Abstract
Mitochondria currently appear to be a major destination for the RNA trafficking and localization processes that control and coordinate gene expression in living cells. A large set of messenger RNAs derived from the nuclear genome is translated at the mitochondrial surface, while an increasing series of noncoding RNAs has been reported to localize in the organelles, including microRNAs, additional small noncoding RNAs, transfer RNAs, and long noncoding RNAs. These RNA species contribute to mitochondrial functions and control of organellar gene expression, but mitochondria might also store and release noncoding RNAs of nuclear origin having cytosolic targets. Conversely, data have emerged implying that small and long noncoding regulatory RNAs are generated within the organelles from the mitochondrial genome. Some of them nevertheless appeared to localize to the nucleus or were recovered in body fluids. Integrating all reported data leads to an intricate picture of multidirectional RNA trafficking and intercompartment communication that can be related to cellular homeostasis, cell differentiation, pathogenesis, or disease. However, a number of facets in this amazing picture are still a matter of debate, as the mechanisms underlying nucleic acid translocation through the mitochondrial membranes remain difficult to assess and the widespread presence of mitochondrial DNA pseudo-sequences in the nuclear genome can make the origin of some transcripts confusing. A detailed panorama of the reported mitochondrial noncoding RNAs and of the questions raised by the data is developed here in relation to major mitochondrial processes.
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Akashi K, Sakurai K, Hirayama J, Fukuzawa H, Ohyama K (1996) Occurrence of nuclear-encoded tRNAIle in mitochondria of the liverwort Marchantia polymorpha. Curr Genet 30:181–185
Akashi K, Hirayama J, Takenaka M, Yamaoka S, Suyama Y, Fukuzawa H, Ohyama K (1997) Accumulation of nuclear-encoded tRNAThr (AGU) in mitochondria of the liverwort Marchantia polymorpha. Biochim Biophys Acta 1350:262–266
Akashi K, Takenaka M, Yamaoka S, Suyama Y, Fukuzawa H, Ohyama K (1998) Coexistence of nuclear DNA-encoded tRNAVal(AAC) and mitochondrial DNA-encoded tRNAVal(UAC) in mitochondria of a liverwort Marchantia polymorpha. Nucleic Acids Res 26:2168–2172
Amunts A, Brown A, Toots J, Scheres SHW, Ramakrishnan V (2015) Ribosome the structure of the human mitochondrial ribosome. Science 348:95–98
Asin-Cayuela J, Gustafsson CM (2007) Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem Sci 32:111–117
Baev V, Milev I, Naydenov M, Vachev T, Apostolova E, Mehterov N, Gozmanva M, Minkov G, Sablok G, Yahubyan G (2014) Insight into small RNA abundance and expression in high- and low-temperature stress response using deep sequencing in Arabidopsis. Plant Physiol Biochem 84:105–114
Baleva M, Gowher A, Kamenski P, Tarassov I, Entelis N, Masquida B (2015) A moonlighting human protein is involved in mitochondrial import of tRNA. Int J Mol Sci 16:9354–9367
Bandiera S, Ruberg S, Girard M, Cagnard N, Hanein S, Chretien D, Munnich A, Lyonnet S, Henrion-Caude A (2011) Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 6:e20746
Bandiera S, Mategot R, Girard M, Demongeot J, Henrion-Caude A (2013) MitomiRs delineating the intracellular localization of microRNAs at mitochondria. Free Radic Biol Med 64:12–19
Baradan R, Hollander JM, Das S (2017) Mitochondrial miRNAs in diabetes: just the tip of the iceberg. Can J Physiol Pharmacol 95:1156–1162
Barman B, Bhattacharyya SN (2015) mRNA targeting to endoplasmic reticulum precedes ago protein interaction and microRNA (miRNA)-mediated translation repression in mammalian cells. J Biol Chem 290:24650–24656
Barrey E, Saint-Auret G, Bonnamy B, Damas D, Boyer O, Gidrol X (2011) Pre-microRNA and mature microRNA in human mitochondria. PLoS One 6:e20220
Beitzinger M, Peters L, Zhu JY, Kremmer E, Meister G (2007) Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol 4:76–84
Bennett JL, Clayton DA (1990) Efficient site-specific cleavage by RNase MRP requires interaction with two evolutionarily conserved mitochondrial RNA sequences. Mol Cell Biol 10:2191–2201
Bhattacharyya SN, Chatterjee S, Adhya S (2002) Mitochondrial RNA import in Leishmania tropica: aptamers homologous to multiple tRNA domains that interact cooperatively or antagonistically at the inner membrane. Mol Cell Biol 22:4372–4382
Bhattacharyya SN, Chatterjee S, Goswami S, Tripathi G, Dey SN, Adhya S (2003) “Ping-pong” interactions between mitochondrial tRNA import receptors within a multiprotein complex. Mol Cell Biol 23:5217–5224
Bian Z, Li LM, Tang R, Hou DX, Chen X, Zhang CY, Zen K (2010) Identification of mouse liver mitochondria-associated miRNAs and their potential biological functions. Cell Res 20:1076–1078
Bianchesssi V, Badi I, Bertolotti M, Nigro P, D’Alessandra Y, Capogrossi MC, Zanobini M, Pompilio G, Raucci A, Lauri A (2015) The mitochondrial lncRNA ASncmtRNA-2 is induced in aging and replicative senescence in endothelial cells. J Mol Cell Cardiol 81:62–70
Boesch P, Ibrahim N, Paulus F, Cosset A, Tarasenko V, Dietrich A (2009) Plant mitochondria possess a short-patch base excision DNA repair pathway. Nucleic Acids Res 37:5690–5700
Boesch P, Ibrahim N, Dietrich A, Lightowlers RN (2010) Membrane association of mitochondrial DNA facilitates base excision repair in mammalian mitochondria. Nucleic Acids Res 38:1478–1488
Bonen L (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8:26–34
Borgna V, Villegas J, Burzio VA, Belmar S, Araya M, Jeldes E, Lobos-Gonzalez L, Silva V, Villota C, Oliveira-Cruz L, Lopez C, Socias T, Castillo O, Burzio LO (2017) Mitochondrial ASncmtRNA-1 and ASncmtRNA-2 as potent targets to inhibit tumor growth and metastasis in the RenCa murine renal adenocarcinoma model. Oncotarget 8:43692–43708
Borralho PM, Rodrigues CM, Steer CJ (2015) microRNAs in mitochondria: an unexplored niche. Adv Exp Med Biol 887:31–51
Bouzaidi-Tiali N, Aeby E, Charriere F, Pusnik M, Schneider A (2007) Elongation factor 1a mediates the specificity of mitochondrial tRNA import in T. brucei. EMBO J 26:4302–4312
Brandina I, Graham J, Lemaitre-Guillier C, Entelis N, Krasheninnikov I, Sweetlove L, Tarassov I, Martin RP (2006) Enolase takes part in a macromolecular complex associated to mitochondria in yeast. Biochim Biophys Acta 1757:1217–1228
