Noncoding RNAs as regulators of cardiomyocyte proliferation and death

Journal of Molecular and Cellular Cardiology

Volumn 89, Issue , 2015, Pages 59-67

  Piccoli, Maria Teresa ^a   Gupta, Shashi Kumar ^a   Thum, Thomas ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Apoptosis; Autophagy; Cardiomyocyte; MicroRNAs; Necrosis; Proliferation

Indexed keywords

LIOTHYRONINE; LONG UNTRANSLATED RNA; MICRORNA; MICRORNA 10A; MICRORNA 132; MICRORNA 133; MICRORNA 133A; MICRORNA 140; MICRORNA 141; MICRORNA 145; MICRORNA 155; MICRORNA 17 92; MICRORNA 195; MICRORNA 199A 3P; MICRORNA 19B; MICRORNA 20A; MICRORNA 212; MICRORNA 29; MICRORNA 30; MICRORNA 30A; MICRORNA 325; MICRORNA 34; MICRORNA 451A; MICRORNA 499; MICRORNA 590 3P; MICRORNA 874; MICRORNA 99A; PROTEIN BNIP3; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

APOPTOSIS; AUTOPHAGY; CARDIAC REGENERATION; CELL COUNT; CELL DEATH; CELL PROLIFERATION; CELL SELF-RENEWAL; CELL SURVIVAL; CELL VIABILITY; DOWN REGULATION; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE REPRESSION; HEART DEVELOPMENT; HEART INFARCTION; HEART MUSCLE CELL; HEART PROTECTION; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MITOSIS; NECROPTOSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; TISSUE REGENERATION; UPREGULATION; ANIMAL; CARDIAC MUSCLE CELL; CYTOLOGY; GENETICS; METABOLISM;

ANIMALS; AUTOPHAGY; CELL DEATH; CELL PROLIFERATION; HUMANS; MICRORNAS; MYOCYTES, CARDIAC; RNA, LONG NONCODING;

EID: 84939841891     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.02.002     Document Type: Review

References (96)

