Mitochondrial noncoding RNA-regulatory network in cardiovascular disease

Abstract

Mitochondrial function and integrity are vital for the maintenance of cellular homeostasis, particularly in high-energy demanding cells. Cardiomyocytes have a large number of mitochondria, which provide a continuous and bulk supply of the ATP necessary for cardiac mechanical function. More than 90% of the ATP consumed by the heart is derived from the mitochondrial oxidative metabolism. Decreased energy supply as the main consequence of mitochondrial dysfunction is closely linked to cardiovascular disease (CVD). The discovery of noncoding RNA (ncRNAs) in the mitochondrial compartment has changed the traditional view of molecular pathways involved in the regulatory network of CVD. Mitochondrial ncRNAs participate in controlling cardiovascular pathogenesis by regulating glycolysis, mitochondrial energy status, and the expression of genes involved in mitochondrial metabolism. Understanding the underlying mechanisms of the association between impaired mitochondrial function resulting from fluctuation in expression levels of ncRNAs and specific disease phenotype can aid in preventing and treating CVD. This review presents an overview of the role of mitochondrial ncRNAs in the complex regulatory network of the cardiovascular pathology. We will summarize and discuss (1) mitochondrial microRNAs (mitomiRs) and long noncoding RNAs (lncRNAs) encoded either by nuclear or mitochondrial genome which are involved in the regulation of mitochondrial metabolism; (2) the role of mitomiRs and lncRNAs in the pathogenesis of several CVD such as hypertension, cardiac hypertrophy, acute myocardial infarction and heart failure; (3) the biomarker and therapeutic potential of mitochondrial ncRNAs in CVD; (4) and the challenges inherent to their translation into clinical application.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    Aoi W, Naito Y, Mizushima K, Takanami Y, Kawai Y, Ichikawa H, Yoshikawa T (2010) The microRNA miR-696 regulates PGC-1α in mouse skeletal muscle in response to physical activity. Am J Physiol Endocrinol Metab 298:E799–806. https://doi.org/10.1152/ajpendo.00448.2009

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Aschrafi A, Schwechter AD, Mameza MG, Natera-Naranjo O, Gioio AE, Kaplan BB (2008) MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J Neurosci 28:12581–12590. https://doi.org/10.1523/JNEUROSCI.3338-08.20

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Bai XY, Ma Y, Ding R, Fu B, Shi S, Chen XM (2011) miR-335 and miR-34a promote renal senescence by suppressing mitochondrial antioxidative enzymes. J Am Soc Nephrol 22:1252–1261. https://doi.org/10.1681/ASN.2010040367

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Bandiera S, Rüberg S, Girard M, Cagnard N, Hanein S, Chrétien D, Munnich A, Lyonnet S, Henrion-Caude A (2011) Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 6:e20746. https://doi.org/10.1371/journal.pone.0020746

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Baars T, Skyschally A, Klein-Hitpass L, Cario E, Erbel R, Heusch G, Kleinbongard P (2014) microRNA expression and its potential role in cardioprotection by ischemic postconditioning in pigs. Pflugers Arch 466:1953–1961. https://doi.org/10.1007/s00424-013-1429-3

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Baradan R, Hollander JM, Das S (2017) Mitochondrial miRNAs in diabetes: just the tip of the iceberg. Can J Physiol Pharmacol 95:1156–1162. https://doi.org/10.1139/cjpp-2016-0580

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    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. https://doi.org/10.1371/journal.pone.0020220

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Bellera N, Barba I, Rodriguez-Sinovas A, Ferret E, Asín MA, Gonzalez-Alujas MT, Pérez-Rodon J, Esteves M, Fonseca C, Toran N, Garcia Del Blanco B, Pérez A, Garcia-Dorado D (2014) Single intracoronary injection of encapsulated antagomir-92a promotes angiogenesis and prevents adverse infarct remodeling. J Am Heart Assoc 3:e000946. https://doi.org/10.1161/JAHA.114.000946

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Boon RA, Dimmeler S (2015) MicroRNAs in myocardial infarction. Nat Rev Cardiol 12:135–142. https://doi.org/10.1038/nrcardio.2014.207

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Bostjancic E, Zidar N, Stajner D, Glavac D (2010) MicroRNA miR-1 is up-regulated in remote myocardium in patients with myocardial infarction. Folia Biol (Praha) 56:27–31

    CAS  Google Scholar 

  11. 11.

    Canfrán-Duque A, Rotllan N, Zhang X, Fernández-Fuertes M, Ramírez-Hidalgo C, Araldi E, Daimiel L, Busto R, Fernández-Hernando C, Suárez Y (2017) Macrophage deficiency of miR-21 promotes apoptosis, plaque necrosis, and vascular inflammation during atherogenesis. EMBO Mol Med 9:1244–1262. https://doi.org/10.15252/emmm.201607492

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Castellanos E, Lanning NJ (2019) Phosphorylation of OXPHOS machinery subunits: functional implications in cell biology and disease. Yale J Biol Med 92:523–531

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Cech TR, Steitz JA (2014) The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157:77–94. https://doi.org/10.1016/j.cell.2014.03.008

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Chen HS, Hsu CY, Chang YC, Chuang HY, Long CY, Hsieh TH, Tsai EM (2017) Benzyl butyl phthalate decreases myogenic differentiation of endometrial mesenchymal stem/stromal cells through miR-137-mediated regulation of PITX2. Sci Rep 7:186. https://doi.org/10.1038/s41598-017-00286-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Chen KH, Dasgupta A, Lin J, Potus F, Bonnet S, Iremonger J, Fu J, Mewburn J, Wu D, Dunham-Snary K, Theilmann AL, Jing ZC, Hindmarch C, Ormiston ML, Lawrie A, Archer SL (2018) Epigenetic dysregulation of the dynamin-related protein 1 binding partners MiD49 and MiD51 increases mitotic mitochondrial fission and promotes pulmonary arterial hypertension: mechanistic and therapeutic implications. Circulation 138:287–304. https://doi.org/10.1161/circulationaha.117.031258

