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Role of noncoding RNAs in regulation of cardiac cell death and cardiovascular diseases

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Abstract

Loss of functional cardiomyocytes is a major underlying mechanism for myocardial remodeling and heart diseases, due to the limited regenerative capacity of adult myocardium. Apoptosis, programmed necrosis, and autophagy contribute to loss of cardiac myocytes that control the balance of cardiac cell death and cell survival through multiple intricate signaling pathways. In recent years, non-coding RNAs (ncRNAs) have received much attention to uncover their roles in cell death of cardiovascular diseases, such as myocardial infarction, cardiac hypertrophy, and heart failure. In addition, based on the view that mitochondrial morphology is linked to three types of cell death, ncRNAs are able to regulate mitochondrial fission/fusion of cardiomyocytes by targeting genes involved in cell death pathways. This review focuses on recent progress regarding the complex relationship between apoptosis/necrosis/autophagy and ncRNAs in the context of myocardial cell death in response to stress. This review also provides insight into the treatment for heart diseases that will guide novel therapies in the future.

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References

  1. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL (1994) Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94:1621–1628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Olivetti G, Abbi R, Quaini F, Kajstura J, Cheng W, Nitahara JA et al (1997) Apoptosis in the failing human heart. New Engl J Med 336:1131–1141

    Article  CAS  PubMed  Google Scholar 

  3. Konstantinidis K, Whelan RS, Kitsis RN (2012) Mechanisms of cell death in heart disease. Arterioscler Throm Vasc 32:1552–1562

    Article  CAS  Google Scholar 

  4. Wang K, Zhou LY, Wang JX, Wang Y, Sun T, Zhao B et al (2015) E2F1-dependent miR-421 regulates mitochondrial fragmentation and myocardial infarction by targeting Pink1. Nat Commun 6:7619

    Article  CAS  PubMed  Google Scholar 

  5. Small EM, Frost RJA, Olson EN (2010) MicroRNAs add a new dimension to cardiovascular disease. Circulation 121:U1022–U1066

    Article  Google Scholar 

  6. Leite-Moreira AM, Lourenco AP, Falcao-Pires I, Leite-Moreira AF (2013) Pivotal role of microRNAs in cardiac physiology and heart failure. Drug Discov Today 18:1243–1249

    Article  CAS  PubMed  Google Scholar 

  7. Kumarswamy R, Thum T (2013) Non-coding RNAs in cardiac remodeling and heart failure. Circ Res 113:676–689

    Article  CAS  PubMed  Google Scholar 

  8. Boon RA, Dimmeler S (2015) MicroRNAs in myocardial infarction. Nat Rev Cardiol 12:135–142

    Article  CAS  PubMed  Google Scholar 

  9. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9:102–114

    Article  CAS  PubMed  Google Scholar 

  10. Chekulaeva M, Filipowicz W (2009) Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr Opin Cell Biol 21:452–460

    Article  CAS  PubMed  Google Scholar 

  11. Berezikov E (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12:846–860

    Article  CAS  PubMed  Google Scholar 

  12. Graves P, Zeng Y (2012) Biogenesis of mammalian microRNAs: a global view. Genom Proteom Bioinform 10:239–245

    Article  CAS  Google Scholar 

  13. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH et al (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16:3–11

    Article  CAS  PubMed  Google Scholar 

  14. Bergsbaken T, Fink SL, Cookson BT (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7:99–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Orogo AM, Gustafsson AB (2013) Cell death in the myocardium: my heart won’t go on. IUBMB Life 65:651–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Skommer J, Rana I, Marques FZ, Zhu W, Du Z, Charchar FJ (2014) Small molecules, big effects: the role of microRNAs in regulation of cardiomyocyte death. Cell Death Dis 5:e1325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gao CF, Ren S, Zhang LL, Nakajima T, Ichinose S, Hara T et al (2001) Caspase-dependent cytosolic release of cytochrome c and membrane translocation of Bax in p53-induced apoptosis. Exp Cell Res 265:145–151

    Article  CAS  PubMed  Google Scholar 

  18. Jiang XJ, Wang XD (2000) Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1. J Biol Chem 275:31199–31203

    Article  CAS  PubMed  Google Scholar 

  19. Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ (2010) Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 121(18):2012–2022

    Article  CAS  PubMed  Google Scholar 

  20. Clerk A, Cullingford TE, Fuller SJ, Giraldo A, Markou T, Pikkarainen S et al (2007) Signaling pathways mediating cardiac myocyte gene expression in physiological and stress responses. J Cell Physiol 212:311–322