1. Lopez A.D.M., Ezzati M., Jamison D.T., Murray C.J. Global Burden of Disease and Risk Factors: Disease Control Priorities Project 2006, World Bank and Oxford University Press, NY.
2. Pagidipati N.J., Gaziano T.A. Estimating deaths from cardiovascular disease: a review of global methodologies of mortality measurement. Circulation 2013, 127(6):749-756.
3. Small E.M., Frost R.J., Olson E.N. MicroRNAs add a new dimension to cardiovascular disease. Circulation 2010, 121(8):1022-1032.
4. Chen J., Wang D.Z. MicroRNAs in cardiovascular development. J Mol Cell Cardiol 2012, 52(5):949-957.
5. Rodriguez A., Griffiths-Jones S., Ashurst J.L., Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res 2004, 14(10A):1902-1910.
6. Lee Y., Kim M., Han J., Yeom K.H., Lee S., Baek S.H., et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004, 23(20):4051-4060.
7. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433(7027):769-773.
8. Ha M., Narry Kim V. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 2014, 15:509-524.
9. Christoffels V.M., Habets P.E., Franco D., Campione M., de Jong F., Lamers W.H., et al. Chamber formation and morphogenesis in the developing mammalian heart. Dev Biol 2000, 223(2):266-278.
10. Li F., Wang X., Capasso J.M., Gerdes A.M. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol 1996, 28(8):1737-1746.
11. Li X., Wang J., Jia Z., Cui Q., Zhang C., Wang W., et al. MiR-499 regulates cell proliferation and apoptosis during late-stage cardiac differentiation via Sox6 and cyclin D1. PLoS One Sep 11 2013, 8(9):e74504.
12. Porrello E.R., Johnson B.A., Aurora A.B., Simpson E., Nam Y.J., Matkovich S.J., et al. MiR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ Res 2011, 109(6):670-679.
13. Zhang Y., Matsushita N., Eigler T., Marbán E. Targeted microRNA interference promotes postnatal cardiac cell cycle re-entry. J Regen Med 2013, 2(2).
14. Porrello E.R., Mahmoud A.I., Simpson E., Johnson B.A., Grinsfelder D., Canseco D., et al. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc Natl Acad Sci U S A 2013, 110(1):187-192.
15. González-Rosa J.M., Martín V., Peralta M., Torres M., Mercader N. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 2011, 138(9):1663-1674.
16. Hullinger T.G., Montgomery R.L., Seto A.G., Dickinson B.A., Semus H.M., Lynch J.M., et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res 2012, 110(1):71-81.
17. Zhang Y., Li T.S., Lee S.T., Wawrowsky K.A., Cheng K., Galang G., et al. Dedifferentiation and proliferation of mammalian cardiomyocytes. PLoS ONE 2010, 5(9):e12559.
18. Soonpaa M.H., Field L.J. Survey of studies examining mammalian cardiomyocyte DNA synthesis. Circ Res 1998, 83(1):15-26.
19. Senyo S.E., Steinhauser M.L., Pizzimenti C.L., Yang V.K., Cai L., Wang M., et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature Jan 17 2013, 493(7432):433-436.
20. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabé-Heider F., Walsh S., et al. Evidence for cardiomyocyte renewal in humans. Science 2009, 324(5923):98-102.
21. Pasumarthi K.B., Field L.J. Cardiomyocyte cell cycle regulation. Circ Res 2002, 90(10):1044-1054.
22. Liang D., Zhen L., Yuan T., Huang J., Deng F., Wuyahan, et al. miR-10a regulates proliferation of human cardiomyocyte progenitor cells by targeting GATA6. PLoS One Jul 28 2014, 9(7):e103097.
23. Mollova M., Bersell K., Walsh S., Savla J., Das L.T., Park S.Y., et al. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc Natl Acad Sci U S A Jan 22 2013, 110(4):1446-1451.
24. van Berlo J.H., Molkentin J.D. An emerging consensus on cardiac regeneration. Nat Med Dec 4 2014, 20(12):1386-1393.
25. Anversa P., Kajstura J., Leri A., Bolli R. Life and death of cardiac stem cells: a paradigm shift in cardiac biology. Circulation 2006, 113(11):1451-1463.
26. Bras-Rosario L., Matsuda A., Pinheiro A.I., Gardner R., Lopes T., Amaral A., et al. Expression profile of microRNAs regulating proliferation and differentiation in mouse adult cardiac stem cells. PLoS One May 17 2013, 8(5):e63041.