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Chen PH, Shih CM, Chang WC, Cheng CH, Lin CW, Ho KH, Su PC, Chen KC (2014) Micro RNA-302b-inhibited E2F3 transcription factor is related to all trans retinoic acid-induced glioma cell apoptosis. J Neurochem 131:731–742. https://doi.org/10.1111/jnc.12820

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Chen W, Wang P, Lu Y, Jin T, Lei X, Liu M, Zhuang P, Liao J, Lin Z, Li B, Peng Y, Pan G, Lv X, Zhang H, Ou Z, Xie S, Lin X, Sun S, Ferrone S, Tannous BA, Ruan Y, Li J, Fan S (2019) Decreased expression of mitochondrial miR-5787 contributes to chemoresistance by reprogramming glucose metabolism and inhibiting MT-CO3 translation. Theranostics 9:5739–5754. https://doi.org/10.7150/thno.37556

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Chen Z, Li Y, Zhang H, Huang P, Luthra R (2010) Hypoxia-regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression. Oncogene 29:4362–4368. https://doi.org/10.1038/onc.2010

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Cheng M, Liu L, Lao Y, Liao W, Liao M, Luo X, Wu J, Xie W, Zhang Y, Xu N (2016) MicroRNA-181a suppresses parkin-mediated mitophagy and sensitizes neuroblastoma cells to mitochondrial uncoupler-induced apoptosis. Oncotarget 7:42274–42287. https://doi.org/10.18632/oncotarget.9786

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Chu X, Wang Y, Pang L, Huang J, Sun X, Chen X (2018) miR-130 aggravates acute myocardial infarction-induced myocardial injury by targeting PPAR-γ. J Cell Biochem 119:7235–7244. https://doi.org/10.1002/jcb.26903

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    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. https://doi.org/10.1371/journal.pone.0096820

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    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. https://doi.org/10.1161/circresaha.112.267732

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Das S, Kohr M, Dunkerly-Eyring B, Lee DI, Bedja D, Kent OA, Leung AK, Henao-Mejia J, Flavell RA, Steenbergen C (2017) Divergent effects of miR-181 family members on myocardial function through protective cytosolic and detrimental mitochondrial microRNA targets. J Am Heart Assoc 6:e004694. https://doi.org/10.1161/jaha.116.004694

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Dávalos A, Goedeke L, Smibert P, Ramírez CM, Warrier NP, Andreo U, Cirera-Salinas D, Rayner K, Suresh U, Pastor-Pareja JC, Esplugues E, Fisher EA, Penalva LO, Moore KJ, Suárez Y, Lai EC, Fernández-Hernando C (2011) miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci 108:9232–9237. https://doi.org/10.1073/pnas.1102281108

    Article  PubMed  Google Scholar 

  25. 25.

    Devaux Y, Zangrando J, Schroen B, Creemers EE, Pedrazzini T, Chang CP, Dorn GW, Thum T, Heymans S (2015) Long noncoding RNAs in cardiac development and ageing. Nat Rev Cardiol 12:415–425. https://doi.org/10.1038/nrcardio.2015.55

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Dikalov SI, Ungvari Z (2013) Role of mitochondrial oxidative stress in hypertension. Am J Physiol Heart Circ Physiol 305:H1417–1427. https://doi.org/10.1152/ajpheart.00089.2013

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Dong Y, Xu W, Liu C, Liu P, Li P, Wang K (2019) Reactive oxygen species related noncoding RNAs as regulators of cardiovascular diseases. Int J Biol Sci 15:680–687. https://doi.org/10.7150/ijbs.30464

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Dong Y, Yoshitomi T, Hu JF, Cui J (2017) Long noncoding RNAs coordinate functions between mitochondria and the nucleus. Epigenetics Chromatin 10:41. https://doi.org/10.1186/s13072-017-0149-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Duarte FV, Palmeira CM, Rolo AP (2014) The role of microRNAs in mitochondria: small players acting wide. Genes (Basel) 5:865–886. https://doi.org/10.3390/genes5040865

    CAS  Article  Google Scholar 

  30. 30.

    Duarte FV, Palmeira CM, Rolo AP (2015) The emerging role of MitomiRs in the pathophysiology of human disease. Adv Exp Med Biol 888:123–154. https://doi.org/10.1007/978-3-319-22671-2_8

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Duroux-Richard I, Roubert C, Ammari M, Présumey J, Grün JR, Häupl T, Grützkau A, Lecellier CH, Boitez V, Codogno P, Escoubet J, Pers YM, Jorgensen C, Apparailly F (2016) miR-125b controls monocyte adaptation to inflammation through mitochondrial metabolism and dynamics. Blood 128:3125–3136. https://doi.org/10.1182/blood-2016-02-697003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Eichner LJ, Perry MC, Dufour CR, Bertos N, Park M, St-Pierre J, Giguère V (2010) miR-378∗ mediates metabolic shift in breast cancer cells via the PGC-1β/ERRγ transcriptional pathway. Cell Metab 12:352–361. https://doi.org/10.1016/j.cmet.2010.09.002

