Mitochondrial noncoding RNA transport
1
조회
0
다운로드
2
인용
0
참고문헌
키워드
초록
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.
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.
참고문헌 (149)
- Gray MW, "Mitochondrial evolution", Science, 283, pp.1476~1481 (1999)
- Lane N, "The energetics of genome complexity", Nature, 467, pp.929~934 (2010)
- Neupert W, "Translocation of proteins into mitochondria", Annu Rev Biochem, 76, pp.723~749 (2007)
- Chacinska A, "Importing mitochondrial proteins: machineries and mechanisms", Cell, 138, pp.628~644 (2009)
- Schmidt O, "Mitochondrial protein import: from proteomics to functional mechanisms", Nat Rev Mol Cell Biol, 11, pp.655~667 (2010)
- Suyama Y, "The origins of mitochondrial ribonucleic acids in Tetrahymena pyriformis", Biochemistry, 6, pp.2829~2839 (1967)
- Chang DD, "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, pp.131~139 (1989)
- Chang DD, "A mammalian mitochondrial RNA processing activity contains nucleusencoded RNA", Science, 235, pp.1178~1184 (1987)
- Yoshionari S, "Existence of nuclear-encoded 5S-rRNA in bovine mitochondria", FEBS Lett, 338, pp.137~142 (1994)
- Kiss T, "Evidence against a mitochondrial location of the 7-2", MRP RNA in mammalian cells, 1992, pp.70, 11~16
- Magalhaes PJ, "Evidence for the presence of 5S rRNA in mammalian mitochondria", Mol Biol Cell, 9, pp.2375~2382 (1998)
- Puranam RS, "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, pp.548~561 (2001)
- Holzmann J, "RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme", Cell, 135, pp.462~474 (2008)
- Bandiera S, "Nuclear outsourcing of RNA interference components to human mitochondria", PLoS One, 6, pp.e20746~ (2011)
- Sripada L, "Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA", PLoS One, 7, pp.e44873~ (2012)
- Kamenski P, "Evidence for an adaptation mechanism of mitochondrial translation via tRNA import from the cytosol", Mol Cell, 26, pp.625~637 (2007)
- Wang G, "PNPASE regulates RNA import into mitochondria", Cell, 142, pp.456~467 (2010)
- Smirnov A, "Biological significance of 5S rRNA import into human mitochondria: role of ribosomal protein MRP-L18", Genes Dev, 25, pp.1289~1305 (2011)
- Noh JH, "HuR and GRSF1 modulate the nuclear export and mitochondrial localization of the lncRNA RMRP.", Genes Dev, 30, pp.1224~1239 (2016)
- O'Brien TW, "Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease", Gene, 286, pp.73~79 (2002)
- Ojala D, "tRNA punctuation model of RNA processing in human mitochondria", Nature, 290, pp.470~474 (1981)
- Attardi G, "Mitochondrial ribssome in HeLa cells", Nat New Biol, 229, pp.133~136 (1971)
- Mercer TR, "The human mitochondrial transcriptome", Cell, 146, pp.645~658 (2011)
- Rackham O, "Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins", RNA, 17, pp.2085~2093 (2011)
- Sanchez MI, "RNA processing in human mitochondria", Cell Cycle, 10, pp.2904~2916 (2011)
- Villegas J, "Expression of a novel non-coding mitochondrial RNA in human proliferating cells", Nucleic Acids Res, 35, pp.7336~7347 (2007)
- Villegas J, "A novel chimeric mitochondrial RNA localized in the nucleus of mouse sperm", DNA Cell Biol, 19, pp.579~588 (2000)
- Burzio VA, "Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells", Proc Natl Acad Sci U S A, 106, pp.9430~9434 (2009)
- Landerer E, "Nuclear localization of the mitochondrial ncRNAs in normal and cancer cells", Cell Oncol (Dordr), 34, pp.297~305 (2011)
- Bianchessi V, "The mitochondrial lncRNA ASncmtRNA-2 is induced in aging and replicative senescence in Endothelial Cells", J Mol Cell Cardiol, 81, pp.62~70 (2015)
- Kumarswamy R, "Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure", Circ Res, 114, pp.1569~1575 (2014)
- Entelis NS, "5 S rRNA and tRNA import into human mitochondria. Comparison of in vitro requirements", J Biol Chem, 276, pp.45642~45653 (2001)