Brandina I, Smirnov A, Kolesnikova O, Entelis N, Krasheninnikov IA, Martin RP, Tarassov I (2007) tRNA import into yeast mitochondria is regulated by the ubiquitin-proteasome system. FEBS Lett 581:4248–4254
Breving K, Esquela-Kerscher A (2010) The complexities of microRNA regulation: mirandering around the rules. Int J Biochem Cell Biol 42:1316–1329
Brown GG, Colas des Francs-Small C, Ostersetzer-Biran O (2014) Group II intron splicing factors in plant mitochondria. Front Plant Sci 5:35
Bunch H (2017) Gene regulation of mammalian long non-coding RNA. Mol Gen Genomics 293:1–15. https://doi.org/10.1007/s00438-00017-01370-00439
Burger G, Zhu Y, Littlejohn TG, Greenwood SJ, Schnare MN, Lang BF, Gray MW (2000) Complete sequence of the mitochondrial genome of Tetrahymena pyriformis and comparison with Paramecium aurelia mitochondrial DNA. J Mol Biol 297:365–380
Burger G, Gray MW, Forget L, Lang BF (2013) Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol Evol 5:418–438
Burzio VA, Villota C, Villegas J, Landerer E, Boccardo E, Villa LL, Martinez R, Lopez C, Gaete F, Toro V, Rodriguez X, Burzio LO (2009) Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells. Proc Natl Acad Sci U S A 106:9430–9434
Buxbaum AR, Haimovich G, Singer RH (2015) In the right place at the right time: visualizing and understanding mRNA localization. Nat Rev Mol Cell Biol 16:95–109
Campbell CT, Kolesar JE, Kaufman BA (2012) Mitochondrial transcription factor a regulates mitochondrial transcription initiation, DNA packaging, and genome copy number. Biochim Biophys Acta 1819:921–929
Campo ML, Peixoto PM, Martinez-Caballero S (2017) Revisiting trends on mitochondrial mega-channels for the import of proteins and nucleic acids. J Bioenerg Biomembr 49:75–99
Cannon MV, Irwin MH, Pinkert CA (2015) Mitochondrially-imported RNA in drug discovery. Drug Dev Res 76:61–71
Carrer M, Liu N, Grueter CE, Williams AH, Frisard MI, Hulver MW, Bassel-Duby R, Olson EN (2012) Control of mitochondrial metabolism and systemic energy homeostasis by microRNAs 378 and 378. Proc Natl Acad Sci U S A 109:15330–15335
Ceci LR, Veronico P, Gallerani R (1996) Identification and mapping of tRNA genes on the Helianthus annuus mitochondrial genome. DNA Seq 6:159–166
Chang DD, Clayton DA (1987) A mammalian mitochondrial RNA processing activity contains nucleus-encoded RNA. Science 235:1178–1184
Chang DD, 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
Charriere F, Helgadottir S, Horn EK, Soll D, Schneider A (2006) Dual targeting of a single tRNA(Trp) requires two different tryptophanyl-tRNA synthetases in Trypanosoma brucei. Proc Natl Acad Sci U S A 103:6847–6852
Chatterjee S, Home P, Mukherjee S, Mahata B, Goswami S, Dhar G, Adhya S (2006) An RNA-binding respiratory component mediates import of type II tRNAs into Leishmania mitochondria. J Biol Chem 281:25270–25277
Chen LL (2016) Linking long noncoding RNA localization and function. Trends Biochem Sci 41:761–772
Chin A, Lecuyer E (2017) RNA localization: making its way to the center stage. Biochim Biophys Acta 1861:2956–2970
Chiu N, Chiu A, Suyama Y (1975) Native and imported transfer RNA in mitochondria. J Mol Biol 99:37–50
Colley SM, Leedman PJ (2009) SRA and its binding partners: an expanding role for RNA-binding coregulators in nuclear receptor-mediated gene regulation. Crit Rev Biochem Mol Biol 44:25–33
Comte C, Tonin Y, Heckel-Mager AM, Boucheham A, Smirnov A, Aure K, Lombes A, Martin RP, Entelis N, Tarassov I (2013) Mitochondrial targeting of recombinant RNAs modulates the level of a heteroplasmic mutation in human mitochondrial DNA associated with Kearns Sayre syndrome. Nucleic Acids Res 41:418–433
Crausaz Esseiva A, Maréchal-Drouard L, Cosset A, Schneider A (2004) The T-stem determines the cytosolic or mitochondrial localization of trypanosomal tRNAsMet. Mol Biol Cell 15:2750–2757
Cristodero M, Seebeck T, Schneider A (2010) Mitochondrial translation is essential in bloodstream forms of Trypanosoma brucei. Mol Microbiol 78:757–769
Dang YL, Martin NC (1993) Yeast mitochondrial RNase P. Sequence of the RPM2 gene and demonstration that its product is a protein subunit of the enzyme. J Biol Chem 268:19791–19796
Das S, Ferlito M, Kent OA, Fox-Talbot K, Wang R, Liu D, Raghavachari N, Yang Y, Wheelan SJ, Murphy E, Steenbergen C (2012) Nuclear miRNA regulates the mitochondrial genome in the heart. Circ Res 110:1596–1603
Das S, Bedja D, Campbell N, Dunkerly B, Chenna V, Maitra A, Steenbergen C (2014) miR-181c regulates the mitochondrial genome, bioenergetics, and propensity for heart failure in vivo. PLoS One 9:e96820
Dasgupta N, Peng Y, Tan Z, Ciraolo G, Wang D, Li R (2015) miRNAs in mtDNA-less cell mitochondria. Cell Death Discov 1:15004
de Gonzalo-Calvo D, Kenneweg F, Bang C, Toro R, van der Meer RW, Rijzewijk LJ, Smit JW, Lamb HJ, Llorente-Cortes V, Thum T (2016) Circulating long-non coding RNAs as biomarkers of left ventricular diastolic function and remodelling in patients with well-controlled type 2 diabetes. Sci Rep 6:37354
Delage L, Dietrich A, Cosset A, Maréchal-Drouard L (2003a) In vitro import of a nuclearly encoded tRNA into mitochondria of Solanum tuberosum. Mol Cell Biol 23:4000–4012
Delage L, Duchêne AM, Zaepfel M, Maréchal-Drouard L (2003b) The anticodon and the D-domain sequences are essential determinants for plant cytosolic tRNAVal import into mitochondria. Plant J 34:623–633
Dietrich A, Maréchal-Drouard L, Carneiro V, Cosset A, Small I (1996a) A single base change prevents import of cytosolic tRNAAla into mitochondria in transgenic plants. Plant J 10:913–918
Dietrich A, Small I, Cosset A, Weil JH, Maréchal-Drouard L (1996b) Editing and import: strategies for providing plant mitochondria with a complete set of functional transfer RNAs. Biochimie 78:518–529
Doersen CJ, Guerrier-Takada C, Altman S, 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
Dong Y, Yoshitomi T, Hu JF, Cui J (2017) Long noncoding RNAs coordinate functions between mitochondria and the nucleus. Epigen Chromatin 10:41
Dorn GW 2nd (2014) LIPCAR: a mitochondrial lnc in the noncoding RNA chain? Circ Res 114:1548–1550
Dörner M, Altmann M, Pääbo S, Mörl M (2001) Evidence for import of a lysyl-tRNA into marsupial mitochondria. Mol Biol Cell 12:2688–2698
Doucet-Beaupré H, Breton S, Chapman EG, Blier PU, Bogan AE, Stewart DT, Hoeh WR (2010) Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA. BMC Evol Biol 10:50
Duchêne AM, Maréchal-Drouard L (2001) The chloroplast-derived trnW and trnM-e genes are not expressed in Arabidopsis mitochondria. Biochem Biophys Res Commun 285:1213–1216