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Eirin A, Lerman A, Lerman LO (2018) Enhancing mitochondrial health to treat hypertension. Curr Hypertens Rep 20:89. https://doi.org/10.1007/s11906-018-0889-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    El-Azzouzi H, Leptidis S, Dirkx E, Hoeks J, van Bree B, Brand K, McClellan EA, Poels E, Sluimer JC, van den Hoogenhof MM, Armand AS, Yin X, Langley S, Bourajjaj M, Olieslagers S, Krishnan J, Vooijs M, Kurihara H, Stubbs A, Pinto YM, Krek W, Mayr M, da Costa Martins PA, Schrauwen P, De Windt LJ (2013) The hypoxia-inducible microRNA cluster miR-199a∼ 214 targets myocardial PPARδ and impairs mitochondrial fatty acid oxidation. Cell Metab 18:341–354. https://doi.org/10.1016/j.cmet.2013.08.009

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Endo K, Naito Y, Ji X, Nakanishi M, Noguchi T, Goto Y, Nonogi H, Ma X, Weng H, Hirokawa G, Asada T, Kakinoki S, Yamaoka T, Fukushima Y, Iwai N (2013) MicroRNA 210 as a biomarker for congestive heart failure. Biol Pharm Bull 36:48–54. https://doi.org/10.1248/bpb.b12-00578

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Fan F, Sun A, Zhao H, Liu X, Zhang W, Jin X, Wang C, Ma X, Shen C, Zou Y, Hu K, Ge J (2013) MicroRNA-34a promotes cardiomyocyte apoptosis post myocardial infarction through down-regulating aldehyde dehydrogenase 2. Curr Pharm Des 19:4865–4873. https://doi.org/10.2174/13816128113199990325

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Fang G, Qi J, Huang L, Zhao X (2019) LncRNA MRAK048635_P1 is critical for vascular smooth muscle cell function and phenotypic switching in essential hypertension. Biosci Rep. https://doi.org/10.1042/bsr20182229

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Fitzpatrick C, Bendek MF, Briones M, Farfán N, Silva VA, Nardocci G, Montecino M, Boland A, Deleuze JF, Villegas J, Villota C, Silva V, Lobos-Gonzalez L, Borgna V, Barrey E, Burzio LO, Burzio VA (2019) Mitochondrial ncRNA targeting induces cell cycle arrest and tumor growth inhibition of MDA-MB-231 breast cancer cells through reduction of key cell cycle progression factors. Cell Death Dis 10:423. https://doi.org/10.1038/s41419-019-1649-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller KI, De Marzo AM, Van Eyk JE, Mendell JT, Dang CV (2009) c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458:762–765. https://doi.org/10.1038/nature07823

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Gao S, Tian X, Chang H, Sun Y, Wu Z, Cheng Z, Dong P, Zhao Q, Ruan J, Bu W (2018) Two novel lncRNAs discovered in human mitochondrial DNA using PacBio full-length transcriptome data. Mitochondrion 38:41–47. https://doi.org/10.1016/j.mito.2017.08.002

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Giuliani A, Cirilli I, Prattichizzo F, Mensà E, Fulgenzi G, Sabbatinelli J, Graciotti L, Olivieri F, Procopio AD, Tiano L, Rippo MR (2018) The mitomiR/Bcl-2 axis affects mitochondrial function and autophagic vacuole formation in senescent endothelial cells. Aging (Albany NY) 10:2855–2873. https://doi.org/10.18632/aging.101591

    CAS  Article  Google Scholar 

  42. 42.

    Goding CR (2016) Targeting the lncRNA SAMMSON reveals metabolic vulnerability in melanoma. Cancer Cell 29:619–621. https://doi.org/10.1016/j.ccell.2016.04.010

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Gomes CP, Spencer H, Ford KL, Michel LY, Baker AH, Emanueli C, Balligand JL, Devaux Y (2017) The function and therapeutic potential of long non-coding RNAs in cardiovascular development and disease. Mol Ther Nucleic Acids 8:494–507. https://doi.org/10.1016/j.omtn.2017.07.014

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Guan X, Wang L, Liu Z, Guo X, Jiang Y, Lu Y, Peng Y, Liu T, Yang B, Shan H, Zhang Y, Xu C (2016) miR-106a promotes cardiac hypertrophy by targeting mitofusin 2. J Mol Cell Cardiol 99:207–217. https://doi.org/10.1016/j.yjmcc.2016.08.016

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Hadas Y, Sultana N, Youssef E, Sharkar MTK, Kaur K, Chepurko E, Zangi L (2019) Optimizing modified mRNA in vitro synthesis protocol for heart gene therapy. Mol Ther Methods Clin Dev 14:300–305. https://doi.org/10.1016/j.omtm.2019.07.006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Hausenloy DJ, Heusch G (2019) Translating cardioprotection for patient benefit: the EU-CARDIOPROTECTION COST action. J Am Coll Cardiol 73:2001–2003. https://doi.org/10.1016/j.jacc.2019.03.020

    Article  PubMed  Google Scholar 

  47. 47.

    He R, Ding C, Yin P, He L, Xu Q, Wu Z, Shi Y, Su L (2019) MiR-1a-3p mitigates isoproterenol-induced heart failure by enhancing the expression of mitochondrial ND1 and COX1. Exp Cell Res 378:87–97. https://doi.org/10.1016/j.yexcr.2019.03.012

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Heger J, Schulz R, Euler G (2016) Molecular switches under TGFβ signalling during progression from cardiac hypertrophy to heart failure. Br J Pharmacol 173:3–14. https://doi.org/10.1111/bph.13344

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Huang LG, Li JP, Pang XM, Chen CY, Xiang HY, Feng LB, Su SY, Li SH, Zhang L, Liu JL (2015) Micro RNA-29c Correlates with neuroprotection induced by FNS by targeting both Birc2 and Bak1 in rat brain after stroke. CNS Neurosci Ther 21:496–503. https://doi.org/10.1111/cns.12383

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Hwang HW, Wentzel EA, Mendell JT (2007) A hexanucleotide element directs microRNA nuclear import. Science 315:97–100. https://doi.org/10.1126/science.1136235