- Li K, "Subcellular partitioning of MRP RNA assessed by ultrastructural and biochemical analysis", J Cell Biol, 124, pp.871~882 (1994)
- Martin RP, "Study of yeast mitochondrial tRNAs by twodimensional polyacrylamide gel electrophoresis: characterization of isoaccepting species and search for imported cytoplasmic tRNAs", Nucleic Acids Res, 4, pp.3497~3510 (1977)
- Simpson AM, "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, pp.5427~5445 (1989)
- Hancock K, "The mitochondrial tRNAs of Trypanosoma brucei are nuclear encoded", J Biol Chem, 265, pp.19208~19215 (1990)
- Mottram JC, "tRNAs of Trypanosoma brucei. Unusual gene organization and mitochondrial importation", J Biol Chem, 266, pp.18313~18317 (1991)
- Lye LF, "Selective import of nuclear-encoded tRNAs into mitochondria of the protozoan Leishmania tarentolae", Mol Biochem Parasitol, 58, pp.233~245 (1993)
- Schneider A, "A nuclear encoded tRNA of Trypanosoma brucei is imported into mitochondria", Mol Cell Biol, 14, pp.2317~2322 (1994)
- Rusconi CP, "Mitochondrial import of only one of three nuclear-encoded glutamine tRNAs in Tetrahymena thermophila", EMBO J, 15, pp.3286~3295 (1996)
- Martin RP, "Import of nuclear deoxyribonucleic acid coded lysine-accepting transfer ribonucleic acid (anticodon C-U-U) into yeast mitochondria", Biochemistry, 18, pp.4600~4605 (1979)
- Tarassov IA, "Mechanisms of tRNA import into yeast mitochondria: an overview", Biochimie, 78, pp.502~510 (1996)
- Marechal-Drouard L, "Import of several tRNAs from the cytoplasm into the mitochondria in bean Phaseolus vulgaris", Nucleic Acids Res, 16, pp.4777~4788 (1988)
- Dietrich A, "Editing and import: strategies for providing plant mitochondria with a complete set of functional transfer RNAs", Biochimie, 78, pp.518~529 (1996)
- Akashi K, "Occurrence of nuclear-encoded tRNAIle in mitochondria of the liverwort Marchantia polymorpha", Curr Genet, 30, pp.181~185 (1996)
- Chen HC, "Evolution of a mitochondrial tRNA PHE gene in A. thaliana: import of cytosolic tRNA PHE into mitochondria", Biochem Biophys Res Commun, 237, pp.432~437 (1997)
- Glover KE, "Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria", J Biol Chem, 276, pp.639~648 (2001)
- Brubacher-Kauffmann S, "Differential import of nuclear-encoded tRNAGly isoacceptors into solanum Tuberosum mitochondria", Nucleic Acids Res, 27, pp.2037~2042 (1999)
- Dorner M, "Evidence for import of a lysyl-tRNA into marsupial mitochondria", Mol Biol Cell, 12, pp.2688~2698 (2001)
- Schneider A, "Mitochondrial tRNA import and its consequences for mitochondrial translation", Annu Rev Biochem, 80, pp.1033~1053 (2011)
- Tarassov I, "Import of nuclear DNA-encoded RNAs into mitochondria and mitochondrial translation", Cell Cycle, 6, pp.2473~2477 (2007)
- Kolesnikova OA, "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, pp.2519~2534 (2004)
- Kolesnikova OA, "Suppression of mutations in mitochondrial DNA by tRNAs imported from the cytoplasm", Science, 289, pp.1931~1933 (2000)
- Tarassov IA, "Mitochondriallyimported cytoplasmic tRNA(Lys)(CUU) of Saccharomyces cerevisiae: in vivo and in vitro targetting systems", Nucleic Acids Res, 20, pp.1277~1281 (1992)
- Rubio MA, "Mammalian mitochondria have the innate ability to import tRNAs by a mechanism distinct from protein import", Proc Natl Acad Sci U S A, 105, pp.9186~9191 (2008)
- Brandina I, "Enolase takes part in a macromolecular complex associated to mitochondria in yeast", Biochim Biophys Acta, 1757, pp.1217~1228 (2006)
- Entelis N, "A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae", Genes Dev, 20, pp.1609~1620 (2006)
- Kamenski P, "tRNA mitochondrial import in yeast: Mapping of the import determinants in the carrier protein, the precursor of mitochondrial lysyl-tRNA synthetase", Mitochondrion, 10, pp.284~293 (2010)