Duchêne AM, Pujol C, Maréchal-Drouard L (2009) Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet 55:1–18
Englmeier R, Pfeffer S, Forster F (2017) Structure of the human mitochondrial ribosome studied in situ by cryoelectron tomography. Structure 25:1574–1581
Entelis NS, Krasheninnikov IA, Martin RP, Tarassov IA (1996) Mitochondrial import of a yeast cytoplasmic tRNALys: possible roles of aminoacylation and modified nucleosides in subcellular partitioning. FEBS Lett 384:38–42
Entelis NS, Kieffer S, Kolesnikova OA, Martin RP, Tarassov IA (1998) Structural requirements of tRNALys for its import into yeast mitochondria. Proc Natl Acad Sci U S A 95:2838–2843
Entelis NS, Kolesnikova OA, Dogan S, Martin RP, Tarassov IA (2001) 5 S rRNA and tRNA import into human mitochondria. Comparison of in vitro requirements. J Biol Chem 276:45642–45653
Entelis N, Brandina I, Kamenski P, Krasheninnikov IA, Martin RP, 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
Esakova O, Krasilnikov AS (2010) Of proteins and RNA: the RNase P/MRP family. RNA 16:1725–1747
Esseiva AC, Naguleswaran A, Hemphill A, Schneider A (2004) Mitochondrial tRNA import in Toxoplasma gondii. J Biol Chem 279:42363–42368
Fang Y, Wu H, Zhang T, Yang M, Yin Y, Pan L, Yu X, Zhang X, Hu S, Al-Mssallem IS, Yu J (2012) A complete sequence and transcriptomic analyses of date palm (Phoenix dactylifera L.) mitochondrial genome. PLoS One 7:e37164
Forster AC, Altman S (1990) Similar cage-shaped structures for the RNA components of all ribonuclease P and ribonuclease MRP enzymes. Cell 62:407–409
Frechin M, Senger B, Braye 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 23:1119–1130
French NS, Norton JD (1997) Structure and functional properties of mouse VL30 retrotransposons. Biochim Biophys Acta 1352:33–47
Furukawa R, Yamada Y, Kawamura E, Harashima H (2015) Mitochondrial delivery of antisense RNA by MITO-porter results in mitochondrial RNA knockdown, and has a functional impact on mitochondria. Biomaterials 57:107–115
Fusté JM, Wanrooij S, Jemt E, Granycome CE, Cluett TJ, Shi Y, Atanassova N, Holt IJ, Gustafsson CM, Falkenberg M (2010) Mitochondrial RNA polymerase is needed for activation of the origin of light-strand DNA replication. Mol Cell 37:67–78
Gao Y, Chen ZY, Wang Y, Liu Y, Ma JX, Li YK (2017) Long non-coding RNA ASncmtRNA-2 is upregulated in diabetic kidneys and high glucose-treated mesangial cells. Exp Ther Med 13:581–587
Geiger J, Dalgaard LT (2017) Interplay of mitochondrial metabolism and microRNAs. Cell Mol Life Sci 74:631–646
Giegé R, Sissler M, Florentz C (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 26:5017–5035
Glover KE, Spencer DF, Gray MW (2001) Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem 276:639–648
Gobert A, Gutmann B, Taschner A, Gossringer M, Holzmann J, Hartmann RK, Rossmanith W, Giege P (2010) A single Arabidopsis organellar protein has RNase P activity. Nat Struct Mol Biol 17:740–744
Gold HA, Topper JN, Clayton DA, Craft J (1989) The RNA processing enzyme RNase MRP is identical to the Th RNP and related to RNase P. Science 245:1377–1380
Gowher A, Smirnov A, Tarassov I, Entelis N (2013) Induced tRNA import into human mitochondria: implication of a host aminoacyl-tRNA-synthetase. PLoS One 8:e66228
Greber BJ, Bieri P, Leibundgut M, Leitner A, Aebersold R, Boehringer D, Ban N (2015) Ribosome. The complete structure of the 55S mammalian mitochondrial ribosome. Science 348:303–308
Grewe F, Edger PP, Keren I, Sultan L, Pires JC, Ostersetzer-Biran O, Mower JP (2014) Comparative analysis of 11 Brassicales mitochondrial genomes and the mitochondrial transcriptome of Brassica oleracea. Mitochondrion 19 Pt B:135–143
Grimes BT, Sisay AK, Carroll HD, Cahoon AB (2014) Deep sequencing of the tobacco mitochondrial transcriptome reveals expressed ORFs and numerous editing sites outside coding regions. BMC Genomics 15:31
Gualberto JM, Mileshina D, Wallet C, Niazi AK, Weber-Lotfi F, Dietrich A (2014) The plant mitochondrial genome: dynamics and maintenance. Biochimie 100:107–120
Gustafsson CM, Falkenberg M, Larsson NG (2016) Maintenance and expression of mammalian mitochondrial DNA. Annu Rev Biochem 85:133–160
Gutmann B, Gobert A, Giege P (2012) PRORP proteins support RNase P activity in both organelles and the nucleus in Arabidopsis. Genes Dev 26:1022–1027
Hancock K, Hajduk SL (1990) The mitochondrial tRNAs of Trypanosoma brucei are nuclear-encoded. J Biol Chem 265:19208–19215
Hernandez-Cid A, Aguirre-Sampieri S, Diaz-Vilchis A, Torres-Larios A (2012) Ribonucleases P/MRP and the expanding ribonucleoprotein world. IUBMB Life 64:521–528
Holec S, Lange H, Kuhn K, Alioua M, Borner T, Gagliardi D (2006) Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol Cell Biol 26:2869–2876
Holec S, Lange H, Canaday J, Gagliardi D (2008) Coping with cryptic and defective transcripts in plant mitochondria. Biochim Biophys Acta 1779:566–573
Hollingsworth MJ, Martin NC (1986) RNase P activity in the mitochondria of Saccharomyces cerevisiae depends on both mitochondrion and nucleus-encoded components. Mol Cell Biol 6:1058–1064
Holzmann J, Frank P, Loffler E, Bennett KL, Gerner C, Rossmanith W (2008) RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135:462–474
Huang L, Mollet S, Souquere S, Le Roy F, Ernoult-Lange M, Pierron G, Dautry F, Weil D (2011) Mitochondria associate with P-bodies and modulate microRNA-mediated RNA interference. J Biol Chem 286:24219–24230
Hwang JY, Han GG, Park JY, Kim EM, An CM, Kang JH, Choi YJ, Kim EB (2016) Complete sequence and polymorphisms of female Ruditapes philippinarum (Mollusca: Bivalvia) mitochondria genome. Mitochondrial DNA A DNA Mapp Seq Anal 27:3462–3463
Ibrahim N, Handa H, Cosset A, Koulintchenko M, Konstantinov Y, Lightowlers RN, Dietrich A, Weber-Lotfi F (2011) DNA delivery to mitochondria: sequence specificity and energy enhancement. Pharm Res 28:2871–2882
Islam MS, Studer B, Byrne SL, Farrell JD, Panitz F, Bendixen C, Møller IM, Asp T (2013) The genome and transcriptome of perennial ryegrass mitochondria. BMC Genomics 14:202
Jagannathan R, Thapa D, Nichols CE, Shepherd DL, Stricker JC, Croston TL, Baseler WA, Lewis SE, Martinez I, Hollander JM (2015) Translational regulation of the mitochondrial genome following redistribution of mitochondrial microRNA in the diabetic heart. Circ Cardiovasc Genet 8:785–802
Jarrous N (2017) Roles of RNase P and its subunits. Trends Genet 33:594–603