27. O'Donnell K.A., Wentzel E.A., Zeller K.I., Dang C.V., Mendell J.T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature Jun 9 2005, 435(7043):839-843.
28. Chen J., Huang Z.P., Seok H.Y., Ding J., Kataoka M., Zhang Z., et al. Mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ Res Jun 7 2013, 112(12):1557-1566.
29. Qin D.N., Qian L., Hu D.L., Yu Z.B., Han S.P., Zhu C., et al. Effects of miR-19b overexpression on proliferation, differentiation, apoptosis and Wnt/β-catenin signaling pathway in P19 cell model of cardiac differentiation in vitro. Cell Biochem Biophys 2013, 66(3):709-722.
30. Yin V.P., Lepilina A., Smith A., Poss K.D. Regulation of zebrafish heart regeneration by miR-133. Dev Biol 2012, 365(2):319-327.
31. Jopling C., Sleep E., Raya M., Martí M., Raya A., Izpisúa Belmonte J.C. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464(7288):606-609.
32. Carè A., Catalucci D., Felicetti F., Bonci D., Addario A., Gallo P., et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007, 13(5):613-618.
33. van Rooij E., Liu N., Olson E.N. MicroRNAs flex their muscles. Trends Genet Apr 2008, 24(4):159-166.
34. Liu N., Bezprozvannaya S., Williams A.H., Qi X., Richardson J.A., Bassel-Duby R., et al. microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev 2008, 22(23):3242-3254.
35. Eulalio A., Mano M., Dal Ferro M., Zentilin L., Sinagra G., Zacchigna S., et al. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 2012, 492(7429):376-381.
36. Cao X., Wang J., Wang Z., Du J., Yuan X., Huang W., et al. MicroRNA profiling during rat ventricular maturation: a role for miR-29a in regulating cardiomyocyte cell cycle re-entry. FEBS Lett 2013, 587(10):1548-1555.
37. Whelan R.S., Kaplinskiy V., Kitsis R.N. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol 2010, 72:19-44.
38. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407(6805):770-776.
39. Crow M.T., Mani K., Nam Y.J., Kitsis R.N. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 2004, 95(10):957-970.
40. Gustafsson A.B., Gottlieb R.A. Bcl-2 family members and apoptosis, taken to heart. Am J Physiol Cell Physiol Jan 2007, 292(1):C45-C51.
41. Gao C.F., Ren S., Zhang L., Nakajima T., Ichinose S., Hara T., et al. Caspase-dependent cytosolic release of cytochrome c and membrane translocation of Bax in p53-induced apoptosis. Exp Cell Res Apr 15 2001, 265(1):145-151.
42. Tanaka A., Youle R.J. A chemical inhibitor of DRP1 uncouples mitochondrial fission and apoptosis. Mol Cell 2008, 29(4):409-410.
43. Ong S.B., Subrayan S., Lim S.Y., Yellon D.M., Davidson S.M., Hausenloy D.J. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation May 11 2010, 121(18):2012-2022.
44. Cassidy-Stone A., Chipuk J.E., Ingerman E., Song C., Yoo C., Kuwana T., et al. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell Feb 2008, 14(2):193-204.
45. Li J., Zhou J., Li Y., Qin D., Li P. Mitochondrial fission controls DNA fragmentation by regulating endonuclease G. Free Radic Biol Med Aug 15 2010, 49(4):622-631.
46. Li J., Li Y., Jiao J., Wang J., Li Y., Qin D., et al. Mitofusin 1 is negatively regulated by microRNA 140 in cardiomyocyte apoptosis. Mol Cell Biol May 2014, 34(10):1788-1799.
47. Chiong M., Wang Z.V., Pedrozo Z., Cao D.J., Troncoso R., Ibacache M., et al. Cardiomyocyte death: mechanisms and translational implications. Cell Death Dis Dec 22 2011, 2:e244.
48. Guerra S., Leri A., Wang X., Finato N., Di Loreto C., Beltrami C.A., et al. Myocyte death in the failing human heart is gender dependent. Circ Res Oct 29 1999, 85(9):856-866.
49. Smith C.C., Davidson S.M., Lim S.Y., Simpkin J.C., Hothersall J.S., Yellon D.M. Necrostatin: a potentially novel cardioprotective agent?. Cardiovasc Drugs Ther 2007, 21(4):227-233.
50. Garlick P.B., Davies M.J., Hearse D.J., Slater T.F. Direct detection of free radicals in the reperfused rat heart using electron spin resonance spectroscopy. Circ Res Nov 1987, 61(5):757-760.
51. Lomonosova E., Chinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. Oncogene Dec 2008, 27(Suppl. 1):S2-S19.
52. Christofferson D.E., Yuan J. Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol Apr 2010, 22(2):263-268.