    Article  CAS  PubMed  Google Scholar 

  21. Bostjancic E, Zidar N, Glavac D (2009) MicroRNA microarray expression profiling in human myocardial infarction. Dis Mark 27:255–268

    Article  CAS  Google Scholar 

  22. Tang Y, Zheng J, Sun Y, Wu Z, Liu Z, Huang G (2009) MicroRNA-1 regulates cardiomyocyte apoptosis by targeting Bcl-2. Int Heart J 50:377–387

    Article  CAS  PubMed  Google Scholar 

  23. Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B et al (2007) The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med 13:486–491

    Article  CAS  PubMed  Google Scholar 

  24. Xu C, Lu Y, Pan Z, Chu W, Luo X, Lin H et al (2007) The muscle-specific microRNAs miR-1 and miR-133 produce opposing effects on apoptosis by targeting HSP60, HSP70 and caspase-9 in cardiomyocytes. J Cell Sci 120:3045–3052

    Article  CAS  PubMed  Google Scholar 

  25. Matkovich SJ, Wang W, Tu Y, Eschenbacher WH, Dorn LE, Condorelli G et al (2010) MicroRNA-133a protects against myocardial fibrosis and modulates electrical repolarization without affecting hypertrophy in pressure-overloaded adult hearts. Circ Res 106:166–175

    Article  CAS  PubMed  Google Scholar 

  26. Wang HJ, Li J, Chi HJ, Zhang F, Zhu XM, Cai J et al (2015) MicroRNA-181c targets Bcl-2 and regulates mitochondrial morphology in myocardial cells. J Cell Mol Med 19:2084–2097

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Cheng Y, Liu X, Zhang S, Lin Y, Yang J, Zhang C (2009) MicroRNA-21 protects against the H(2)O(2)-induced injury on cardiac myocytes via its target gene PDCD4. J Mol Cell Cardiol 47:5–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Rane S, He M, Sayed D, Vashistha H, Malhotra A, Sadoshima J et al (2009) Downregulation of miR-199a derepresses hypoxia-inducible factor-1alpha and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res 104:879–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ren XP, Wu J, Wang X, Sartor MA, Qian J, Jones K et al (2009) MicroRNA-320 is involved in the regulation of cardiac ischemia/reperfusion injury by targeting heat-shock protein 20. Circulation 119:2357–2366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Wang JX, Gao J, Ding SL, Wang K, Jiao JQ, Wang Y et al (2015) Oxidative modification of miR-184 enables It to target Bcl-xL and Bcl-w. Mol Cell 59:50–61

    Article  CAS  PubMed  Google Scholar 

  32. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T et al (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 14:193–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Li P (2010) MicroRNAs in cardiac apoptosis. J Cardiovasc Transl Res 3:219–224

    Article  PubMed  Google Scholar 

  34. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F et al (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 1:515–525

    Article  CAS  PubMed  Google Scholar 

  35. Li JC, Donath S, Li YR, Qin D, Prabhakar BS, Li PF (2016) miR-30 Regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. Plos Genet 6(1):e1000795

    Article  CAS  Google Scholar 

  36. Wang JX, Jiao JQ, Li QA, Long B, Wang K, Liu JP et al (2011) miR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat Med 17(1):71–78

    Article  PubMed  CAS  Google Scholar 

  37. Li JC, Zhou J, Li YR, Qin DN, Li PF (2010) Mitochondrial fission controls DNA fragmentation by regulating endonuclease G. Free Radic Biol Med 49:622–631

    Article  CAS  PubMed  Google Scholar 

  38. Li JC, Li YZ, Jiao JQ, Wang JX, Li YR, Qin DN et al (2014) Mitofusin 1 is negatively regulated by microRNA 140 in cardiomyocyte apoptosis. Mol Cell Biol 34:1788–1799

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Dagda RK, Cherra SJ, Kulich SM, Tandon A, Park D, Chu CT (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 284:13843–13855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wang K, Zhou LY, Wang JX, Wang Y, Sun T, Zhao B et al (2015) E2F1-dependent miR-421 regulates mitochondrial fragmentation and myocardial infarction by targeting Pink1. Nat Commun 6:7619

    Article  CAS  PubMed  Google Scholar 

  41. Wang K, Liu CY, Zhang XJ, Feng C, Zhou LY, Zhao Y et al (2015) miR-361-regulated prohibitin inhibits mitochondrial fission and apoptosis and protects heart from ischemia injury. Cell Death Differ 22(6):1058–1068