Jash S, Adhya S (2011) Suppression of reactive oxygen species in cells with multiple mitochondrial DNA deletions by exogenous protein-coding RNAs. Mitochondrion 11:607–614
Jash S, Chowdhury T, Adhya S (2012) Modulation of mitochondrial respiratory capacity by carrier-mediated transfer of RNA in vivo. Mitochondrion 12:262–270
Jung KA, Lee S, Kwak MK (2017) NFE2L2/NRF2 activity is linked to mitochondria and AMP-activated protein kinase signaling in cancers through miR-181c/mitochondria-encoded cytochrome c oxidase regulation. Antioxid Redox Signal 27:945–961
Kamarajan BP, Sridhar J, Subramanian S (2012) In silico prediction of microRNAs in plant mitochondria. Int J Bioautomat 16:251–262
Kamenski P, Kolesnikova O, Jubenot V, Entelis N, Krasheninnikov IA, Martin RP, Tarassov I (2007) Evidence for an adaptation mechanism of mitochondrial translation via tRNA import from the cytosol. Mol Cell 26:625–637
Kamenski P, Smirnova E, Kolesnikova O, Krasheninnikov IA, Martin RP, Entelis N, Tarassov I (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
Kapushoc ST, Alfonzo JD, Simpson L (2002) Differential localization of nuclear-encoded tRNAs between the cytosol and mitochondrion in Leishmania tarentolae. RNA 8:57–68
Karicheva OZ, Kolesnikova OA, Schirtz T, Vysokikh MY, Mager-Heckel AM, Lombes A, Boucheham A, Krasheninnikov IA, Martin RP, Entelis N, Tarassov I (2011) Correction of the consequences of mitochondrial 3243A>G mutation in the MT-TL1 gene causing the MELAS syndrome by tRNA import into mitochondria. Nucleic Acids Res 39:8173–8186
Kim D, Sung YM, Park J, Kim S, Kim J, Park J, Ha H, Bae JY, Kim S, Baek D (2016) General rules for functional microRNA targeting. Nat Genet 48:1517–1526
Kim KM, Noh JH, Abdelmohsen K, Gorospe M (2017) Mitochondrial noncoding RNA transport. BMB Rep 50:164–174
Kiss T, Filipowicz W (1992) Evidence against a mitochondrial location of the 7-2/MRP RNA in mammalian cells. Cell 70:11–16
Kitow J, Derda AA, Beermann J, Kumarswarmy R, Pfanne A, Fendrich J, Lorenzen JM, Xiao K, Bavendiek U, Bauersachs J, Thum T (2016) Mitochondrial long noncoding RNAs as blood based biomarkers for cardiac remodeling in patients with hypertrophic cardiomyopathy. Am J Physiol Heart Circ Physiol 311:H707–H712
Klemm BP, Wu N, Chen Y, Liu X, Kaitany KJ, Howard MJ, Fierke CA (2016) The diversity of ribonuclease P: protein and RNA catalysts with analogous biological functions. Biomol Ther 6:E27
Klimenko ES, Mileikob VA, Morozkinb ES, Laktionovb PP, Konstantinov YM (2011) Study of DNA import and export in potato (Solanum tuberosum) mitochondria using quantitative PCR. Biochem (Moscow) Suppl Ser A Membr Cell Biol 5:170–176
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 289:1931–1933
Kolesnikova O, Entelis N, Kazakova H, Brandina I, Martin RP, Tarassov I (2002) Targeting of tRNA into yeast and human mitochondria: the role of anticodon nucleotides. Mitochondrion 2:95–107
Kolesnikova OA, Entelis NS, Jacquin-Becker C, Goltzene F, Chrzanowska-Lightowlers ZM, Lightowlers RN, Martin RP, Tarassov I (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
Kolesnikova O, Kazakova H, Comte C, Steinberg S, Kamenski P, Martin RP, Tarassov I, Entelis N (2010) Selection of RNA aptamers imported into yeast and human mitochondria. RNA 16:926–941
Koley S, Adhya S (2013) A voltage-gated pore for translocation of tRNA. Biochem Biophys Res Commun 439:23–29
Konstantinov YM, Dietrich A, Weber-Lotfi F, Ibrahim N, Klimenko ES, Tarasenko VI, Bolotova TA, Koulintchenko MV (2016) DNA import into mitochondria. Biochem Mosc 81:1044–1056
Koulintchenko M, Konstantinov Y, Dietrich A (2003) Plant mitochondria actively import DNA via the permeability transition pore complex. EMBO J 22:1245–1254
Koulintchenko M, Temperley RJ, Mason PA, Dietrich A, Lightowlers RN (2006) Natural competence of mammalian mitochondria allows the molecular investigation of mitochondrial gene expression. Hum Mol Genet 15:143–154
Kren BT, Wong PY, Sarver A, Zhang X, Zeng Y, Steer CJ (2009) MicroRNAs identified in highly purified liver-derived mitochondria may play a role in apoptosis. RNA Biol 6:65–72
Kumar R, Maréchal-Drouard L, Akama K, Small I (1996) Striking differences in mitochondrial tRNA import between different plant species. Mol Gen Genet 252:404–411
Kumarswamy R, Bauters C, Volkmann I, Maury F, Fetisch J, Holzmann A, Lemesle G, de Groote P, Pinet F, Thum T (2014) Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ Res 114:1569–1575
Laforest MJ, Delage L, Maréchal-Drouard L (2005) The T-domain of cytosolic tRNAVal, an essential determinant for mitochondrial import. FEBS Lett 579:1072–1078
Landerer E, Villegas J, Burzio VA, Oliveira L, Villota C, Lopez C, Restovic F, Martinez R, Castillo O, Burzio LO (2011) Nuclear localization of the mitochondrial ncRNAs in normal and cancer cells. Cell Oncol (Dordr) 34:297–305
Lechner M, Rossmanith W, Hartmann RK, Tholken C, Gutmann B, Giege P, Gobert A (2015) Distribution of ribonucleoprotein and protein-only RNase P in eukarya. Mol Biol Evol 32:3186–3193
Lesnik C, Golani-Armon A, Arava Y (2015) Localized translation near the mitochondrial outer membrane: an update. RNA Biol 12:801–809
Leucci E, Vendramin R, Spinazzi M, Laurette P, Fiers M, Wouters J, Radaelli E, Eyckerman S, Leonelli C, Vanderheyden K, Rogiers A, Hermans E, Baatsen P, Aerts S, Amant F, Van Aelst S, van den Oord J, de Strooper B, Davidson I, Lafontaine DL, Gevaert K, Vandesompele J, Mestdagh P, Marine JC (2016) Melanoma addiction to the long non-coding RNA SAMMSON. Nature 531:518–522
Leung AK (2015) The whereabouts of microRNA actions: cytoplasm and beyond. Trends Cell Biol 25:601–610
Leygue E (2007) Steroid receptor RNA activator (SRA1): unusual bifaceted gene products with suspected relevance to breast cancer. Nucl Recept Signal 5:e006
Li K, Smagula CS, Parsons WJ, Richardson JA, Gonzalez M, Hagler HK, Williams RS (1994) Subcellular partitioning of MRP RNA assessed by ultrastructural and biochemical analysis. J Cell Biol 124:871–882
Li H, Zhang X, Wang F, Zhou L, Yin Z, Fan J, Nie X, Wang P, Fu XD, Chen C, Wang DW (2016) MicroRNA-21 lowers blood pressure in spontaneous hypertensive rats by upregulating mitochondrial translation. Circulation 134:734–751
Lightowlers RN, Chrzanowska-Lightowlers ZM (2008) PPR (pentatricopeptide repeat) proteins in mammals: important aids to mitochondrial gene expression. Biochem J 416:e5–e6
Lithgow T, Schneider A (2010) Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc Lond Ser B Biol Sci 365:799–817
