Small molecules, big effects: The role of microRNAs in regulation of cardiomyocyte death

Cell Death and Disease

Volumn 5, Issue 7, 2014, Pages

  Skommer, J ^a   Rana, I ^a   Marques, F Z ^a   Zhu, W ^b   Du, Z ^b   Charchar, F J ^a  

^a UNIVERSITY OF BALLARAT   (Australia)

^b THE SECOND AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

APOPTOSIS; AUTOPHAGY; BIOINFORMATICS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; CELL DEATH; CELL SURVIVAL; GENE EXPRESSION; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; INTRACELLULAR SIGNALING; NECROPTOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; APOPTOSIS; CARDIOVASCULAR DISEASES; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; MYOCYTES, CARDIAC;

EID: 84905504653     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.287     Document Type: Review

References (197)

1. Orogo AM, Gustafsson AB. Cell death in the myocardium: my heart won't go on. IUBMB Life 2013; 65: 651-656
2. Konstantinidis K, Whelan RS, Kitsis RN. Mechanisms of cell death in heart disease. Arterioscler Thromb Vasc Biol 2012; 32: 1552-1562
3. Reeve JL, Duffy AM, O'Brien T, Samali A. Don't lose heart-therapeutic value of apoptosis prevention in the treatment of cardiovascular disease. J Cell Mol Med 2005; 9: 609-622
4. Vela L, Gonzalo O, Naval J, Marzo I. Direct interaction of Bax and Bak proteins with Bcl-2 homology domain 3 (BH3)-only proteins in living cells revealed by fluorescence complementation. J Biol Chem 2013; 288: 4935-4946
5. Dussmann H, Rehm M, Concannon CG, Anguissola S, Wurstle M, Kacmar S et al. Singlecell quantification of Bax activation and mathematical modelling suggest pore formation on minimal mitochondrial Bax accumulation. Cell Death Differ 2010; 17: 278-290
6. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Mol Cell 2010; 37: 299-310
7. Ow YP, Green DR, Hao Z, Mak TW. Cytochrome c: functions beyond respiration. Nat Rev Mol Cell Biol 2008; 9: 532-542
8. Mace PD, Riedl SJ. Molecular cell death platforms and assemblies. Curr Opin Cell Biol 2010; 22: 828-836
9. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK. Non-genetic origins of cell-tocell variability in TRAIL-induced apoptosis. Nature 2009; 459: 428-432
10. Skommer J, Raychaudhuri S, Wlodkowic D. Timing is everything: stochastic origins of cell-to-cell variability in cancer cell death. Front Biosci (Landmark Ed) 2011; 16: 307-314
11. Skommer J, Brittain T, Raychaudhuri S. Bcl-2 inhibits apoptosis by increasing the timeto- death and intrinsic cell-to-cell variations in the mitochondrial pathway of cell death. Apoptosis 2010; 15: 1223-1233
12. Gaudet S, Spencer SL, Chen WW, Sorger PK. Exploring the contextual sensitivity of factors that determine cell-to-cell variability in receptor-mediated apoptosis. PLoS Comput Biol 2012; 8: e1002482
13. Ohtani K, Dimmeler S. Control of cardiovascular differentiation by microRNAs. Basic Res Cardiol 2011; 106: 5-11
14. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011; 12: 99-110
15. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011; 39(Database issue): D152-D157
16. Leite-Moreira AM, Lourenco AP, Falcao-Pires I, Leite-Moreira AF. Pivotal role of microRNAs in cardiac physiology and heart failure. Drug Discov Today 2013; 18: 1243-1249
17. Kumarswamy R, Thum T. Non-coding RNAs in cardiac remodeling and heart failure. Circ Res 2013; 113: 676-689
18. Ono K, Kuwabara Y, Han J. MicroRNAs and cardiovascular diseases. FEBS J 2011; 278: 1619-1633
19. Da Sacco L, Masotti A. Recent insights and novel bioinformatics tools to understand the role of microRNAs binding to 5' untranslated region. Int J Mol Sci 2012; 14: 480-495
20. Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 2012; 13: 271-282