- Tarassov I, "Mitochondrial import of a cytoplasmic lysine-tRNA in yeast is mediated by cooperation of cytoplasmic and mitochondrial lysyltRNA synthetases", EMBO J, 14, pp.3461~3471 (1995)
- Tarassov I, "An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA", J Mol Biol, 245, pp.315~323 (1995)
- Kolesnikova O, "Selection of RNA aptamers imported into yeast and human mitochondria", RNA, 16, pp.926~941 (2010)
- Gowher A, "Induced tRNA import into human mitochondria: implication of a host aminoacyl-tRNA-synthetase", PLoS One, 8, pp.e66228~ (2013)
- Eilers M, "Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria", Nature, 322, pp.228~232 (1986)
- Entelis NS, "Structural requirements of tRNALys for its import into yeast mitochondria", Proc Natl Acad Sci U S A, 95, pp.2838~2843 (1998)
- Vestweber D, "DNA-protein conjugates can enter mitochondria via the protein import pathway", Nature, 338, pp.170~172 (1989)
- Nierlich DP, "Fragmentary 5S rRNA gene in the human mitochondrial genome", Mol Cell Biol, 2, pp.207~209 (1982)
- Pelham HR, "A specific transcription factor that can bind either the 5S RNA gene or 5S RNA", Proc Natl Acad Sci U S A, 77, pp.4170~4174 (1980)
- Guddat U, "Proteinmediated nuclear export of RNA: 5S rRNA containing small RNPs in xenopus oocytes", Cell, 60, pp.619~628 (1990)
- Chan YL, "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, pp.12879~12886 (1987)
- Steitz JA, "A 5S rRNA", L5 complex is a precursor to ribosome assembly in mammalian cells, 1988, pp.106, 545~556
- Rudt F, "Cytoplasmic retention and nuclear import of 5S ribosomal RNA containing RNPs", EMBO J, 15, pp.1383~1391 (1996)
- Smirnov A, "Two distinct structural elements of 5S rRNA are needed for its import into human mitochondria", RNA, 14, pp.749~759 (2008)
- Smirnov A, "Mitochondrial enzyme rhodanese is essential for 5 S ribosomal RNA import into human mitochondria", J Biol Chem, 285, pp.30792~30803 (2010)
- Ridanpaa M, "Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia", Cell, 104, pp.195~203 (2001)
- Hermanns P, "Consequences of mutations in the non-coding RMRP RNA in cartilage-hair hypoplasia", Hum Mol Genet, 14, pp.3723~3740 (2005)
- Chu S, "The RNA of RNase MRP is required for normal processing of ribosomal RNA", Proc Natl Acad Sci U S A, 91, pp.659~663 (1994)
- Schmitt ME, "Nuclear RNase MRP is required for correct processing of pre-5. 8S rRNA in Saccharomyces cerevisiae", Mol Cell Biol, 13, pp.7935~7941 (1993)
- Gill T, "RNase MRP cleaves the CLB2 mRNA to promote cell cycle progression: novel method of mRNA degradation", Mol Cell Biol, 24, pp.945~953 (2004)
- Maida Y, "An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA", Nature, 461, pp.230~235 (2009)
- Chen HW, "Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis", Mol Cell Biol, 26, pp.8475~8487 (2006)
- Chen HW, "Human polynucleotide phosphorylase: location matters", Trends Cell Biol, 17, pp.600~608 (2007)
- Rainey RN, "A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space", Mol Cell Biol, 26, pp.8488~8497 (2006)
- Guerrier-Takada C, "The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme", Cell, 35, pp.849~857 (1983)
- Pannucci JA, "RNase P RNAs from some Archaea are catalytically active", Proc Natl Acad Sci U S A, 96, pp.7803~7808 (1999)
- Kikovska E, "Eukaryotic RNase P RNA mediates cleavage in the absence of protein", Proc Natl Acad Sci U S A, 104, pp.2062~2067 (2007)
- Doersen CJ, "Characterization of an RNase P activity from HeLa cell mitochondria. Comparison with the cytosol RNase P activity", J Biol Chem, 260, pp.5942~5949 (1985)
- Rossmanith W, "Characterization of human mitochondrial RNase P: novel aspects in tRNA processing", Biochem Biophys Res Commun, 247, pp.234~241 (1998)