Liu TT, Zhu D, Chen W, Deng W, He H, He G, Bai B, Qi Y, Chen R, Deng XW (2013) A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa. Mol Plant 6:830–846
Lobos-Gonzalez L, Silva V, Araya M, Restovic F, Echenique J, Oliveira-Cruz L, Fitzpatrick C, Briones M, Villegas J, Villota C, Vidaurre S, Borgna V, Socias M, Valenzuela S, Lopez C, Socias T, Varas M, Diaz J, Burzio LO, Burzio VA (2016) Targeting antisense mitochondrial ncRNAs inhibits murine melanoma tumor growth and metastasis through reduction in survival and invasion factors. Oncotarget 7:58331–58350
Long Y, Wang X, Youmans DT, Cech TR (2017) How do lncRNAs regulate transcription? Sci Adv 3:eaao2110
Lu Q, Wierzbicki S, Krasilnikov AS, Schmitt ME (2010) Comparison of mitochondrial and nucleolar RNase MRP reveals identical RNA components with distinct enzymatic activities and protein components. RNA 16:529–537
Magalhaes PJ, Andreu AL, Schon EA (1998) Evidence for the presence of 5S rRNA in mammalian mitochondria. Mol Biol Cell 9:2375–2382
Mahapatra S, Adhya S (1996) Import of RNA into Leishmania mitochondria occurs through direct interaction with membrane-bound receptors. J Biol Chem 271:20432–20437
Mahapatra S, Ghosh S, Bera SK, Ghosh T, Das A, Adhya S (1998) The D arm of tRNATyr is necessary and sufficient for import into Leishmania mitochondria in vitro. Nucleic Acids Res 26:2037–2041
Mahata B, Bhattacharyya SN, Mukherjee S, Adhya S (2005) Correction of translational defects in patient-derived mutant mitochondria by complex-mediated import of a cytoplasmic tRNA. J Biol Chem 280:5141–5144
Mahata B, Mukherjee S, Mishra S, Bandyopadhyay A, Adhya S (2006) Functional delivery of a cytosolic tRNA into mutant mitochondria of human cells. Science 314:471–474
Mahato B, Jash S, Adhya S (2011) RNA-mediated restoration of mitochondrial function in cells harboring a Kearns Sayre syndrome mutation. Mitochondrion 11:564–574
Maida Y, Yasukawa M, Furuuchi M, Lassmann T, Possemato R, Okamoto N, Kasim V, Hayashizaki Y, Hahn WC, Masutomi K (2009) An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA. Nature 461:230–235
Makarova JA, Shkurnikov MU, Wicklein D, Lange T, Samatov TR, Turchinovich AA, Tonevitsky AG (2016) Intracellular and extracellular microRNA: an update on localization and biological role. Prog Histochem Cytochem 51:33–49
Maniataki E, Mourelatos Z (2005) Human mitochondrial tRNAMet is exported to the cytoplasm and associates with the Argonaute 2 protein. RNA 11:849–852
Maréchal-Drouard L, Guillemaut P, Cosset A, Arbogast M, Weber F, Weil JH, Dietrich A (1990) Transfer RNAs of potato (Solanum tuberosum) mitochondria have different genetic origins. Nucleic Acids Res 18:3689–3696
Marker C, Zemann A, Terhorst T, Kiefmann M, Kastenmayer JP, Green P, Bachellerie JP, Brosius J, Huttenhofer A (2002) Experimental RNomics: identification of 140 candidates for small non-messenger RNAs in the plant Arabidopsis thaliana. Curr Biol 12:2002–2013
Martin RP, Schneller JM, Stahl A, 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
Matsuda D, Dreher TW (2004) The tRNA-like structure of turnip yellow mosaic virus RNA is a 3′-translational enhancer. Virology 321:36–46
Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA, Shearwood AM, Haugen E, Bracken CP, Rackham O, Stamatoyannopoulos JA, Filipovska A, Mattick JS (2011) The human mitochondrial transcriptome. Cell 146:645–658
Michaelis G, Vahrenholz C, Pratje E (1990) Mitochondrial DNA of Chlamydomonas reinhardtii: the gene for apocytochrome b and the complete functional map of the 15.8 kb DNA. Mol Gen Genet 223:211–216
Milani L, Ghiselli F, Maurizii MG, Passamonti M (2011) Doubly uniparental inheritance of mitochondria as a model system for studying germ line formation. PLoS One 6:e28194
Mileshina D, Koulintchenko M, Konstantinov Y, Dietrich A (2011) Transfection of plant mitochondria and in organello gene integration. Nucleic Acids Res 39:e115
Miller DL, Martin NC (1983) Characterization of the yeast mitochondrial locus necessary for tRNA biosynthesis: DNA sequence analysis and identification of a new transcript. Cell 34:911–917
Mukherjee S, Basu S, Home P, Dhar G, Adhya S (2007) Necessary and sufficient factors for the import of transfer RNA into the kinetoplast mitochondrion. EMBO Rep 8:589–595
Mukherjee S, Mahata B, Mahato B, Adhya S (2008) Targeted mRNA degradation by complex-mediated delivery of antisense RNAs to intracellular human mitochondria. Hum Mol Genet 17:1292–1298
Mukherjee J, Mahato B, Adhya S (2014) Vesicular transport of a ribonucleoprotein to mitochondria. Biol Open 3:1083–1091
Murcha MW, Kubiszewski-Jakubiak S, Teixeira PF, Gügel IL, Kmiec B, Narsai R, Ivanova A, Megel C, Schock A, Kraus S, Berkowitz O, Glaser E, Philippar K, Maréchal-Drouard L, Soll J, Whelan J (2016) Plant-specific preprotein and amino acid transporter proteins are required for tRNA import into mitochondria. Plant Physiol 172:2471–2490
Nagao A, Suzuki T, Katoh T, Sakaguchi Y, Suzuki T (2009) Biogenesis of glutaminyl-mt tRNAGln in human mitochondria. Proc Natl Acad Sci U S A 106:16209–16214
Nguyen TT, Brenu EW, Staines DR, Marshall-Gradisnik SM (2014) MicroRNAs in the intracellular space, regulation of organelle specific pathways in health and disease. MicroRNA 3:98–107
Noh JH, Kim KM, Abdelmohsen K, Yoon JH, Panda AC, Munk R, Kim J, Curtis J, Moad CA, Wohler CM, Indig FE, de Paula W, Dudekula DB, De S, Piao Y, Yang X, Martindale JL, de Cabo R, Gorospe M (2016) HuR and GRSF1 modulate the nuclear export and mitochondrial localization of the lncRNA RMRP. Genes Dev 30:1224–1239
Noutsopoulos D, Markopoulos G, Vartholomatos G, Kolettas E, Kolaitis N, Tzavaras T (2010) VL30 retrotransposition signals activation of a caspase-independent and p53-dependent death pathway associated with mitochondrial and lysosomal damage. Cell Res 20:553–562
Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Ohyama K (1992) Transfer RNA genes in the mitochondrial genome from a liverwort, Marchantia polymorpha: the absence of chloroplast-like tRNAs. Nucleic Acids Res 20:3773–3777
Owen GI (2017) Cancer’s new Achilles’ heel? Oncotarget 8:55774–55775
Paris Z, Rubio MA, Lukes J, Alfonzo JD (2009) Mitochondrial tRNA import in Trypanosoma brucei is independent of thiolation and the Rieske protein. RNA 15:1398–1406
Patrushev M, Kasymov V, Patrusheva V, Ushakova T, Gogvadze V, Gaziev A (2004) Mitochondrial permeability transition triggers the release of mtDNA fragments. Cell Mol Life Sci 61:3100–3103