21. Lytle JR, Yario TA, Steitz JA. Target mRNAs are repressed as efficiently by microRNAbinding sites in the 5' UTR as in the 3' UTR. Proc Natl Acad Sci USA 2007; 104: 9667-9672
22. Orom UA, Nielsen FC, Lund AH. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 2008; 30: 460-471
23. Vasudevan S. Posttranscriptional upregulation by microRNAs. Wiley Interdiscip Rev RNA 2012; 3: 311-330
24. Berezikov E. Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 2011; 12: 846-860
25. Bernardo BC, Charchar FJ, Lin RC, McMullen JR. A microRNA guide for clinicians and basic scientists: background and experimental techniques. Heart Lung Circ 2012; 21: 131-142
26. Graves P, Zeng Y. Biogenesis of mammalian microRNAs: a global view. Genomics Proteomics Bioinformatics 2012; 10: 239-245
27. Bhayani MK, Calin GA, Lai SY. Functional relevance of miRNA sequences in human disease. Mutat Res 2012; 731: 14-19
28. Witkos TM, Koscianska E, Krzyzosiak WJ. Practical aspects of microRNA target prediction. Curr Mol Med 2011; 11: 93-109
29. Saxena A, Tabin CJ. miRNA-processing enzyme Dicer is necessary for cardiac outflow tract alignment and chamber septation. Proc Natl Acad Sci USA 2010; 107: 87-91
30. da Costa Martins PA, Bourajjaj M, Gladka M, Kortland M, van Oort RJ, Pinto YM et al. Conditional dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling. Circulation 2008; 118: 1567-1576
31. Chen JF, Murchison EP, Tang R, Callis TE, Tatsuguchi M, Deng Z et al. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci USA 2008; 105: 2111-2116
32. Leist M, Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001; 2: 589-598
33. Meier P, Vousden KH. Lucifer's labyrinth-ten years of path finding in cell death. Mol Cell 2007; 28: 746-754
34. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009; 16: 3-11
35. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 2009; 7: 99-109
36. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004; 116: 205-219
37. Skommer J, Wlodkowic D, Deptala A. Larger than life: mitochondria and the Bcl-2 family. Leuk Res 2007; 31: 277-286
38. Danial NN. BCL-2 family proteins: critical checkpoints of apoptotic cell death. Clin Cancer Res 2007; 13: 7254-7263
39. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002; 2: 647-656
40. Gonzalvez F, Ashkenazi A. New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 2010; 29: 4752-4765
41. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 2004; 95: 957-970
42. Takemura G, Fujiwara H. Role of apoptosis in remodeling after myocardial infarction. Pharmacol Ther 2004; 104: 1-16
43. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 1994; 94: 1621-1628
44. Fliss H, Gattinger D. Apoptosis in ischemic and reperfused rat myocardium. Circ Res 1996; 79: 949-956
45. Freude B, Masters TN, Robicsek F, Fokin A, Kostin S, Zimmermann R et al. Apoptosis is initiated by myocardial ischemia and executed during reperfusion. J Mol Cell Cardiol 2000; 32: 197-208
46. Wang XL, Liu HR, Tao L, Liang F, Yan L, Zhao RR et al. Role of iNOS-derived reactive nitrogen species and resultant nitrative stress in leukocytes-induced cardiomyocyte apoptosis after myocardial ischemia/ reperfusion. Apoptosis 2007; 12: 1209-1217.
47. Lee Y, Gustafsson AB. Role of apoptosis in cardiovascular disease. Apoptosis 2009; 14: 536-548
48. Narula J, Pandey P, Arbustini E, Haider N, Narula N, Kolodgie FD et al. Apoptosis in heart failure: release of cytochrome c from mitochondria and activation of caspase-3 in human cardiomyopathy. Proc Natl Acad Sci USA 1999; 96: 8144-8149
49. Scheubel RJ, Bartling B, Simm A, Silber RE, Drogaris K, Darmer D et al. Apoptotic pathway activation from mitochondria and death receptors without caspase-3 cleavage in failing human myocardium: fragile balance of myocyte survival? J Am Coll Cardiol 2002; 39: 481-488
