10.1074/jbc.M113.528968

Cited by

  1. How long noncoding RNAs enforce their will on mitochondrial activity: regulation of mitochondrial respiration, reactive oxygen species production, apoptosis, and metabolic reprogramming in cancer 2018, https://doi.org/10.1007/s00294-017-0744-1
  2. pp.15216543, 2018, https://doi.org/10.1002/iub.1919
  3. Non-coding RNAs: long non-coding RNAs and microRNAs in endocrine-related cancers vol.25, pp.4, 2018, https://doi.org/10.1530/ERC-17-0548
  4. A microRNA’s journey to the center of the mitochondria vol.315, pp.2, 2018, https://doi.org/10.1152/ajpheart.00714.2017