Patrushev M, Kasymov V, Patrusheva V, Ushakova T, Gogvadze V, Gaziev AI (2006) Release of mitochondrial DNA fragments from brain mitochondria of irradiated mice. Mitochondrion 6:43–47
Pfaff J, Meister G (2013) Argonaute and GW182 proteins: an effective alliance in gene silencing. Biochem Soc Trans 41:855–860
Picardi E, Horner DS, Chiara M, Schiavon R, Valle G, Pesole G (2010) Large-scale detection and analysis of RNA editing in grape mtDNA by RNA deep-sequencing. Nucleic Acids Res 38:4755–4767
Pinti MV, Hathaway QA, Hollander JM (2017) Role of microRNA in metabolic shift during heart failure. Am J Physiol Heart Circ Physiol 312:H33–H45
Posakony JW, England JM, Attardi G (1977) Mitochondrial growth and division during the cell cycle in HeLa cells. J Cell Biol 74:468–491
Pozzi A, Plazzi F, Milani L, Ghiselli F, Passamonti M (2017) SmithRNAs: could mitochondria “bend” nuclear regulation? Mol Biol Evol 34:1960–1973
Puranam RS, 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
Rackham O, Shearwood AM, Mercer TR, Davies SM, Mattick JS, Filipovska A (2011) Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA 17:2085–2093
Rassow J, Dekker PJ, van Wilpe S, Meijer M, Soll J (1999) The preprotein translocase of the mitochondrial inner membrane: function and evolution. J Mol Biol 286:105–120
Richly E, Leister D (2004) NUMTs in sequenced eukaryotic genomes. Mol Biol Evol 21:1081–1084
Rinehart J, Krett B, Rubio MA, Alfonzo JD, Söll D (2005) Saccharomyces cerevisiae Imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev 19:583–592
Rippo MR, Olivieri F, Monsurro V, Prattichizzo F, Albertini MC, Procopio AD (2014) MitomiRs in human inflamm-aging: a hypothesis involving miR-181a, miR-34a and miR-146a. Exp Gerontol 56:154–163
Rivas A, Burzio V, Landerer E, Borgna V, Gatica S, Avila R, Lopez C, Villota C, de la Fuente R, Echenique J, Burzio LO, Villegas J (2012) Determination of the differential expression of mitochondrial long non-coding RNAs as a noninvasive diagnosis of bladder cancer. BMC Urol 12:37
Ro S, Ma HY, Park C, Ortogero N, Song R, Hennig GW, Zheng H, Lin YM, Moro L, Hsieh JT, Yan W (2013) The mitochondrial genome encodes abundant small noncoding RNAs. Cell Res 23:759–774
Rorbach J, Gao F, Powell CA, D’Souza A, Lightowlers RN, Minczuk M, Chrzanowska-Lightowlers ZM (2016) Human mitochondrial ribosomes can switch their structural RNA composition. Proc Natl Acad Sci U S A 113:12198–12201
Rossmanith W (2012) Of P and Z: mitochondrial tRNA processing enzymes. Biochim Biophys Acta 1819:1017–1026
Rossmanith W, Karwan RM (1998) Characterization of human mitochondrial RNase P: novel aspects in tRNA processing. Biochem Biophys Res Commun 247:234–241
Rossmanith W, Tullo A, Potuschak T, Karwan R, Sbisa E (1995) Human mitochondrial tRNA processing. J Biol Chem 270:12885–12891
Rubio MAT, Hopper AK (2011) Transfer RNA travels from the cytoplasm to organelles. Wiley Interdiscip Rev RNA 2:802–817
Rubio MA, Rinehart JJ, Krett B, Duvezin-Caubet S, Reichert AS, Söll D, Alfonzo JD (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
Rurek M (2016) Participation of non-coding RNAs in plant organelle biogenesis. Acta Biochim Pol 63:653–663
Rusconi CP, Cech TR (1996) The anticodon is the signal sequence for mitochondrial import of glutamine tRNA in Tetrahymena. Genes Dev 10:2870–2880
Russo A, Cirulli C, Amoresano A, Pucci P, Pietropaolo C, Russo G (2008) Cis-acting sequences and trans-acting factors in the localization of mRNA for mitochondrial ribosomal proteins. Biochim Biophys Acta 1779:820–829
Salinas T, Schaeffer C, Maréchal-Drouard L, Duchêne AM (2005) Sequence dependence of tRNAGly import into tobacco mitochondria. Biochimie 87:863–872
Salinas T, Duchêne AM, Delage L, Nilsson S, Glaser E, Zaepfel M, Maréchal-Drouard L (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
Salinas T, Duchêne AM, Maréchal-Drouard L (2008) Recent advances in tRNA mitochondrial import. Trends Biochem Sci 33:320–329
Salinas T, Duby F, Larosa V, Coosemans N, Bonnefoy N, Motte P, Maréchal-Drouard L, Remacle C (2012) Co-evolution of mitochondrial tRNA import and codon usage determines translational efficiency in the green alga Chlamydomonas. PLoS Genet 8:e1002946
Salinas T, El Farouk-Ameqrane S, Ubrig E, Sauter C, Duchêne AM, Maréchal-Drouard L (2014) Molecular basis for the differential interaction of plant mitochondrial VDAC proteins with tRNAs. Nucleic Acids Res 42:9937–9948
Salinas-Giegé T, Giegé R, Giegé P (2015) tRNA biology in mitochondria. Int J Mol Sci 16:4518–4559
Sbicego S, Nabholz CE, Hauser R, Blum B, Schneider A (1998) In vivo import of unspliced tRNATyr containing synthetic introns of variable length into mitochondria of Leishmania tarentolae. Nucleic Acids Res 26:5251–5255
Schekman R (2010) Editorial expression of concern: a bifunctional tRNA import receptor from Leishmania mitochondria. Proc Natl Acad Sci U S A 107:9476
Schneider A (2011) Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu Rev Biochem 80:1033–1053
Schneider A, Maréchal-Drouard L (2000) Mitochondrial tRNA import: are there distinct mechanisms? Trends Cell Biol 10:509–513
Seidman D, Johnson D, Gerbasi V, Golden D, Orlando R, Hajduk S (2012) Mitochondrial membrane complex that contains proteins necessary for tRNA import in Trypanosoma brucei. J Biol Chem 287:8892–8903
Sharma A, Sharma A (2015) Plasmodium falciparum Mitochondria import tRNAs along with an active phenylalanyl-tRNA synthetase. Biochem J 465:459–469
Shearman JR, Sangsrakru D, Ruang-Areerate P, Sonthirod C, Uthaipaisanwong P, Yoocha T, Poopear S, Theerawattanasuk K, Tragoonrung S, Tangphatsornruang S (2014) Assembly and analysis of a male sterile rubber tree mitochondrial genome reveals DNA rearrangement events and a novel transcript. BMC Plant Biol 14:45
Shepherd DL, Hathaway QA, Pinti MV, Nichols CE, Durr AJ, Sreekumar S, Hughes KM, Stine SM, Martinez I, Hollander JM (2017) Exploring the mitochondrial microRNA import pathway through polynucleotide Phosphorylase (PNPase). J Mol Cell Cardiol 110:15–25
Shi X, Chen DH, Suyama Y (1994) A nuclear tRNA gene cluster in the protozoan Leishmania tarentolae and differential distribution of nuclear-encoded tRNAs between the cytosol and mitochondria. Mol Biochem Parasitol 65:23–37
Shinde S, Bhadra U (2015) A complex genome-microRNA interplay in human mitochondria. Biomed Res Int 2015:206382