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Jeong JH, Kang YC, Piao Y, Kang S, Pak YK (2017) miR-24-mediated knockdown of H2AX damages mitochondria and the insulin signaling pathway. Exp Mol Med 49:e313. https://doi.org/10.1038/emm.2016.174

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Jiang F, Zhou X, Huang J (2016) Long non-coding RNA-ROR mediates the reprogramming in cardiac hypertrophy. PLoS One 11:e0152767. https://doi.org/10.1371/journal.pone.0152767

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Jin L, Lin X, Yang L, Fan X, Wang W, Li S, Li J, Liu X, Bao M, Cui X, Yang J, Cui Q, Geng B, Cai J (2018) AK098656, A novel vascular smooth muscle cell–dominant long noncoding RNA, promotes hypertension. Hypertension 71:262–272. https://doi.org/10.1161/hypertensionaha.117.09651

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Jorge Ruiz-Orera M, Albà M (2019) Conserved regions in long non-coding RNAs contain abundant translation and protein–RNA interaction signatures. NAR Genom Bioinform 1:e2. https://doi.org/10.1093/nargab/lqz002

    Article  Google Scholar 

  55. 55.

    Jusic A, Devaux Y, EU-CardioRNA COST Action (CA17129) (2019) Noncoding RNAs in hypertension. Hypertension 74:477–492. https://doi.org/10.1161/hypertensionaha.119.13412

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Jusic A, Hajrulahovic A, Devaux Y (2019) Noncoding RNAs regulatory network in mitochondria. MitoFit Preprint Arch. https://doi.org/10.26124/mitofit:ea19.MiPSchool.0006

    Article  Google Scholar 

  57. 57.

    Kang T, Lu W, Xu W, Anderson L, Bacanamwo M, Thompson W, Chen YE, Liu D (2013) MicroRNA-27 (miR-27) targets prohibitin and impairs adipocyte differentiation and mitochondrial function in human adipose-derived stem cells. J Biol Chem 288:34394–34402. https://doi.org/10.1074/jbc.M113.514372

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Kar D, Bandyopadhyay A (2018) Targeting peroxisome proliferator activated receptor α (PPAR α) for the prevention of mitochondrial impairment and hypertrophy in cardiomyocytes. Cell Physiol Biochem 49:245–259. https://doi.org/10.1159/000492875

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    Karbiener M, Pisani DF, Frontini A, Oberreiter LM, Lang E, Vegiopoulos A, Mössenböck K, Bernhardt GA, Mayr T, Hildner F, Grillari J, Ailhaud G, Herzig S, Cinti S, Amri EZ, Scheideler M (2014) MicroRNA-26 family is required for human adipogenesis and drives characteristics of brown adipocytes. Stem Cells 32:1578–1590. https://doi.org/10.1002/stem.1603

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Kim KM, Noh JH, Abdelmohsen K, Gorospe M (2017) Mitochondrial noncoding RNA transport. BMB Rep 50:164–174. https://doi.org/10.5483/bmbrep.2017.50.4.013

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Kim YJ, Hwang SJ, Bae YC, Jung JS (2009) MiR-21 regulates adipogenic differentiation through the modulation of TGF-β signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells 27:3093–3102. https://doi.org/10.1002/stem.23

    CAS  Article  PubMed  Google Scholar 

  62. 62.

    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. https://doi.org/10.1161/circresaha.114.303915

    CAS  Article  PubMed  Google Scholar 

  63. 63.

    Latronico MV, Condorelli G (2009) MicroRNAs and cardiac pathology. Nat Rev Cardiol 6:419–429. https://doi.org/10.1038/nrcardio.2009.56

    CAS  Article  PubMed  Google Scholar 

  64. 64.

    Lee J, Harris AN, Holley CL, Mahadevan J, Pyles KD, Lavagnino Z, Scherrer DE, Fujiwara H, Sidhu R, Zhang J, Huang SC, Piston DW, Remedi MS, Urano F, Ory DS, Schaffer JE (2016) Rpl13a small nucleolar RNAs regulate systemic glucose metabolism. J Clin Invest 126:4616–4625. https://doi.org/10.1172/JCI88069

    Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    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. https://doi.org/10.1038/nature17161

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    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. https://doi.org/10.1161/circulationaha.116.023926

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Li HJ, Sun XM, Li ZK, Yin QW, Pang H, Pan JJ, Li X, Chen W (2017) LncRNA UCA1 promotes mitochondrial function of bladder cancer via the MiR-195/ARL2 signaling pathway. Cell Physiol Biochem 43:2548–2561. https://doi.org/10.1159/000484507

    CAS  Article  PubMed  Google Scholar 

  68. 68.

    Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P (2010) miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet 6:e1000795. https://doi.org/10.1371/journal.pgen.1000795

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Li J, Li Y, Jiao J, Wang J, Li Y, Qin D, Li P (2014) Mitofusin 1 is negatively regulated by microRNA 140 in cardiomyocyte apoptosis. Mol Cell Biol 34:1788–1799. https://doi.org/10.1128/MCB.00774-13

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Li SP, Liu B, Song B, Wang CX, Zhou YC (2015) miR-28 promotes cardiac ischemia by targeting mitochondrial aldehyde dehydrogenase 2 (ALDH2) in mus musculus cardiac myocytes. Eur Rev Med Pharmacol Sci 19:752–758

    PubMed  Google Scholar 

  71. 71.

    Li SZ, Hu YY, Zhao J, Zhao YB, Sun JD, Yang YF, Ji CC, Liu ZB, Cao WD, Qu Y, Liu WP, Cheng G, Fei Z (2014) MicroRNA-34a induces apoptosis in the human glioma cell line, A172, through enhanced ROS production and NOX2 expression. Biochem Biophys Res Commun 444:6–12. https://doi.org/10.1016/j.bbrc.2013.12.136

    CAS  Article  PubMed  Google Scholar 

  72. 72.