- Bartkiewicz M, "Identification and characterization of an RNA molecule that copurifies with RNase P activity from HeLa cells", Genes Dev, 3, pp.488~499 (1989)
- Huntzinger E, "Gene silencing by microRNAs: contributions of translational repression and mRNA decay", Nat Rev Genet, 12, pp.99~110 (2011)
- Filipowicz W, "Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?", Nat Rev Genet, 9, pp.102~114 (2008)
- Fabian MR, "Regulation of mRNA translation and stability by microRNAs", Annu Rev Biochem, 79, pp.351~379 (2010)
- Bartel DP, "MicroRNAs: target recognition and regulatory functions", Cell, 136, pp.215~233 (2009)
- Kim VN, "Biogenesis of small RNAs in animals", Nat Rev Mol Cell Biol, 10, pp.126~139 (2009)
- Newman MA, "Emerging paradigms of regulated microRNA processing", Genes Dev, 24, pp.1086~1092 (2010)
- Kloosterman WP, "The diverse functions of microRNAs in animal development and disease", Dev Cell, 11, pp.441~450 (2006)
- Lingor P, "Apoptosome: An up-and-coming therapeutical tool", pp.95~117 (2010), Springer Netherlands
- Catalanotto C, "MicroRNA in Control of Gene Expression: An Overview of Nuclear Functions", Int J Mol Sci, 17 (2016)
- Yao S, "MicroRNA biogenesis and their functions in regulating stem cell potency and differentiation", Biol Proced Online, 18, pp.8~ (2016)
- Bushati N, "microRNA functions", Annu Rev Cell Dev Biol, 23, pp.175~205 (2007)
- Abdelmohsen K, "Noncoding RNA control of cellular senescence", Wiley Interdiscip Rev RNA, 6, pp.615~629 (2015)
- Rottiers V, "MicroRNAs in metabolism and metabolic disorders", Nat Rev Mol Cell Biol, 13, pp.239~250 (2012)
- Shah MY, "microRNA Therapeutics in Cancer - An Emerging Concept", EBioMedicine, 12, pp.34~42 (2016)
- Saeidimehr S, "MicroRNA-Based Linkage between Aging and Cancer: from Epigenetics View Point", Cell J, 18, pp.117~126 (2016)
- Das S, "Nuclear miRNA regulates the mitochondrial genome in the heart", Circ Res, 110, pp.1596~1603 (2012)
- Sripada L, "Mitochondria : one of the destinations of miRNAs", Mitochondrion, 12, pp.593~599 (2012)
- Bienertova-Vasku J, "The role of microRNAs in mitochondria in cancer", Cancer Lett, 336, pp.1~7 (2013)
- Barrey E, "Pre-microRNA and mature microRNA in human mitochondria", PLoS One, 6, pp.e20220~ (2011)
- Srinivasan H, "Mitochondrial miRNA (MitomiR): a new player in cardiovascular health", Can J Physiol Pharmacol, 93, pp.855~861 (2015)
- Zhang X, "MicroRNA directly enhances mitochondrial translation during muscle differentiation", Cell, 158, pp.607~619 (2014)
- Bandiera S, "MitomiRs delineating the intracellular localization of microRNAs at mitochondria", Free Radic Biol Med, 64, pp.12~19 (2013)
- Duarte FV, "The Role of microRNAs in Mitochondria: Small Players Acting Wide", Genes (Basel), 5, pp.865~886 (2014)
- Das S, "miR-181c regulates the mitochondrial genome, bioenergetics, and propensity for heart failure in vivo", PLoS One, 9, pp.e96820~ (2014)
- Dasgupta N, "miRNAs in mtDNA-less cell mitochondria", Cell Death Discov, 1, pp.15004~ (2015)
- Bukeirat M, "MiR-34a regulates blood-brain barrier permeability and mitochondrial function by targeting cytochrome c", J Cereb Blood Flow Metab, 36, pp.387~392 (2016)
- Jagannathan R, "Translational Regulation of the Mitochondrial Genome Following Redistribution of Mitochondrial MicroRNA in the Diabetic Heart", Circ Cardiovasc Genet, 8, pp.785~802 (2015)
- Guttman M, "Modular regulatory principles of large non-coding RNAs", Nature, 482, pp.339~346 (2012)
- Kretz M, "Control of somatic tissue differentiation by the long non-coding RNA TINCR", Nature, 493, pp.231~235 (2013)
- Guttman M, "Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals", Nature, 458, pp.223~227 (2009)
- Khalil AM, "Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression", Proc Natl Acad Sci U S A, 106, pp.11667~11672 (2009)