50. Malmberg M, Parkka J, Vahasilta T, Saraste A, Laitio T, Kiss J et al. Cardiomyocyte apoptosis after cardioplegic ischemia: comparison to unprotected regional ischemiareperfusion. Eur Surg Res 2011; 46: 19-25
51. Vahasilta T, Malmberg M, Saraste A, Koskenvuo JW, Parkka JP, Valtonen M et al. Cardiomyocyte apoptosis after antegrade and retrograde cardioplegia during aortic valve surgery. Ann Thorac Surg 2011; 92: 1351-1357
52. Roy N, Friehs I, Cowan DB, Zurakowski D, McGowan FX, del Nido PJ. Dopamine induces postischemic cardiomyocyte apoptosis in vivo: an effect ameliorated by propofol. Ann Thorac Surg 2006; 82: 2192-2199
53. Kristen AV, Ackermann K, Buss S, Lehmann L, Schnabel PA, Haunstetter A et al. Inhibition of apoptosis by the intrinsic but not the extrinsic apoptotic pathway in myocardial ischemia-reperfusion. Cardiovasc Pathol 2013; 22: 280-286
54. Gilles S, Zahler S, Welsch U, Sommerhoff CP, Becker BF. Release of TNF-alpha during myocardial reperfusion depends on oxidative stress and is prevented by mast cell stabilizers. Cardiovasc Res 2003; 60: 608-616
55. Dorge H, Schulz R, Belosjorow S, Post H, van de Sand A, Konietzka I et al. Coronary microembolization: the role of TNF-alpha in contractile dysfunction. J Mol Cell Cardiol 2002; 34: 51-62
56. Lee P, Sata M, Lefer DJ, Factor SM, Walsh K, Kitsis RN. Fas pathway is a critical mediator of cardiac myocyte death and MI during ischemia-reperfusion in vivo. Am J Physiol Heart Circ Physiol 2003; 284: H456-H463
57. Chien H, Dix RD. Evidence for multiple cell death pathways during development of experimental cytomegalovirus retinitis in mice with retrovirus-induced immunosuppression: apoptosis, necroptosis, and pyroptosis. J Virol 2012; 86: 10961-10978
58. Goc A, Kochuparambil ST, Al-Husein B, Al-Azayzih A, Mohammad S, Somanath PR. Simultaneous modulation of the intrinsic and extrinsic pathways by simvastatin in mediating prostate cancer cell apoptosis. BMC Cancer 2012; 12: 409
59. Rosato RR, Almenara JA, Dai Y, Grant S. Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Mol Cancer Ther 2003; 2: 1273-1284
60. Lin CC, Yang JS, Chen JT, Fan S, Yu FS, Yang JL et al. Berberine induces apoptosis in human HSC-3 oral cancer cells via simultaneous activation of the death receptor-mediated and mitochondrial pathway. Anticancer Res 2007; 27: 3371-3378
61. Jeremias I, Kupatt C, Martin-Villalba A, Habazettl H, Schenkel J, Boekstegers P et al. Involvement of CD95/Apo1/Fas in cell death after myocardial ischemia. Circulation 2000; 102: 915-920
62. Long B, Wang K, Li N, Murtaza I, Xiao JY, Fan YY et al. miR-761 regulates the mitochondrial network by targeting mitochondrial fission factor. Free Radic Biol Med 2013; 65: 371-379
63. Otera H, Wang C, Cleland MM, Setoguchi K, Yokota S, Youle RJ et al. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 2010; 191: 1141-1158
64. Sundaresan NR, Pillai VB, Gupta MP. Emerging roles of SIRT1 deacetylase in regulating cardiomyocyte survival and hypertrophy. J Mol Cell Cardiol 2011; 51: 614-618
65. Yamamoto T, Sadoshima J. Protection of the heart against ischemia/reperfusion by silent information regulator 1. Trends Cardiovasc Med 2011; 21: 27-32
66. Hsu CP, Zhai P, Yamamoto T, Maejima Y, Matsushima S, Hariharan N et al. Silent information regulator 1 protects the heart from ischemia/reperfusion. Circulation 2010; 122: 2170-2182
67. Cha MJ, Jang JK, Ham O, Song BW, Lee SY, Lee CY et al. MicroRNA-145 suppresses ROS-induced Ca2+ overload of cardiomyocytes by targeting CaMKIIdelta. Biochem Biophys Res Commun 2013; 435: 720-726