    Article  CAS  PubMed  Google Scholar 

  42. Wang K, Zhang DL, Long B, An T, Zhang J, Zhou LY et al (2015) NFAT4-dependent miR-324-5p regulates mitochondrial morphology and cardiomyocyte cell death by targeting Mtfr1. Cell Death Dis 6:e2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Singal PK, Iliskovic N (1998) Doxorubicin-induced cardiomyopathy. New Engl J Med 339(13):900–905

    Article  CAS  PubMed  Google Scholar 

  44. Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ, Moens AL (2012) Doxorubicin-induced cardiomyopathy: from molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol 52:1213–1225

    Article  CAS  PubMed  Google Scholar 

  45. Tony H, Yu K, Qiutang Z (2015) MicroRNA-208a silencing attenuates doxorubicin induced myocyte apoptosis and cardiac dysfunction. Oxidative Med Cell Longev 2015:597032

    Article  CAS  Google Scholar 

  46. Wang JX, Zhang XJ, Feng C, Sun T, Wang K, Wang Y et al (2015) MicroRNA-532-3p regulates mitochondrial fission through targeting apoptosis repressor with caspase recruitment domain in doxorubicin cardiotoxicity. Cell Death Dis 6:e1677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Tong Z, Jiang B, Wu Y, Liu Y, Li Y, Gao M et al (2015) MiR-21 protected cardiomyocytes against doxorubicin-induced apoptosis by targeting BTG2. Int J Mol Sci 16(7):14511–14525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Roca-Alonso L, Castellano L, Mills A, Dabrowska AF, Sikkel MB, Pellegrino L et al (2015) Myocardial MiR-30 downregulation triggered by doxorubicin drives alterations in beta-adrenergic signaling and enhances apoptosis. Cell Death Dis 6:e1754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Papait R, Kunderfranco P, Stirparo GG, Latronico MVG, Condorelli G (2013) Long noncoding RNA: a new player of heart failure? J Cardiovasc Transl 6:876–883

    Article  Google Scholar 

  50. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Piccoli MT, Gupta SK, Thum T (2015) Noncoding RNAs as regulators of cardiomyocyte proliferation and death. J Mol Cell Cardiol 89:59–67

    Article  CAS  PubMed  Google Scholar 

  52. Ginger MR, Shore AN, Contreras A, Rijnkels M, Miller J, Gonzalez-Rimbau MF et al (2006) A noncoding RNA is a potential marker of cell fate during mammary gland development. Proc Natl Acad Sci USA 103:5781–5786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kanduri C (2011) Kcnq1ot1: a chromatin regulatory RNA. Semin Cell Dev Biol 22:343–350

    Article  CAS  PubMed  Google Scholar 

  54. Grote P, Wittler L, Hendrix D, Koch F, Wahrisch S, Beisaw A et al (2013) The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell 24:206–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Ishii N, Ozaki K, Sato H, Mizuno H, Saito S, Takahashi A et al (2006) Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J Hum Genet 51:1087–1099

    Article  CAS  PubMed  Google Scholar 

  56. Wang K, Long B, Zhou LY, Liu F, Zhou QY, Liu CY et al (2014) CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 downregulation. Nat Commun 5:3596

    PubMed  Google Scholar 

  57. Hsu MT, Coca-Prados M (1979) Electron microscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells. Nature 280(5720):339–340

    Article  CAS  PubMed  Google Scholar 

  58. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A et al (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495:333–338

    Article  CAS  PubMed  Google Scholar 

  59. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK et al (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388

    Article  CAS  PubMed  Google Scholar 

  60. Wang K, Long B, Liu F, Wang JX, Liu CY, Zhao B et al (2016) A circular RNA protects the heart from pathological hypertrophy and heart failure by targeting miR-223. Eur Heart J 37(33):2602–2611

    Article  PubMed  Google Scholar 

  61. Koseki T, Inohara N, Chen S, Nunez G (1998) ARC, an inhibitor of apoptosis expressed in skeletal muscle and heart that interacts selectively with caspases. Proc Natl Acad Sci USA 95(9):5156–5160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Li YZ, Lu DY, Tan WQ, Wang JX, Li PF (2008) p53 initiates apoptosis by transcriptionally targeting the antiapoptotic protein ARC. Mol Cell Biol 28:564–574