    Lin B, Feng DG, Xu J (2019) microRNA-665 silencing improves cardiac function in rats with heart failure through activation of the cAMP signaling pathway. J Cell Physiol 234:13169–13181. https://doi.org/10.1002/jcp.27987

    CAS  Article  PubMed  Google Scholar 

  73. 73.

    Lin Q, Gao Z, Alarcon RM, Ye J, Yun Z (2009) A role of miR-27 in the regulation of adipogenesis. FEBS J 6:2348–2358. https://doi.org/10.1111/j.1742-4658.2009.06967.x

    CAS  Article  Google Scholar 

  74. 74.

    Liu BL, Cheng M, Hu S, Wang S, Wang L, Tu X, Huang CX, Jiang H, Wu G (2018) Overexpression of miR-142-3p improves mitochondrial function in cardiac hypertrophy. Biomed Pharmacother 108:1347–1356. https://doi.org/10.1016/j.biopha.2018.09.146

    CAS  Article  PubMed  Google Scholar 

  75. 75.

    Liu JJ, Zhang H, Xing F, Tang B, Wu SL, Xuan L, Kang PF, Xu Q, Wang HJ, Zhang NR, Wang XJ (2018) MicroRNA-138 promotes proliferation and suppresses mitochondrial depolarization in human pulmonary artery smooth muscle cells through targeting TASK-1. Mol Med Rep 17:3021–3027. https://doi.org/10.3892/mmr.2017.8200

    CAS  Article  PubMed  Google Scholar 

  76. 76.

    Liu L, An X, Li Z, Song Y, Li L, Zuo S, Liu N, Yang G, Wang H, Cheng X, Zhang Y, Yang X, Wang J (2016) The H19 long noncoding RNA is a novel negative regulator of cardiomyocyte hypertrophy. Cardiovasc Res 111:56–65. https://doi.org/10.1093/cvr/cvw078

    CAS  Article  PubMed  Google Scholar 

  77. 77.

    Long J, Badal SS, Ye Z, Wang Y, Ayanga BA, Galvan DL, Green NH, Chang BH, Overbeek PA, Danesh FR (2016) Long noncoding RNA Tug1 regulates mitochondrial bioenergetics in diabetic nephropathy. J Clin Invest 126:4205–4218. https://doi.org/10.1172/JCI87927

    Article  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Lu Z, Li S, Zhao S, Fa X (2016) Upregulated miR-17 regulates hypoxia-mediated human pulmonary artery smooth muscle cell proliferation and apoptosis by targeting mitofusin 2. Med Sci Monit 22:3301–3308. https://doi.org/10.12659/msm.900487

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Ma C, Zhang C, Ma M, Zhang L, Zhang L, Zhang F, Chen Y, Cao F, Li M, Wang G, Shen T, Yao H, Liu Y, Pan Z, Song S, Zhu D (2017) MiR-125a regulates mitochondrial homeostasis through targeting mitofusin 1 to control hypoxic pulmonary vascular remodeling. J Mol Med (Berl) 95:977–993. https://doi.org/10.1007/s00109-017-1541-5

    CAS  Article  Google Scholar 

  80. 80.

    Macgregor-Das AM, Das S (2018) A microRNA’s journey to the center of the mitochondria. Am J Physiol Heart Circ Physiol 315:H206–H215. https://doi.org/10.1152/ajpheart.00714.2017

    CAS  Article  PubMed  Google Scholar 

  81. 81.

    Mance LG, Mawla I, Shell SM, Cahoon B (2020) Mitochondrial mRNA fragments are circularized in a human HEK cell line. Mitochondrion 51:1–6. https://doi.org/10.1016/j.mito.2019.11.002

    CAS  Article  PubMed  Google Scholar 

  82. 82.

    Marques FZ, Romaine SP, Denniff M, Eales J, Dormer J, Garrelds IM, Wojnar L, Musialik K, Duda-Raszewska B, Kiszka B, Duda M, Morris BJ, Samani NJ, Danser AJ, Bogdanski P, Zukowska-Szczechowska E, Charchar FJ, Tomaszewski M (2015) Signatures of mir-181a on the renal transcriptome and blood pressure. Mol Med 21:739–748. https://doi.org/10.2119/molmed.2015.00096

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Montgomery TA, Ruvkun G (2013) MicroRNAs visit the ER. Cell 153:511–512. https://doi.org/10.1016/j.cell.2013.04.014

    CAS  Article  PubMed  Google Scholar 

  84. 84.

    Murri M, el Azzouzi H (2018) MicroRNAs as regulators of mitochondrial dysfunction and obesity. Am J Physiol Heart Circ Physiol 315:H291–H302. https://doi.org/10.1152/ajpheart.00691.2017

    CAS  Article  PubMed  Google Scholar 

  85. 85.

    Nasci VL, Chuppa S, Griswold L, Goodreau KA, Dash RK, Kriegel AJ (2019) miR-21-5p regulates mitochondrial respiration and lipid content in H9C2 cells. Am J Physiol Heart Circ Physiol 316:H710–H721. https://doi.org/10.1152/ajpheart.00538.2017

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Nishi H, Ono K, Iwanaga Y, Horie T, Nagao K, Takemura G, Kinoshita M, Kuwabara Y, Mori RT, Hasegawa K, Kita T, Kimura T (2010) MicroRNA-15b modulates cellular ATP levels and degenerates mitochondria via Arl2 in neonatal rat cardiac myocytes. J Biol Chem 285:4920–4930. https://doi.org/10.1074/jbc.M109.082610

    CAS  Article  PubMed  Google Scholar 

  87. 87.