68. Meloni M, Marchetti M, Garner K, Littlejohns B, Sala-Newby G, Xenophontos N et al. Local inhibition of microRNA-24 improves reparative angiogenesis and left ventricle remodeling and function in mice with myocardial infarction. Mol Ther 2013; 21: 1390-1402
69. Zhou M, Cai J, Tang Y, Zhao Q. MiR-17-92 cluster is a novel regulatory gene of cardiac ischemic/reperfusion injury. Med Hypotheses 2013; 81: 108-110
70. van Empel VP, De Windt LJ. Myocyte hypertrophy and apoptosis: a balancing act. Cardiovasc Res 2004; 63: 487-499
71. Zhu W, Zhao Y, Xu Y, Sun Y, Wang Z, Yuan W et al. Dissection of protein interactomics highlights MicroRNA synergy. PLoS One 2013; 8: e63342
72. Naeem H, Kuffner R, Csaba G, Zimmer R. miRSel: automated extraction of associations between microRNAs and genes from the biomedical literature. BMC Bioinformatics 2010; 11: 135
73. Zhai P, Eurell TE, Cooke PS, Lubahn DB, Gross DR. Myocardial ischemia-reperfusion injury in estrogen receptor-alpha knockout and wild-type mice. Am J Physiol Heart Circ Physiol 2000; 278: H1640-H1647
74. Pelzer T, Schumann M, Neumann M, deJager T, Stimpel M, Serfling E et al. 17beta-estradiol prevents programmed cell death in cardiac myocytes. Biochem Biophys Res Commun 2000; 268: 192-200
75. Gabel SA, Walker VR, London RE, Steenbergen C, Korach KS, Murphy E. Estrogen receptor beta mediates gender differences in ischemia/reperfusion injury. J Mol Cell Cardiol 2005; 38: 289-297
76. Shen T, Yang C, Ding L, Zhu Y, Ruan Y, Cheng H et al. Tbx20 functions as an important regulator of estrogen-mediated cardiomyocyte protection during oxidative stress. Int J Cardiol 2013; 168: 3704-3714
77. Knowlton AA, Lee AR. Estrogen and the cardiovascular system. Pharmacol Ther 2012; 135: 54-70
78. Puzianowska-Kuznicka M. ESR1 in myocardial infarction. Clin Chim Acta 2012; 413: 81-87
79. Cao J, Zhu T, Lu L, Geng L, Wang L, Zhang Q et al. Estrogen induces cardioprotection in male C57BL/6J mice after acute myocardial infarction via decreased activity of matrix metalloproteinase-9 and increased Akt-Bcl-2 anti-apoptotic signaling. Int J Mol Med 2011; 28: 231-237
80. Voss MR, Stallone JN, Li M, Cornelussen RN, Knuefermann P, Knowlton AA. Gender differences in the expression of heat shock proteins: the effect of estrogen. Am J Physiol Heart Circ Physiol 2003; 285: H687-H692
81. Kam KW, Qi JS, Chen M, Wong TM. Estrogen reduces cardiac injury and expression of beta1-adrenoceptor upon ischemic insult in the rat heart. J Pharmacol Exp Ther 2004; 309: 8-15
82. Wang M, Crisostomo P, Wairiuko GM, Meldrum DR. Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 2006; 290: H2204-H2209
83. Wang M, Crisostomo PR, Markel T, Wang Y, Lillemoe KD, Meldrum DR. Estrogen receptor beta mediates acute myocardial protection following ischemia. Surgery 2008; 144: 233-238
84. Liou CM, Yang AL, Kuo CH, Tin H, Huang CY, Lee SD. Effects of 17beta-estradiol on cardiac apoptosis in ovariectomized rats. Cell Biochem Funct 2010; 28: 521-528
85. Liu H, Pedram A, Kim JK. Oestrogen prevents cardiomyocyte apoptosis by suppressing p38alpha-mediated activation of p53 and by down-regulating p53 inhibition on p38beta. Cardiovasc Res 2011; 89: 119-128
86. Kim JK, Pedram A, Razandi M, Levin ER. Estrogen prevents cardiomyocyte apoptosis through inhibition of reactive oxygen species and differential regulation of p38 kinase isoforms. J Biol Chem 2006; 281: 6760-6767
87. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol 2010; 221: 3-12
88. Kubli DA, Gustafsson AB. Mitochondria and mitophagy: the yin and yang of cell death control. Circ Res 2012; 111: 1208-1221
89. Marzetti E, Csiszar A, Dutta D, Balagopal G, Calvani R, Leeuwenburgh C. Role of mitochondrial dysfunction and altered autophagy in cardiovascular aging and disease: from mechanisms to therapeutics. Am J Physiol Heart Circ Physiol 2013; 305: H459-H476