    Article  CAS  PubMed  Google Scholar 

  63. Du WJ, Pan ZW, Chen X, Wang LM, Zhang Y, Li S et al (2014) By targeting Stat3 microRNA-17-5p promotes cardiomyocyte apoptosis in response to ischemia followed by reperfusion. Cell Physiol Biochem 34:955–965

    Article  CAS  PubMed  Google Scholar 

  64. Danielson LS, Park DS, Rotllan N, Chamorro-Jorganes A, Guijarro MV, Fernandez-Hernando C et al (2013) Cardiovascular dysregulation of miR-17-92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis. Faseb J 27:1460–1467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Qin YJ, Yu YQ, Dong H, Bian XH, Guo X, Dong SM (2012) MicroRNA 21 inhibits left ventricular remodeling in the early phase of rat model with ischemia–reperfusion injury by suppressing cell apoptosis. Int J Med Sci 9:413–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ding SL, Wang JX, Jiao JQ, Tu X, Wang Q, Liu F et al (2013) A pre-microRNA-149 (miR-149) genetic variation affects miR-149 maturation and its ability to regulate the Puma protein in apoptosis. J Biol Chem 288:26865–26877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Long B, Wang K, Li N, Murtaza I, Xiao JY, Fan YY et al (2013) miR-761 regulates the mitochondrial network by targeting mitochondrial fission factor. Free Radic Biol Med 65:371–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wang JX, Jiao JQ, Li Q, Long B, Wang K, Liu JP et al (2011) miR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat Med 17:71–78

    Article  PubMed  CAS  Google Scholar 

  69. Lv G, Shao S, Dong H, Bian X, Yang X, Dong S (2014) MicroRNA-214 protects cardiac myocytes against H2O2-induced injury. J Cell Biochem 115:93–101

    Article  CAS  PubMed  Google Scholar 

  70. Li R, Yan G, Li Q, Sun H, Hu Y, Sun J et al (2012) MicroRNA-145 protects cardiomyocytes against hydrogen peroxide (H(2)O(2))-induced apoptosis through targeting the mitochondria apoptotic pathway. PLoS One 7:e44907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Fang J, Song XW, Tian J, Chen HY, Li DF, Wang JF et al (2012) Overexpression of microRNA-378 attenuates ischemia-induced apoptosis by inhibiting caspase-3 expression in cardiac myocytes. Apoptosis 17:410–423

    Article  CAS  PubMed  Google Scholar 

  72. Zhu H, Yang Y, Wang Y, Li J, Schiller PW, Peng T (2011) MicroRNA-195 promotes palmitate-induced apoptosis in cardiomyocytes by down-regulating Sirt1. Cardiovasc Res 92:75–84

    Article  CAS  PubMed  Google Scholar 

  73. Tabuchi T, Satoh M, Itoh T, Nakamura M (2012) MicroRNA-34a regulates the longevity-associated protein SIRT1 in coronary artery disease: effect of statins on SIRT1 and microRNA-34a expression. Clin Sci (Lond) 123:161–171

    Article  CAS  Google Scholar 

  74. Wu W, Liu P, Li J (2012) Necroptosis: an emerging form of programmed cell death. Crit Rev Oncol Hematol 82:249–258

    Article  PubMed  Google Scholar 

  75. Galluzzi L, Kepp O, Kroemer G (2009) RIP kinases initiate programmed necrosis. J Mol Cell Biol 1:8–10

    Article  CAS  PubMed  Google Scholar 

  76. Fiers W, Beyaert R, Boone E, Cornelis S, Declercq W, Decoster E et al (1995) TNF-induced intracellular signaling leading to gene induction or to cytotoxicity by necrosis or by apoptosis. J Inflamm 47:67–75

    CAS  PubMed  Google Scholar 

  77. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S et al (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1:489–495

    Article  CAS  PubMed  Google Scholar 

  78. Degterev A, Hitomi J, Germscheid M, Ch’en IL, Korkina O, Teng X et al (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4:313–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Whelan RS, Kaplinskiy V, Kitsis RN (2010) Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol 72:19–44

    Article  CAS  PubMed  Google Scholar 

  80. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA et al (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434:658–662

    Article  CAS  PubMed  Google Scholar 

  81. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H et al (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434:652–658

    Article  CAS  PubMed  Google Scholar 

  82. Wang K, An T, Zhou LY, Liu CY, Zhang XJ, Feng C et al (2015) E2F1-regulated miR-30b suppresses cyclophilin D and protects heart from ischemia/reperfusion injury and necrotic cell death. Cell Death Differ 22:743–754