    Politz JC, Hogan EM, Pederson T (2009) MicroRNAs with a nucleolar location. RNA 15:1705–1715. https://doi.org/10.1261/rna.1470409

    CAS  Article  PubMed  Google Scholar 

  88. 88.

    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. https://doi.org/10.1261/rna.029405.111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Rech M, Kuhn AR, Lumens J, Carai P, van Leeuwen R, Verhesen W, Verjans R, Lecomte J, Liu Y, Luiken JJFP, Mohren R, Cillero-Pastor B, Heymans S, Knoops K, van Bilsen M, Schroen B (2019) AntagomiR-103 and -107 treatment affects cardiac function and metabolism. Mol Ther Nucleic Acids 14:424–437. https://doi.org/10.1016/j.omtn.2018.12.010

    CAS  Article  PubMed  Google Scholar 

  90. 90.

    Reddy S, Hu DQ, Zhao M, Blay E Jr, Sandeep N, Ong SG, Jung G, Kooiker KB, Coronado M, Fajardo G, Bernstein D (2017) miR-21 is associated with fibrosis and right ventricular failure. JCI Insight 2:91625. https://doi.org/10.1172/jci.insight.91625

    Article  PubMed  Google Scholar 

  91. 91.

    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. https://doi.org/10.1038/cr.2013.37

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  92. 92.

    Ru Q, Li WL, Xiong Q, Chen L, Tian X, Li CY (2018) Voltage-gated potassium channel blocker 4-aminopyridine induces glioma cell apoptosis by reducing expression of microRNA-10b-5p. Mol Biol Cell 29:1125–1136. https://doi.org/10.1091/mbc.E17-02-0120

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  93. 93.

    Ruan X, Li P, Chen Y, Shi Y, Pirooznia M, Seifuddin F, Suemizu H, Ohnishi Y, Yoneda N, Nishiwaki M, Shepherdson J, Suresh A, Singh K, Ma Y, Jiang CF, Cao H (2020) In vivo functional analysis of non-conserved human lncRNAs associated with cardiometabolic traits. Nat Commun 11:45. https://doi.org/10.1038/s41467-019-13688-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  94. 94.

    Salgado-Somoza A, Zhang L, Vausort M, Devaux Y (2017) The circular RNA MICRA for risk stratification after myocardial infarction. Int J Cardiol Heart Vasc 10(17):33–36. https://doi.org/10.1016/j.ijcha.2017.11.001

    Article  Google Scholar 

  95. 95.

    Santer L, López B, Ravassa S, Baer C, Riedel I, Chatterjee S, Moreno MU, González A, Querejeta R, Pinet F, Thum T, Díez J (2019) Circulating long noncoding RNA LIPCAR predicts heart failure outcomes in patients without chronic kidney disease. Hypertension 73:820–828. https://doi.org/10.1161/HYPERTENSIONAHA.118.12261

    CAS  Article  PubMed  Google Scholar 

  96. 96.

    Schulte C, Barwari T, Joshi A, Theofilatos K, Zampetaki A, Barallobre-Barreiro J, Singh B, Sörensen NA, Neumann JT, Zeller T, Westermann D, Blankenberg S, Marber M, Liebetrau C, Mayr M (2019) Comparative analysis of circulating non-coding RNAs versus protein biomarkers in the detection of myocardial injury. Circ Res 125:328–340. https://doi.org/10.1161/circresaha.119.314937

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  97. 97.

    Shaw TA, Singaravelu R, Powdrill MH, Nhan J, Ahmed N, Özcelik D, Pezacki JP (2018) MicroRNA-124 regulates fatty acid and triglyceride homeostasis. Science 10:149–157. https://doi.org/10.1016/j.isci.2018.11.028

    CAS  Article  Google Scholar 

  98. 98.

    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. https://doi.org/10.1016/j.yjmcc.2017.06.012

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  99. 99.

    Siasos G, Tsigkou V, Kosmopoulos M, Theodosiadis D, Simantiris S, Tagkou NM, Tsimpiktsioglou A, Stampouloglou PK, Oikonomou E, Mourouzis K, Philippou A, Vavuranakis M, Stefanadis C, Tousoulis D, Papavassiliou AG (2018) Mitochondria and cardiovascular diseases-from pathophysiology to treatment. Ann Transl Med 6:256. https://doi.org/10.21037/atm.2018.06.21

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  100. 100.

    Sirey TM, Ponting CP (2016) Insights into the post-transcriptional regulation of the mitochondrial electron transport chain. Biochem Soc trans 44:1491–1498. https://doi.org/10.1042/BST20160100

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  101. 101.

    Steenbergen C, Das S, Su J, Wong R, Murphy E (2009) Cardioprotection and altered mitochondrial adenine nucleotide transport. Basic Res Cardiol 104:149–156. https://doi.org/10.1007/s00395-009-0002-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  102. 102.

    Sun D, Li C, Liu J, Wang Z, Liu Y, Luo C, Chen Y, Wen S (2019) Expression profile of microRNAs in hypertrophic cardiomyopathy and effects of microRNA-20 in inducing cardiomyocyte hypertrophy through regulating gene MFN2. DNA Cell Biol 38:796–807. https://doi.org/10.1089/dna.2019.4731

    CAS  Article  PubMed  Google Scholar 

  103. 103.

    Thum T (2014) Noncoding RNAs and myocardial fibrosis. Nat Rev Cardiol 11:655–663. https://doi.org/10.1038/nrcardio.2014.125

    CAS  Article  PubMed  Google Scholar 

  104. 104.

    Tomasetti M, Neuzil J, Dong L (2014) MicroRNAs as regulators of mitochondrial function: role in cancer suppression. Biochim Biophys Acta 1840:1441–1453. https://doi.org/10.1016/j.bbagen.2013.09.002

    CAS  Article  PubMed  Google Scholar 

  105. 105.