Sieber F, Duchêne AM, Maréchal-Drouard L (2011) Mitochondrial RNA import from diversity of natural mechanisms to potential applications. Int Rev Cell Mol Biol 287:145–190
Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241
Small I, Maréchal-Drouard L, Masson J, Pelletier G, Cosset A, Weil JH, Dietrich A (1992) In vivo import of a normal or mutagenized heterologous transfer RNA into the mitochondria of transgenic plants: towards novel ways of influencing mitochondrial gene expression? EMBO J 11:1291–1296
Smirnov A, Tarassov I, Mager-Heckel AM, Letzelter M, Martin RP, Krasheninnikov IA, Entelis N (2008) Two distinct structural elements of 5S rRNA are needed for its import into human mitochondria. RNA 14:749–759
Smirnov A, Comte C, Mager-Heckel AM, Addis V, Krasheninnikov IA, Martin RP, Entelis N, Tarassov I (2010) Mitochondrial enzyme rhodanese is essential for 5 S ribosomal RNA import into human mitochondria. J Biol Chem 285:30792–30803
Smirnov A, Entelis N, Martin RP, Tarassov I (2011) Biological significance of 5S rRNA import into human mitochondria: role of ribosomal protein MRP-L18. Genes Dev 25:1289–1305
Song S, Jiang F, Yuan J, Guo W, Miao Y (2013) Exceptionally high cumulative percentage of NUMTs originating from linear mitochondrial DNA molecules in the Hydra magnipapillata genome. BMC Genomics 14:447
Srinivasan H, Das S (2015) Mitochondrial miRNA (MitomiR): a new player in cardiovascular health. Can J Physiol Pharmacol 93:855–861
Sripada L, Tomar D, Prajapati P, Singh R, Singh AK, Singh R (2012a) Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 7:e44873
Sripada L, Tomar D, Singh R (2012b) Mitochondria: one of the destinations of miRNAs. Mitochondrion 12:593–599
Sripada L, Singh K, Lipatova AV, Singh A, Prajapati P, Tomar D, Bhatelia K, Roy M, Singh R, Godbole MM, Chumakov PM, Singh R (2017) Hsa-miR-4485 regulates mitochondrial functions and inhibits the tumorigenicity of breast cancer cells. J Mol Med (Berl) 95:641–651
Stalder L, Heusermann W, Sokol L, Trojer D, Wirz J, Hean J, Fritzsche A, Aeschimann F, Pfanzagl V, Basselet P, Weiler J, Hintersteiner M, Morrissey DV, Meisner-Kober NC (2013) The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J 32:1115–1127
Stohl LL, Clayton DA (1992) Saccharomyces cerevisiae Contains an RNase MRP that cleaves at a conserved mitochondrial RNA sequence implicated in replication priming. Mol Cell Biol 12:2561–2569
Sultan LD, Mileshina D, Grewe F, Rolle K, Abudraham S, Glodowicz P, Niazi AK, Keren I, Shevtsov S, Klipcan L, Barciszewski J, Mower JP, Dietrich A, Ostersetzer-Biran O (2016) The reverse transcriptase/RNA maturase protein MatR is required for the splicing of various group II introns in Brassicaceae mitochondria. Plant Cell 28:2805–2829
Sun T, Bentolila S, Hanson MR (2016) The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci 21:962–973
Suyama Y (1967) The origins of mitochondrial ribonucleic acids in Tetrahymena pyriformis. Biochemistry 6:2829–2839
Suyama Y (1986) Two dimensional polyacrylamide gel electrophoresis analysis of Tetrahymena mitochondrial tRNA. Curr Genet 10:411–420
Takenaka M, Zehrmann A, Verbitskiy D, Hartel B, Brennicke A (2013) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352
Taliaferro JM, Wang ET, Burge CB (2014) Genomic analysis of RNA localization. RNA Biol 11:1040–1050
Tan T, Pach R, Crausaz Esseiva A, Ivens A, Schneider A (2002a) tRNAs in Trypanosoma brucei: genomic organization, expression, and mitochondrial import. Mol Cell Biol 22:3707–3717
Tan TH, Bochud-Allemann N, Horn EK, Schneider A (2002b) Eukaryotic-type elongator tRNAMet of Trypanosoma brucei becomes formylated after import into mitochondria. Proc Natl Acad Sci U S A 99:1152–1157
Tarassov I, Entelis N (1992) Mitochondrially-imported cytoplasmic tRNALys(CUU) of Saccharomyces cerevisiae: in vivo and in vitro targeting systems. Nucleic Acids Res 20:1277–1281
Tarassov I, Entelis N, Martin RP (1995a) An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA. J Mol Biol 245:315–323
Tarassov I, Entelis N, Martin RP (1995b) Mitochondrial import of a cytoplasmic lysine-tRNA in yeast is mediated by cooperation of cytoplasmic and mitochondrial lysyl-tRNA synthetases. EMBO J 14:3461–3471
Tarassov I, Kamenski P, Kolesnikova O, Karicheva O, Martin RP, Krasheninnikov IA, Entelis N (2007) Import of nuclear DNA-encoded RNAs into mitochondria and mitochondrial translation. Cell Cycle 6:2473–2477
Tonin Y, Heckel AM, Vysokikh M, Dovydenko I, Meschaninova M, Rotig A, Munnich A, Venyaminova A, Tarassov I, Entelis N (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
Topper JN, Clayton DA (1990a) Characterization of human MRP/Th RNA and its nuclear gene: full length MRP/Th RNA is an active endoribonuclease when assembled as an RNP. Nucleic Acids Res 18:793–799
Topper JN, Clayton DA (1990b) Secondary structure of the RNA component of a nuclear/mitochondrial ribonucleoprotein. J Biol Chem 265:13254–13262
Tschopp F, Charriere F, Schneider A (2011) In vivo study in Trypanosoma brucei links mitochondrial transfer RNA import to mitochondrial protein import. EMBO Rep 12:825–832
Val R, Wyszko E, Valentin C, Szymanski M, Cosset A, Alioua M, Dreher TW, Barciszewski J, Dietrich A (2011) Organelle trafficking of chimeric ribozymes and genetic manipulation of mitochondria. Nucleic Acids Res 39:9262–9274
Valach M, Burger G, Gray MW, Lang BF (2014) Widespread occurrence of organelle genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res 42:13764–13777
Valentino A, Calarco A, Di Salle A, Finicelli M, Crispi S, Calogero RA, Riccardo F, Sciarra A, Gentilucci A, Galderisi U, Margarucci S, Peluso G (2017) Deregulation of microRNAs mediated control of carnitine cycle in prostate cancer: molecular basis and pathophysiological consequences. Oncogene 36:6030–6040
Vargas JNS, Kar AN, Kowalak JA, Gale JR, Aschrafi A, Chen CY, Gioio AE, Kaplan BB (2016) Axonal localization and mitochondrial association of precursor microRNA 338. Cell Mol Life Sci 73:4327–4340
Vendramin R, Marine JC, Leucci E (2017) Non-coding RNAs: the dark side of nuclear-mitochondrial communication. EMBO J 36:1123–1133
Vidaurre S, Fitzpatrick C, Burzio VA, Briones M, Villota C, Villegas J, Echenique J, Oliveira-Cruz L, Araya M, Borgna V, Socias T, Lopez C, Avila R, Burzio LO (2014) Down-regulation of the antisense mitochondrial non-coding RNAs (ncRNAs) is a unique vulnerability of cancer cells and a potential target for cancer therapy. J Biol Chem 289:27182–27198
Viereck J, Thum T (2017) Circulating noncoding RNAs as biomarkers of cardiovascular disease and injury. Circ Res 120:381–399