    Article  CAS  PubMed  Google Scholar 

  83. Liu J, van Mil A, Vrijsen K, Zhao J, Gao L, Metz CH et al (2011) MicroRNA-155 prevents necrotic cell death in human cardiomyocyte progenitor cells via targeting RIP1. J Cell Mol Med 15:1474–1482

    Article  CAS  PubMed  Google Scholar 

  84. Wang K, Liu F, Zhou LY, Ding SL, Long B, Liu CY et al (2013) miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death Dis 4:e709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Lee EW, Kim JH, Ahn YH, Seo J, Ko A, Jeong M et al (2012) Ubiquitination and degradation of the FADD adaptor protein regulate death receptor-mediated apoptosis and necroptosis. Nat Commun 3:978

    Article  PubMed  CAS  Google Scholar 

  86. Wang JX, Zhang XJ, Li Q, Wang K, Wang Y, Jiao JQ et al (2015) MicroRNA-103/107 regulate programmed necrosis and myocardial ischemia/reperfusion injury through targeting FADD. Circ Res 117:352–363

    Article  CAS  PubMed  Google Scholar 

  87. Wang K, Long B, Li N, Li L, Liu CY, Dong YH et al (2016) MicroRNA-2861 regulates programmed necrosis in cardiomyocyte by impairing adenine nucleotide translocase 1 expression. Free Radic Biol Med 91:58–67

    Article  CAS  PubMed  Google Scholar 

  88. Walther T, Tschope C, Sterner-Kock A, Westermann D, Heringer-Walther S, Riad A et al (2007) Accelerated mitochondrial adenosine diphosphate/adenosine triphosphate transport improves hypertension-induced heart disease. Circulation 115:333–344

    Article  CAS  PubMed  Google Scholar 

  89. Wang K, Liu F, Liu CY, An T, Zhang J, Zhou LY et al (2016) The long noncoding RNA NRF regulates programmed necrosis and myocardial injury during ischemia and reperfusion by targeting miR-873. Cell Death Differ 23(8):1394–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. He CC, Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43:67–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132(1):27–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Taneike M, Yamaguchi O, Nakai A, Hikoso S, Takeda T, Mizote I et al (2010) Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy 6(5):600–606

    Article  CAS  PubMed  Google Scholar 

  93. Sciarretta S, Volpe M, Sadoshima J (2014) Mammalian target of rapamycin signaling in cardiac physiology and disease. Circ Res 114(3):549–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Li Q, Xie J, Li R, Shi J, Sun J, Gu R et al (2014) Overexpression of microRNA-99a attenuates heart remodelling and improves cardiac performance after myocardial infarction. J Cell Mol Med 18:919–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Su M, Wang J, Wang C, Wang X, Dong W, Qiu W et al (2015) MicroRNA-221 inhibits autophagy and promotes heart failure by modulating the p27/CDK2/mTOR axis. Cell Death Differ 22:986–999

    Article  CAS  PubMed  Google Scholar 

  96. Bo L, Su-Ling D, Fang L, Lu-Yu Z, Tao A, Stefan D et al (2014) Autophagic program is regulated by miR-325. Cell Death Differ 21:967–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Pan W, Zhong Y, Cheng C, Liu B, Wang L, Li A et al (2013) MiR-30-regulated autophagy mediates angiotensin II-induced myocardial hypertrophy. PLoS One 8:e53950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW et al (2007) MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation 116:258–267

    Article  CAS  PubMed  Google Scholar 

  99. Ucar A, Gupta SK, Fiedler J, Erikci E, Kardasinski M, Batkai S et al (2012) The miRNA-212/132 family regulates both cardiac hypertrophy and cardiomyocyte autophagy. Nat Commun 3:1078

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Song L, Su M, Wang S, Zou Y, Wang X, Wang Y et al (2014) MiR-451 is decreased in hypertrophic cardiomyopathy and regulates autophagy by targeting TSC1. J Cell Mol Med 18:2266–2274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Gupta SK, Foinquinos A, Thum S, Remke J, Zimmer K, Bauters C et al (2016) Preclinical development of a MicroRNA-based therapy for elderly patients with myocardial infarction. J Am Coll Cardiol 68:1557–1571

    Article  CAS  PubMed  Google Scholar 

  102. Wang K, Liu CY, Zhou LY, Wang JX, Wang M, Zhao B et al (2015) APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat Commun 6:6779