    Vargas JN, 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. https://doi.org/10.1007/s00018-016-2270-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  106. 106.

    Vausort M, Wagner DR, Devaux Y (2014) Long noncoding RNAs in patients with acute myocardial infarction. Circ Res 115:668–677. https://doi.org/10.1161/circresaha.115.303836

    CAS  Article  PubMed  Google Scholar 

  107. 107.

    Vendramin R, Marine JC, Leucci E (2017) Non-coding RNAs: the dark side of nuclear–mitochondrial communication. EMBO J 36:1123–1133. https://doi.org/10.15252/embj.201695546

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Venkataraman S, Alimova I, Fan R, Harris P, Foreman N, Vibhakar R (2010) MicroRNA 128a increases intracellular ROS level by targeting Bmi-1 and inhibits medulloblastoma cancer cell growth by promoting senescence. PLoS One 5:e10748. https://doi.org/10.1371/journal.pone.0010748

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  109. 109.

    Villota C, Campos A, Vidaurre S, Oliveira-Cruz L, Boccardo E, Burzio VA, Varas M, Villegas J, Villa LL, Valenzuela PD, Socías 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. https://doi.org/10.1074/jbc.M111.326694

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Wang J, Jia Z, Zhang C, Sun M, Wang W, Chen P, Ma K, Zhang Y, Li X, Zhou C (2014) miR-499 protects cardiomyocytes from H2O2-induced apoptosis via its effects on Pdcd4 and Pacs2. RNA Biol 11:339–350. https://doi.org/10.4161/rna.28300

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Wang J, Wu M, Wen J, Yang K, Li M, Zhan X, Feng L, Li M, Huang X (2014) MicroRNA-155 induction by Mycobacterium bovis BCG enhances ROS production through targeting SHIP1. Mol Immunol 62:29–36. https://doi.org/10.1016/j.molimm.2014.05.012

    CAS  Article  PubMed  Google Scholar 

  112. 112.

    Wang K, Gan TY, Li N, Liu CY, Zhou LY, Gao JN, Chen C, Yan KW, Ponnusamy M, Zhang YH, Li PF (2017) Circular RNA mediates cardiomyocyte death via miRNA-dependent upregulation of MTP18 expression. Cell Death Differ 24:1111–1120. https://doi.org/10.1038/cdd.2017.61

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  113. 113.

    Wang K, Liu F, Zhou LY, Long B, Yuan SM, Wang Y, Liu CY, Sun T, Zhang XJ, Li PF (2014) The long noncoding RNA CHRF regulates cardiac hypertrophy by targeting miR-489. Circ Res 114:1377–1388. https://doi.org/10.1161/circresaha.114.302476

    CAS  Article  PubMed  Google Scholar 

  114. 114.

    Wang L, Huang H, Fan Y, Kong B, Hu H, Hu K, Guo J, Mei Y, Liu WL (2014) Effects of downregulation of microRNA-181a on H2O2-induced H9c2 cell apoptosis via the mitochondrial apoptotic pathway. Oxid Med Cell Longev 2014:960362. https://doi.org/10.1155/2014/960362

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  115. 115.

    Wang T, Li M, Guan J, Li P, Wang H, Guo Y, Shuai S, Li X (2011) MicroRNAs miR-27a and miR-143 regulate porcine adipocyte lipid metabolism. Int J Mol Sci 12:7950–7959. https://doi.org/10.3390/ijms12117950

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  116. 116.

    Wang X, Li D, Chen H, Wei X, Xu X (2019) Expression of long noncoding RNA LIPCAR promotes cell proliferation, cell migration, and change in phenotype of vascular smooth muscle cells. Med Sci Monit 25:7645–7651. https://doi.org/10.12659/MSM.915681

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  117. 117.

    Wang X, Song C, Zhou X, Han X, Li J, Wang Z, Shang H, Liu Y, Cao H (2017) Mitochondria associated microRNA expression profiling of heart failure. Biomed Res Int 2017:4042509. https://doi.org/10.1155/2017/4042509

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  118. 118.

    Wang Z, Zhang XJ, Ji YX, Zhang P, Deng KQ, Gong J, Ren S, Wang X, Chen I, Wang H, Gao C, Yokota T, Ang YS, Li S, Cass A, Vondriska TM, Li G, Deb A, Srivastava D, Yang HT, Xiao X, Li H, Wang Y (2016) The long noncoding RNA Chaer defines an epigenetic checkpoint in cardiac hypertrophy. Nat Med 22:1131–1139. https://doi.org/10.1038/nm.4179

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  119. 119.

    Wiedemann N, Pfanner N (2017) Mitochondrial machineries for protein import and assembly. Annu Rev Biochem 86:685–714. https://doi.org/10.1146/annurev-biochem-060815-014352

    CAS  Article  PubMed  Google Scholar 

  120. 120.

    Wijnen WJ, van der Made I, van den Oever S, Hiller M, de Boer BA, Picavet DI, Chatzispyrou IA, Houtkooper RH, Tijsen AJ, Hagoort J, van Veen H, Everts V, Ruijter JM, Pinto YM, Creemers EE (2014) Cardiomyocyte-specific miRNA-30c over-expression causes dilated cardiomyopathy. PLoS One 9:e96290. https://doi.org/10.1371/journal.pone.0096290

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  121. 121.

    Xiao Y, Zhang X, Fan S, Cui G, Shen Z (2016) MicroRNA-497 inhibits cardiac hypertrophy by targeting Sirt4. PLoS One 11:e0168078. https://doi.org/10.1371/journal.pone.0168078

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  122. 122.