90. Dutta D, Calvani R, Bernabei R, Leeuwenburgh C, Marzetti E. Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ Res 2012; 110: 1125-1138
91. Gottlieb RA, Mentzer RM Jr. Autophagy: an affair of the heart. Heart Fail Rev 2013; 18: 575-584
92. Nishida K, Kyoi S, Yamaguchi O, Sadoshima J, Otsu K. The role of autophagy in the heart. Cell Death Differ 2009; 16: 31-38
93. Singh KK, Yanagawa B, Quan A, Wang R, Garg A, Khan R et al. Autophagy gene fingerprint in human ischemia and reperfusion. J Thorac Cardiovasc Surg 2013; 147: 1065-1072
94. Dutta D, Xu J, Kim JS, Dunn WA Jr, Leeuwenburgh C. Upregulated autophagy protects cardiomyocytes from oxidative stress-induced toxicity. Autophagy 2013; 9: 328-344
95. Kanamori H, Takemura G, Goto K, Maruyama R, Ono K, Nagao K et al. Autophagy limits acute myocardial infarction induced by permanent coronary artery occlusion. Am J Physiol Heart Circ Physiol 2011; 300: H2261-H2271
96. 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 2010; 6: 600-606
97. Takemura G, Kanamori H, Goto K, Maruyama R, Tsujimoto A, Fujiwara H et al. Autophagy maintains cardiac function in the starved adult. Autophagy 2009; 5: 1034-1036
98. Tannous P, Zhu H, Johnstone JL, Shelton JM, Rajasekaran NS, Benjamin IJ et al. Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc Natl Acad Sci USA 2008; 105: 9745-9750
99. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 2007; 13: 619-624
100. Zhao Y, Xue T, Yang X, Zhu H, Ding X, Lou L et al. Autophagy plays an important role in sunitinib-mediated cell death in H9c2 cardiac muscle cells. Toxicol Appl Pharmacol 2010; 248: 20-27
101. Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X et al. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy 2009; 5: 816-823.
102. Meenhuis A, van Veelen PA, de Looper H, van Boxtel N, van den Berge IJ, Sun SM et al. MiR-17/20/93/106 promote hematopoietic cell expansion by targeting sequestosome 1-regulated pathways in mice. Blood 2011; 118: 916-925
103. Comincini S, Allavena G, Palumbo S, Morini M, Durando F, Angeletti F et al. microRNA- 17 regulates the expression of ATG7 and modulates the autophagy process, improving the sensitivity to temozolomide and low-dose ionizing radiation treatments in human glioblastoma cells. Cancer Biol Ther 2013; 14: 574-586
104. Li SH, Guo J, Wu J, Sun Z, Han M, Shan SW et al. miR-17 targets tissue inhibitor of metalloproteinase 1 and 2 to modulate cardiac matrix remodeling. FASEB J 2013; 27: 4254-4265
105. Shen S, Niso-Santano M, Adjemian S, Takehara T, Malik SA, Minoux H et al. Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity. Mol Cell 2012; 48: 667-680
106. Elschami M, Scherr M, Philippens B, Gerardy-Schahn R. Reduction of STAT3 expression induces mitochondrial dysfunction and autophagy in cardiac HL-1 cells. Eur J Cell Biol 2013; 92: 21-29
107. Podewski EK, Hilfiker-Kleiner D, Hilfiker A, Morawietz H, Lichtenberg A, Wollert KC et al. Alterations in Janus kinase (JAK)-signal transducers and activators of transcription (STAT) signaling in patients with end-stage dilated cardiomyopathy. Circulation 2003; 107: 798-802
108. Boengler K, Buechert A, Heinen Y, Roeskes C, Hilfiker-Kleiner D, Heusch G et al. Cardioprotection by ischemic postconditioning is lost in aged and STAT3-deficient mice. Circ Res 2008; 102: 131-135
109. Cambi GE, Lucchese G, Djeokeng MM, Modesti A, Fiaschi T, Faggian G et al. Impaired JAK2-induced activation of STAT3 in failing human myocytes. Mol Biosyst 2012; 8: 2351-2359
110. Hoshino A, Matoba S, Iwai-Kanai E, Nakamura H, Kimata M, Nakaoka M et al. p53- TIGAR axis attenuates mitophagy to exacerbate cardiac damage after ischemia. J Mol Cell Cardiol 2012; 52: 175-184