    Article  CAS  PubMed  Google Scholar 

  103. Huang J, Sun W, Huang H, Ye J, Pan W, Zhong Y et al (2014) miR-34a modulates angiotensin II-induced myocardial hypertrophy by direct inhibition of ATG9A expression and autophagic activity. PLoS One 9:e94382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Li XX, Zeng Z, Li Q, Xu QL, Xie JH, Hao HX et al (2015) Inhibition of microRNA-497 ameliorates anoxia/reoxygenation injury in cardiomyocytes by suppressing cell apoptosis and enhancing autophagy. Oncotarget 6:18829–18844

    Article  PubMed  PubMed Central  Google Scholar 

  105. Nishida K, Yamaguchi O, Otsu K (2008) Crosstalk between autophagy and apoptosis in heart disease. Circ Res 103:343–351

    Article  CAS  PubMed  Google Scholar 

  106. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26:1749–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Yamaguchi O, Higuchi Y, Hirotani S, Kashiwase K, Nakayama H, Hikoso S et al (2003) Targeted deletion of apoptosis signal-regulating kinase 1 attenuates left ventricular remodeling. Proc Natl Acad Sci USA 100:15883–15888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Marquez RT, Xu L (2012) Bcl-2: beclin 1 complex: multiple, mechanisms regulating autophagy/apoptosis toggle switch. Am J Cancer Res 2:214–221

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Crighton D, Wilkinson S, O’Prey J, Syed N, Smith P, Harrison PR et al (2006) DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126:121–134

    Article  CAS  PubMed  Google Scholar 

  110. Pyo JO, Jang MH, Kwon YK, Lee HJ, Jun JIL, Woo HN et al (2005) Essential roles of Atg5 and FADD in autophagic cell death—dissection of autophagic cell death into vacuole formation and cell death. J Biol Chem 280:20722–20729

    Article  CAS  PubMed  Google Scholar 

  111. Whelan RS, Konstantinidis K, Wei AC, Chen Y, Reyna DE, Jha S et al (2012) Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci USA 109:6566–6571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Diwan A, Matkovich SJ, Yuan QY, Zhao W, Yatani A, Brown JH et al (2009) Endoplasmic reticulum-mitochondria crosstalk in NIX-mediated murine cell death. J Clin Investig 119:203–212

    CAS  PubMed  Google Scholar 

  113. Ng F, Tang BL (2013) Sirtuins’ modulation of autophagy. J Cell Physiol 228:2262–2270

    Article  CAS  PubMed  Google Scholar 

  114. Ham O, Lee SY, Lee CY, Park JH, Lee J, Seo HH, et al (2015) Let-7b suppresses apoptosis and autophagy of human mesenchymal stem cells transplanted into ischemia/reperfusion injured heart 7 by targeting caspase-3. Stem Cell Res Ther 6

  115. Zou Y, Liu W, Zhang J, Xiang D (2016) miR-153 regulates apoptosis and autophagy of cardiomyocytes by targeting Mcl-1. Mol Med Rep 14:1033–1039

    Article  CAS  PubMed  Google Scholar 

  116. Widera C, Gupta SK, Lorenzen JM, Bang C, Bauersachs J, Bethmann K et al (2011) Diagnostic and prognostic impact of six circulating microRNAs in acute coronary syndrome. J Mol Cell Cardiol 51(5):872–875

    Article  CAS  PubMed  Google Scholar 

  117. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C et al (2010) Circulating microRNAs in patients with coronary artery disease. Circ Res 107(5):677–684

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Chao Chen of the Institute for Translational Medicine, Qingdao University, China for his generous assistance with literature searches.

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Correspondence to Peifeng Li or Kun Wang.

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This work was supported by the Natural Science Foundation of China (Grant nos: 31430041, 81470522, 81522005), Applied Basic Research Programs of Qingdao, China (Grant no: 17-1-1-46-jch), and Shandong Provincial Natural Science Foundation, China (Grant no: ZR2016CQ31).

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The authors have declared there are no potential conflicts of interest, funding, acknowledgements.

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Dong, Y., Liu, C., Zhao, Y. et al. Role of noncoding RNAs in regulation of cardiac cell death and cardiovascular diseases. Cell. Mol. Life Sci. 75, 291–300 (2018). https://doi.org/10.1007/s00018-017-2640-8

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  • DOI: https://doi.org/10.1007/s00018-017-2640-8

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