    Yadav S, Pandey A, Shukla A, Talwelkar SS, Kumar A, Pant AB, Parmar D (2011) miR-497 and miR-302b regulate ethanol-induced neuronal cell death through BCL2 protein and cyclin D2. J Biol Chem 286:37347–37357. https://doi.org/10.1074/jbc.M111.235531

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  123. 123.

    Yan K, An T, Zhai M, Huang Y, Wang Q, Wang Y, Zhang R, Wang T, Liu J, Zhang Y, Zhang J, Wang K (2019) Mitochondrial miR-762 regulates apoptosis and myocardial infarction by impairing ND2. Cell Death Dis 10:500. https://doi.org/10.1038/s41419-019-1734-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  124. 124.

    Yang F, Zhang H, Mei Y, Wu M (2014) Reciprocal regulation of HIF-1α and lincRNA-p21 modulates the Warburg effect. Mol Cell 53:88–100. https://doi.org/10.1016/j.molcel.2013.11.004

    CAS  Article  PubMed  Google Scholar 

  125. 125.

    Zaglia T, Ceriotti P, Campo A, Borile G, Armani A, Carullo P, Prando V, Coppini R, Vida V, Stølen TO, Ulrik W, Cerbai E, Stellin G, Faggian G, De Stefani D, Sandri M, Rizzuto R, Di Lisa F, Pozzan T, Catalucci D, Mongillo M (2017) Content of mitochondrial calcium uniporter (MCU) in cardiomyocytes is regulated by microRNA-1 in physiologic and pathologic hypertrophy. Proc Natl Acad Sci 114:E9006–E9015. https://doi.org/10.1073/pnas.1708772114

    CAS  Article  PubMed  Google Scholar 

  126. 126.

    Zhang C, Zhang J, Zhang A, Wang Y, Han L, You Y, Pu P, Kang C (2010) PUMA is a novel target of miR-221/222 in human epithelial cancers. Int J Oncol 37:1621–1626. https://doi.org/10.3892/ijo_00000816

    CAS  Article  PubMed  Google Scholar 

  127. 127.

    Zhang J, Xing Q, Zhou X, Li J, Li Y, Zhang L, Zhou Q, Tang B (2017) Circulating miRNA-21 is a promising biomarker for heart failure. Mol Med Rep 16:7766–7774. https://doi.org/10.3892/mmr.2017.7575

    CAS  Article  PubMed  Google Scholar 

  128. 128.

    Zhang J, Zhang X, Li C, Yue L, DingN RiordanT, Yang L, Li Y, Jen C, Lin S, Zhou D, Chen F (2019) Circular RNA profiling provides insights into their subcellular distribution and molecular characteristics in HepG2 cells. RNA Biol 16(2):220–232. https://doi.org/10.1080/15476286.2019.1565284

    Article  PubMed  PubMed Central  Google Scholar 

  129. 129.

    Zhang Q, Wang F, Wang F, Wu N (2019) Long noncoding RNA MAGI1-IT1 regulates cardiac hypertrophy by modulating miR-302e/DKK1/Wnt/beta-catenin signaling pathway. J Cell Physiol 235:245–253. https://doi.org/10.1002/jcp.28964

    CAS  Article  PubMed  Google Scholar 

  130. 130.

    Zhang X, Ji R, Liao X, Castillero E, Kennel PJ, Brunjes DL, Franz M, Möbius-Winkler S, Drosatos K, George I, Chen EI, Colombo PC, Schulze PC (2018) MicroRNA-195 regulates metabolism in failing myocardium via alterations in sirtuin 3 expression and mitochondrial protein acetylation. Circulation 137:2052–2067. https://doi.org/10.1161/circulationaha.117.030486

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  131. 131.

    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. https://doi.org/10.1016/j.cell.2014.05.047

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  132. 132.

    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. https://doi.org/10.1038/s41598-017-07611-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  133. 133.

    Zhao Y, Ponnusamy M, Liu C, Tian J, Dong Y, Gao J, Wang C, Zhang Y, Zhang L, Wang K, Li P (2017) MiR-485-5p modulates mitochondrial fission through targeting mitochondrial anchored protein ligase in cardiac hypertrophy. Biochim Biophys Acta Mol Basis Dis 1863:2871–2881. https://doi.org/10.1016/j.bbadis.2017.07.034

    CAS  Article  PubMed  Google Scholar 

  134. 134.

    Zimmer-Bensch G (2019) Emerging roles of long non-coding RNAs as drivers of brain evolution. Cells 8:1399. https://doi.org/10.3390/cells8111399

    CAS  Article  PubMed Central  Google Scholar 

  135. 135.

    Zisoulis DG, Kai ZS, Chang RK, Pasquinelli AE (2012) Autoregulation of microRNA biogenesis by let-7 and Argonaute. Nature 486:541–544. https://doi.org/10.1038/nature11134

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This article is based upon work from EU-CardioRNA COST Action CA17129 (www.cardiorna.eu) supported by COST (European Cooperation in Science and Technology). AJ is supported by the University of Tuzla, Bosnia and Herzegovina. YD is funded by the National Research Fund (Grants Nos. C14/BM/8225223 and C17/BM/11613033), the Ministry of Higher Education and Research and the Fondation Coeur—Daniel Wagner of Luxembourg.

Author information

Affiliations

Authors

Consortia

Corresponding author

Correspondence to Yvan Devaux.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jusic, A., Devaux, Y. & the EU-CardioRNA COST Action (CA17129). Mitochondrial noncoding RNA-regulatory network in cardiovascular disease. Basic Res Cardiol 115, 23 (2020). https://doi.org/10.1007/s00395-020-0783-5

Download citation

Keywords

  • Mitochondria
  • MicroRNAs
  • Long noncoding RNAs
  • Biomarkers
  • Cardiovascular disease