111. Bensaad K, Cheung EC, Vousden KH. Modulation of intracellular ROS levels by TIGAR controls autophagy. EMBO J 2009; 28: 3015-3026
112. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006; 126: 107-120
113. Kimata M, Matoba S, Iwai-Kanai E, Nakamura H, Hoshino A, Nakaoka M et al. p53 and TIGAR regulate cardiac myocyte energy homeostasis under hypoxic stress. Am J Physiol Heart Circ Physiol 2010; 299: H1908-H1916
114. Giansanti V, Torriglia A, Scovassi AI. Conversation between apoptosis and autophagy: 'Is it your turn or mine?'. Apoptosis 2011; 16: 321-333
115. Nishida K, Yamaguchi O, Otsu K. Crosstalk between autophagy and apoptosis in heart disease. Circ Res 2008; 103: 343-351
116. Marquez RT, Xu L. Bcl-2:Beclin 1 complex: multiple, mechanisms regulating autophagy/ apoptosis toggle switch. Am J Cancer Res 2012; 2: 214-221
117. Luo S, Rubinsztein DC. BCL2L11/BIM: a novel molecular link between autophagy and apoptosis. Autophagy 2013; 9: 104-105
118. Luo S, Garcia-Arencibia M, Zhao R, Puri C, Toh PP, Sadiq O et al. Bim inhibits autophagy by recruiting Beclin 1 to microtubules. Mol Cell 2012; 47: 359-370
119. Wirawan E, Vande Walle L, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I et al. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 2010; 1: e18
120. Li H, Wang P, Sun Q, Ding WX, Yin XM, Sobol RW et al. Following cytochrome c release, autophagy is inhibited during chemotherapy-induced apoptosis by caspase 8-mediated cleavage of Beclin 1. Cancer Res 2011; 71: 3625-3634
121. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L et al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8: 1124-1132
122. Yin X, Cao L, Kang R, Yang M, Wang Z, Peng Y et al. UV irradiation resistanceassociated gene suppresses apoptosis by interfering with BAX activation. EMBO Rep 2011; 12: 727-734
123. Rubinstein AD, Eisenstein M, Ber Y, Bialik S, Kimchi A. The autophagy protein Atg12 associates with antiapoptotic Bcl-2 family members to promote mitochondrial apoptosis. Mol Cell 2011; 44: 698-709
124. Pyo JO, Jang MH, Kwon YK, Lee HJ, Jun JI, Woo HN et al. Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death. J Biol Chem 2005; 280: 20722-20729
125. Boon RA, Iekushi K, Lechner S, Seeger T, Fischer A, Heydt S et al. MicroRNA-34a regulates cardiac ageing and function. Nature 2013; 495: 107-110
126. Kavela S, Shinde SR, Ratheesh R, Viswakalyan K, Bashyam MD, Gowrishankar S et al. PNUTS functions as a proto-oncogene by sequestering PTEN. Cancer Res 2013; 73: 205-214
127. Ng F, Tang BL. Sirtuins' modulation of autophagy. J Cell Physiol 2013; 228: 2262-2270
128. Salminen A, Kaarniranta K. SIRT1: regulation of longevity via autophagy. Cell Signal 2009; 21: 1356-1360
129. Fyhrquist F, Saijonmaa O. Telomere length and cardiovascular aging. Ann Med 2012; 44(Suppl 1): S138-S142
130. Ivanov A, Pawlikowski J, Manoharan I, van Tuyn J, Nelson DM, Rai TS et al. Lysosomemediated processing of chromatin in senescence. J Cell Biol 2013; 202: 129-143
131. Wang F, Chen HZ, Lv X, Liu DP. SIRT1 as a novel potential treatment target for vascular aging and age-related vascular diseases. Curr Mol Med 2013; 13: 155-164
132. Ota H, Eto M, Ogawa S, Iijima K, Akishita M, Ouchi Y. SIRT1/eNOS axis as a potential target against vascular senescence, dysfunction and atherosclerosis. J Atheroscler Thromb 2010; 17: 431-435
133. Henriquez M, Armisen R, Stutzin A, Quest AF. Cell death by necrosis, a regulated way to go. Curr Mol Med 2008; 8: 187-206
134. Wu W, Liu P, Li J. Necroptosis: an emerging form of programmed cell death. Crit Rev Oncol Hematol 2012; 82: 249-258
135. Guerra S, Leri A, Wang X, Finato N, Di Loreto C, Beltrami CA et al. Myocyte death in the failing human heart is gender dependent. Circ Res 1999; 85: 856-866