Villegas J, Zarraga AM, Muller I, Montecinos L, Werner E, Brito M, Meneses AM, Burzio LO (2000) A novel chimeric mitochondrial RNA localized in the nucleus of mouse sperm. DNA Cell Biol 19:579–588
Villegas J, Araya P, Bustos-Obregon E, Burzio LO (2002a) Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells. Mol Hum Reprod 8:977–983
Villegas J, Muller I, Arredondo J, Pinto R, Burzio LO (2002b) A putative RNA editing from U to C in a mouse mitochondrial transcript. Nucleic Acids Res 30:1895–1901
Villegas J, Burzio V, Villota C, Landerer E, Martinez R, Santander M, Pinto R, Vera MI, Boccardo E, Villa LL, Burzio LO (2007) Expression of a novel non-coding mitochondrial RNA in human proliferating cells. Nucleic Acids Res 35:7336–7347
Villota C, Campos A, Vidaurre S, Oliveira-Cruz L, Boccardo E, Burzio VA, Varas M, Villegas J, Villa LL, Valenzuela PD, Socias M, Roberts S, Burzio LO (2012) Expression of mitochondrial non-coding RNAs (ncRNAs) is modulated by high risk human papillomavirus (HPV) oncogenes. J Biol Chem 287:21303–21315
Vincent T, Vingadassalon A, Ubrig E, Azeredo K, Srour O, Cognat V, Graindorge S, Salinas T, Marechal-Drouard L, Duchene AM (2017) A genome-scale analysis of mRNAs targeting to plant mitochondria: upstream AUGs in 5′-UTRs reduce mitochondrial association. Plant J 92(6):1132–1142. https://doi.org/10.1111/tpj.13749
Vinogradova E, Salinas T, Cognat V, Remacle C, Maréchal-Drouard L (2009) Steady-state levels of imported tRNAs in Chlamydomonas mitochondria are correlated with both cytosolic and mitochondrial codon usages. Nucleic Acids Res 37:1521–1528
Walker SC, Engelke DR (2008) A protein-only RNase P in human mitochondria. Cell 135:412–414
Wang WX, Springer JE (2015) Role of mitochondria in regulating microRNA activity and its relevance to the central nervous system. Neural Regen Res 10:1026–1028
Wang G, Chen HW, Oktay Y, Zhang J, Allen EL, Smith GM, Fan KC, Hong JS, French SW, McCaffery JM, Lightowlers RN, Morse HC 3rd, Koehler CM, Teitell MA (2010) PNPASE regulates RNA import into mitochondria. Cell 142:456–467
Wang G, Shimada E, Koehler CM, Teitell MA (2012a) PNPASE and RNA trafficking into mitochondria. Biochim Biophys Acta 1819:998–1007
Wang G, Shimada E, Zhang J, Hong JS, Smith GM, Teitell MA, Koehler CM (2012b) Correcting human mitochondrial mutations with targeted RNA import. Proc Natl Acad Sci U S A 109:4840–4845
Wang Y, Wang X, Deng W, Fan X, Liu TT, He G, Chen R, Terzaghi W, Zhu D, Deng XW (2014) Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. Mol Plant 7:514–527
Wang WX, Visavadiya NP, Pandya JD, Nelson PT, Sullivan PG, Springer JE (2015) Mitochondria-associated microRNAs in rat hippocampus following traumatic brain injury. Exp Neurol 265:84–93
Wang J, Meng X, Dobrovolskaya OB, Orlov YL, Chen M (2017) Non-coding RNAs and their roles in stress response in plants. Genomics Proteomics Bioinformatics 15:301–312
Weber-Lotfi F, Koulintchenko MV, Ibrahim N, Hammann P, Mileshina DV, Konstantinov YM, Dietrich A (2015) Nucleic acid import into mitochondria: new insights into the translocation pathways. Biochim Biophys Acta 1853:3165–3181
Weis BL, Schleiff E, Zerges W (2013) Protein targeting to subcellular organelles via mRNA localization. Biochim Biophys Acta 1833:260–273
Woischnik M, Moraes CT (2002) Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res 12:885–893
Wu Z, Cuthbert JM, Taylor DR, Sloan DB (2015a) The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes. Proc Natl Acad Sci U S A 112:10185–10191
Wu Z, Stone JD, Storchova H, Sloan DB (2015b) High transcript abundance, RNA editing, and small RNAs in intergenic regions within the massive mitochondrial genome of the angiosperm Silene noctiflora. BMC Genomics 16:938
Yamada Y, Furukawa R, Harashima H (2016) A dual-ligand liposomal system composed of a cell-penetrating peptide and a mitochondrial RNA aptamer synergistically facilitates cellular uptake and mitochondrial targeting. J Pharm Sci 105:1705–1713
Yamamura S, Imai-Sumida M, Tanaka Y, Dahiya R (2017) Interaction and cross-talk between non-coding RNAs. Cell Mol Life Sci 10:1007
Yang W, Wu JM, Bi AD, Ou-Yang YC, Shen HH, Chirn GW, Zhou JH, Weiss E, Holman EP, Liao DJ (2013) Possible formation of mitochondrial-RNA containing chimeric or trimeric RNA implies a post-transcriptional and post-splicing mechanism for RNA fusion. PLoS One 8:e77016
Yang KC, Yamada KA, Patel AY, Topkara VK, George I, Cheema FH, Ewald GA, Mann DL, Nerbonne JM (2014) Deep RNA sequencing reveals dynamic regulation of myocardial noncoding RNAs in failing human heart and remodeling with mechanical circulatory support. Circulation 129:1009–1021
Yoshionari S, Koike T, Yokogawa T, Nishikawa K, Ueda T, Miura K, Watanabe K (1994) Existence of nuclear-encoded 5S-rRNA in bovine mitochondria. FEBS Lett 338:137–142
Zelenka J, Jezek P (2016) Import of fluorescent RNA into mitochondria of living cells. Methods Mol Biol 1351:175–181
Zelenka J, Alan L, Jaburek M, Jezek P (2014) Import of desired nucleic acid sequences using addressing motif of mitochondrial ribosomal 5S-rRNA for fluorescent in vivo hybridization of mitochondrial DNA and RNA. J Bioenerg Biomembr 46:147–156
Zhang X, Zuo X, Yang B, Li Z, Xue Y, Zhou Y, Huang J, Zhao X, Zhou J, Yan Y, Zhang H, Guo P, Sun H, Guo L, Zhang Y, Fu XD (2014) MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 158:607–619
Zhang Z, Gao W, Long QQ, Zhang J, Li YF, Liu DC, Yan JJ, Yang ZJ, Wang LS (2017) Increased plasma levels of lncRNA H19 and LIPCAR are associated with increased risk of coronary artery disease in a Chinese population. Sci Rep 7:7491
Acknowledgments
We acknowledge the support of our work by the French Centre National de la Recherche Scientifique (CNRS, UPR2357), the University of Strasbourg, the Agence Nationale de la Recherche (grant numbers ANR-06-MRAR-037-02, ANR-09-BLAN-0240-01), and the Ministère de la Recherche et de l’Enseignement Supérieur (Investissements d’Avenir/Laboratoire d’Excellence MitoCross, grant number ANR-11-LABX-0057_MITOCROSS).
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Weber-Lotfi, F., Dietrich, A. (2018). Intercompartment RNA Trafficking in Mitochondrial Function and Communication. In: Cruz-Reyes, J., Gray, M. (eds) RNA Metabolism in Mitochondria. Nucleic Acids and Molecular Biology, vol 34. Springer, Cham. https://doi.org/10.1007/978-3-319-78190-7_4
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