53. Li J., McQuade T., Siemer A.B., Napetschnig J., Moriwaki K., Hsiao Y.S., et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell Jul 20 2012, 150(2):339-350.
54. Baines C.P. The cardiac mitochondrion: nexus of stress. Annu Rev Physiol 2010, 72:61-80.
55. Vaseva A.V., Marchenko N.D., Ji K., Tsirka S.E., Holzmann S., Moll U.M. P53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell Jun 22 2012, 149(7):1536-1548.
56. Liu J., van Mil A., Vrijsen K., Zhao J., Gao L., Metz C.H., et al. MicroRNA-155 prevents necrotic cell death in human cardiomyocyte progenitor cells via targeting RIP1. J Cell Mol Med Jul 2011, 15(7):1474-1482.
57. Wang K., Liu F., Zhou L.Y., Ding S.L., Long B., Liu C.Y., et al. miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death Dis Jul 4 2013, 4:e709.
58. Frank D., Gantenberg J., Boomgaarden I., Kuhn C., Will R., Jarr K.U., et al. MicroRNA-20a inhibits stress-induced cardiomyocyte apoptosis involving its novel target Egln3/PHD3. J Mol Cell Cardiol Mar 2012, 52(3):711-717.
59. 2)-induced apoptosis through targeting the mitochondria apoptotic pathway. PLoS One 2012, 7(9).
60. Qian L., Van Laake L.W., Huang Y., Liu S., Wendland M.F., Srivastava D. miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J Exp Med Mar 14 2011, 208(3):549-560.
61. Du W., Pan Z., Chen X., Wang L., Zhang Y., Li S., et al. By targeting Stat3 microRNA-17-5p promotes cardiomyocyte apoptosis in response to ischemia followed by reperfusion. Cell Physiol Biochem 2014, 34(3):955-965.
62. Forini F., Kusmic C., Nicolini G., Mariani L., Zucchi R., Matteucci M., et al. Triiodothyronine prevents cardiac ischemia/reperfusion mitochondrial impairment and cell loss by regulating miR30a/p53 Axis. Endocrinology Nov 2014, 155(11):4581-4590.
63. Yeh C.H., Chen T.P., Wang Y.C., Lin Y.M., Fang S.W. Carvedilol treatment after myocardial infarct decreases cardiomyocytic apoptosis in the peri-infarct zone during cardioplegia-induced cardiac arrest. Shock Apr 2013, 39(4):343-352.
64. Narula J., Haider N., Virmani R., DiSalvo T.G., Kolodgie F.D., Hajjar R.J., et al. Apoptosis in myocytes in end-stage heart failure. N Engl J Med Oct 17 1996, 335(16):1182-1189.
65. Teiger E., Than V.D., Richard L., Wisnewsky C., Tea B.S., Gaboury L., et al. Apoptosis in pressure overload-induced heart hypertrophy in the rat. J Clin Invest Jun 15 1996, 97(12):2891-2897.
66. Pimentel D.R., Amin J.K., Xiao L., Miller T., Viereck J., Oliver-Krasinski J., et al. Reactive oxygen species mediate amplitude-dependent hypertrophic and apoptotic responses to mechanical stretch in cardiac myocytes. Circ Res Aug 31 2001, 89(5):453-460.
67. Chen X., Gong J., Zeng H., Chen N., Huang R., Huang Y., et al. MicroRNA145 targets BNIP3 and suppresses prostate cancer progression. Cancer Res Apr 1 2010, 70(7):2728-2738.
68. Lin Y., Liu X., Cheng Y., Yang J., Huo Y., Zhang C. Involvement of microRNAs in hydrogen peroxide-mediated gene regulation and cellular injury response in vascular smooth muscle cells. J Biol Chem Mar 20 2009, 284(12):7903-7913.
69. Ng I.H., Yeap Y.Y., Ong L.S., Jans D.A., Bogoyevitch M.A. Oxidative stress impairs multiple regulatory events to drive persistent cytokine-stimulated STAT3 phosphorylation. Biochim Biophys Acta Mar 2014, 1843(3):483-494.
70. Xu C., Hu Y., Hou L., Ju J., Li X., Du N., et al. beta-Blocker carvedilol protects cardiomyocytes against oxidative stress-induced apoptosis by up-regulating miR-133 expression. J Mol Cell Cardiol Oct 2014, 75:111-121.
71. Li J., Donath S., Li Y., Qin D., Prabhakar B.S., Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet Jan 2010, 6(1):e1000795.
72. Zhu H., Fan G.C. Role of microRNAs in the reperfused myocardium towards post-infarct remodelling. Cardiovasc Res May 1 2012, 94(2):284-292.
73. He B., Xiao J., Ren A.J., Zhang Y.F., Zhang H., Chen M., et al. Role of miR-1 and miR-133a in myocardial ischemic postconditioning. J Biomed Sci Mar 16 2011, 18. (22-0127-18-22).
74. Choi A.M., Ryter S.W., Levine B. Autophagy in human health and disease. N Engl J Med 2013, 368(7):651-662.