- Rinn JL, "Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs", Cell, 129, pp.1311~1323 (2007)
- Mattick JS, "Non-coding RNA", Hum Mol Genet, 15(1), pp.R17~R29 (2006)
- Carpenter S, "A long noncoding RNA mediates both activation and repression of immune response genes", Science, 341, pp.789~792 (2013)
- Huarte M, "A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response", Cell, 142, pp.409~419 (2010)
- Salinas T, "The voltage-dependent anion channel, a major component of the tRNA import machinery in plant mitochondria", Proc Natl Acad Sci U S A, 103, pp.18362~18367 (2006)
- O'Brien TW, "The general occurrence of 55 S ribosomes in mammalian liver mitochondria", J Biol Chem, 246, pp.3409~3417 (1971)
- Grivell LA, "Isolation of yeast mitochondrial ribosomes highly active in protein synthesis", Biochim Biophys Acta, 247, pp.91~103 (1971)
- Sharma MR, "Structure of a mitochondrial ribosome with minimal RNA", Proc Natl Acad Sci U S A, 106, pp.9637~9642 (2009)
- Sharma MR, "Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins", Cell, 115, pp.97~108 (2003)
- Smits P, "Reconstructing the evolution of the mitochondrial ribosomal proteome", Nucleic Acids Res, 35, pp.4686~4703 (2007)
- Mears JA, "A structural model for the large subunit of the mammalian mitochondrial ribosome", J Mol Biol, 358, pp.193~212 (2006)
- Agrawal RK, "Structural aspects of mitochondrial translational apparatus", Curr Opin Struct Biol, 22, pp.797~803 (2012)
- Cha MY, "Mitochondriaspecific accumulation of amyloid beta induces mitochondrial dysfunction leading to apoptotic cell death", PLoS One, 7, pp.e34929~ (2012)
- Reddy PH, "Amyloid beta, mitochondrial structural and functional dynamics in Alzheimer's disease", Exp Neurol, 218, pp.286~292 (2009)
- Canugovi C, "Base excision DNA repair levels in mitochondrial lysates of Alzheimer's disease", Neurobiol Aging, 35, pp.1293~1300 (2014)
- Marongiu R, "Mutant Pink1 induces mitochondrial dysfunction in a neuronal cell model of Parkinson's disease by disturbing calcium flux", J Neurochem, 108, pp.1561~1574 (2009)
- Mortiboys H, "Mitochondrial function and morphology are impaired in parkin-mutant fibroblasts", Ann Neurol, 64, pp.555~565 (2008)
- Canet-Aviles RM, "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, pp.9103~9108 (2004)
- Devi L, "Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain", J Biol Chem, 283, pp.9089~9100 (2008)
- Ide T, "Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction", Circ Res, 88, pp.529~535 (2001)
- Ballinger SW, "Mitochondrial integrity and function in atherogenesis", Circulation, 106, pp.544~549 (2002)
- Romanello V, "Mitochondrial fission and remodelling contributes to muscle atrophy", EMBO J, 29, pp.1774~1785 (2010)
- Crescenzo R, "Mitochondrial efficiency and insulin resistance", Front Physiol, 5, pp.512~ (2014)
- Mathur S, "Structural alterations of skeletal muscle in copd", Front Physiol, 5, pp.104~ (2014)
- Antunes F, "Fasting boosts sensitivity of human skin melanoma to cisplatin-induced cell death", Biochem Biophys Res Commun (2016)
- Katsetos CD, "Mitochondrial dysfunction in gliomas", Semin Pediatr Neurol, 20, pp.216~227 (2013)
- Trifunovic A, "Premature ageing in mice expressing defective mitochondrial DNA polymerase", Nature, 429, pp.417~423 (2004)
- Sastre J, "Mitochondria, oxidative stress and aging", Free Radic Res, 32, pp.189~198 (2000)
- Smirnov AV, "Specific features of 5S rRNA structure - its interactions with macromolecules and possible functions", Biochemistry (Mosc), 73, pp.1418~1437 (2008)
- Tonin Y, "Modeling of antigenomic therapy of mitochondrial diseases by mitochondrially addressed RNA targeting a pathogenic point mutation in mitochondrial DNA", J Biol Chem, 289, pp.13323~13334 (2014)