75. Nishida K., Yamaguchi O., Otsu K. Crosstalk between autophagy and apoptosis in heart disease. Circ Res Aug 15 2008, 103(4):343-351.
76. Taneike M., Yamaguchi O., Nakai A., Hikoso S., Takeda T., Mizote I., et al. Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy Jul 2010, 6(5):600-606.
77. Ucar A., Gupta S.K., Fiedler J., Erikci E., Kardasinski M., Batkai S., et al. The miRNA-212/132 family regulates both cardiac hypertrophy and cardiomyocyte autophagy. Nat Commun 2012, 3:1078.
78. Sciarretta S., Volpe M., Sadoshima J. Mammalian target of rapamycin signaling in cardiac physiology and disease. Circ Res Jan 31 2014, 114(3):549-564.
79. Li Q., Xie J., Li R., Shi J., Sun J., Gu R., et al. Overexpression of microRNA-99a attenuates heart remodelling and improves cardiac performance after myocardial infarction. J Cell Mol Med May 2014, 18(5):919-928.
80. Bo L., Su-Ling D., Fang L., Lu-Yu Z., Tao A., Stefan D., et al. Autophagic program is regulated by miR-325. Cell Death Differ Jun 2014, 21(6):967-977.
81. Pan W., Zhong Y., Cheng C., Liu B., Wang L., Li A., et al. MiR-30-regulated autophagy mediates angiotensin II-induced myocardial hypertrophy. PLoS One 2013, 8(1):e53950.
82. Huang J., Sun W., Huang H., Ye J., Pan W., Zhong Y., et al. miR-34a modulates angiotensin II-induced myocardial hypertrophy by direct inhibition of ATG9A expression and autophagic activity. PLoS One Apr 11 2014, 9(4):e94382.
83. Song L., Su M., Wang S., Zou Y., Wang X., Wang Y., et al. MiR-451 is decreased in hypertrophic cardiomyopathy and regulates autophagy by targeting TSC1. J Cell Mol Med Sep 2014, 11.
84. Schlossarek S., Englmann D.R., Sultan K.R., Sauer M., Eschenhagen T., Carrier L. Defective proteolytic systems in Mybpc3-targeted mice with cardiac hypertrophy. Basic Res Cardiol Jan 2012, 107(1):235. -011-0235-3.
85. Brockdorff N., Ashworth A., Kay G.F., McCabe V.M., Norris D.P., Cooper P.J., et al. The product of the mouse Xist gene is a 15kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell Oct 30 1992, 71(3):515-526.
86. Brown C.J., Hendrich B.D., Rupert J.L., Lafreniere R.G., Xing Y., Lawrence J., et al. The human XIST gene: analysis of a 17kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell Oct 30 1992, 71(3):527-542.
87. Papait R., Kunderfranco P., Stirparo G.G., Latronico M.V., Condorelli G. Long noncoding RNA: a new player of heart failure?. J Cardiovasc Transl Res Dec 2013, 6(6):876-883.
88. Wang K.C., Chang H.Y. Molecular mechanisms of long noncoding RNAs. Mol Cell Sep 16 2011, 43(6):904-914.
89. Maass P.G., Luft F.C., Bahring S. Long non-coding RNA in health and disease. J Mol Med (Berl) Apr 2014, 92(4):337-346.
90. Zhao Y., Feng G., Wang Y., Yue Y., Zhao W. Regulation of apoptosis by long non-coding RNA HIF1A-AS1 in VSMCs: implications for TAA pathogenesis. Int J Clin Exp Pathol Oct 15 2014, 7(11):7643-7652.
91. Zheng H., Yang S., Yang Y., Yuan S.X., Wu F.Q., Wang L.L., et al. Epigenetically silenced long noncoding-SRHC promotes proliferation of hepatocellular carcinoma. J Cancer Res Clin Oncol Dec 16 2014, (in press).
92. Nie F., Sun M., Yang J., Xie M., Xu T., Xia R., et al. Long noncoding RNA ANRIL promotes non-small cell lung cancer cell proliferation and inhibits apoptosis by silencing KLF2 and P21 expression. Mol Cancer Ther Dec 2014, 12.
93. Liz J., Portela A., Soler M., Gomez A., Ling H., Michlewski G., et al. Regulation of pri-miRNA processing by a long noncoding RNA transcribed from an ultraconserved region. Mol Cell Jul 3 2014, 55(1):138-147.
94. Wang K., Long B., Zhou L.Y., Liu F., Zhou Q.Y., Liu C.Y., et al. CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 downregulation. Nat Commun Apr 7 2014, 5:3596.
95. Stenvang J., Petri A., Lindow M., Obad S., Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence Jan 9 2012, 3(1). (1-907X-3-1).
96. Jessup M., Greenberg B., Mancini D., Cappola T., Pauly D.F., Jaski B., et al. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID): a phase 2trial of intracoronary gene therapy of sarcoplasmic reticulum Ca2+-ATPase in patients with advanced heart failure. Circulation 2011, 124(3):304-313.