136. Smith CC, Davidson SM, Lim SY, Simpkin JC, Hothersall JS, Yellon DM. Necrostatin: a potentially novel cardioprotective agent? Cardiovasc Drugs Ther 2007; 21: 227-233
137. Bamber AR, Pryce J, Cook A, Ashworth M, Sebire NJ. Myocardial necrosis and infarction in newborns and infants. Forensic Sci Med Pathol 2013; 9: 521-527
138. Wang K, Liu F, Zhou LY, Ding SL, Long B, Liu CY et al. miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death Dis 2013; 4: e709
139. O'Donnell MA, Perez-Jimenez E, Oberst A, Ng A, Massoumi R, Xavier R et al. Caspase 8 inhibits programmed necrosis by processing CYLD. Nat Cell Biol 2011; 13: 1437-1442
140. Liu J, van Mil A, Vrijsen K, Zhao J, Gao L, Metz CH et al. MicroRNA-155 prevents necrotic cell death in human cardiomyocyte progenitor cells via targeting RIP1. J Cell Mol Med 2011; 15: 1474-1482
141. Zhang YY, Liu H. Connections between various trigger factors and the RIP1/ RIP3 signaling pathway involved in necroptosis. Asian Pac J Cancer Prev 2013; 14: 7069-7074
142. Chiong M, Wang ZV, Pedrozo Z, Cao DJ, Troncoso R, Ibacache M et al. Cardiomyocyte death: mechanisms and translational implications. Cell Death Dis 2011; 2: e244
143. Smith CC, Yellon DM. Necroptosis, necrostatins and tissue injury. J Cell Mol Med 2011; 15: 1797-1806
144. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005; 434: 652-658
145. Frank SA. Evolution of robustness and cellular stochasticity of gene expression. PLoS Biol 2013; 11: e1001578
146. Giampieri E, Remondini D, de Oliveira L, Castellani G, Lio P. Stochastic analysis of a miRNA-protein toggle switch. Mol Biosyst 2011; 7: 2796-2803
147. Bostjancic E, Zidar N, Glavac D. MicroRNA microarray expression profiling in human myocardial infarction. Dis Markers 2009; 27: 255-268
148. Pan Z, Sun X, Ren J, Li X, Gao X, Lu C et al. miR-1 exacerbates cardiac ischemiareperfusion injury in mouse models. PLoS One 2012; 7: e50515
149. Glass C, Singla DK. MicroRNA-1 transfected embryonic stem cells enhance cardiac myocyte differentiation and inhibit apoptosis by modulating the PTEN/Akt pathway in the infarcted heart. Am J Physiol Heart Circ Physiol 2011; 301: H2038-H2049
150. Tang Y, Zheng J, Sun Y, Wu Z, Liu Z, Huang G. MicroRNA-1 regulates cardiomyocyte apoptosis by targeting Bcl-2. Int Heart J 2009; 50: 377-387
151. Yu XY, Song YH, Geng YJ, Lin QX, Shan ZX, Lin SG et al. Glucose induces apoptosis of cardiomyocytes via microRNA-1 and IGF-1. Biochem Biophys Res Commun 2008; 376: 548-552
152. Shan H, Li X, Pan Z, Zhang L, Cai B, Zhang Y et al. Tanshinone IIA protects against sudden cardiac death induced by lethal arrhythmias via repression of microRNA-1. Br J Pharmacol 2009; 158: 1227-1235
153. Zhang Y, Zhang L, Chu W, Wang B, Zhang J, Zhao M et al. Tanshinone IIA inhibits miR-1 expression through p38 MAPK signal pathway in post-infarction rat cardiomyocytes. Cell Physiol Biochem 2010; 26: 991-998
154. Karakikes I, Chaanine AH, Kang S, Mukete BN, Jeong D, Zhang S et al. Therapeutic cardiac-targeted delivery of miR-1 reverses pressure overload-induced cardiac hypertrophy and attenuates pathological remodeling. J Am Heart Assoc 2013; 2: e000078
155. Xu C, Lu Y, Pan Z, Chu W, Luo X, Lin H et al. 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 2007; 120(Pt 17): 3045-3052
156. He B, Xiao J, Ren AJ, Zhang YF, Zhang H, Chen M et al. Role of miR-1 and miR-133a in myocardial ischemic postconditioning. J Biomed Sci 2011; 18: 22
157. Li C, Fang Z, Jiang T, Zhang Q, Liu C, Zhang C et al. Serum microRNAs profile from genome-wide serves as a fingerprint for diagnosis of acute myocardial infarction and angina pectoris. BMC Med Genomics 2013; 6: 16
158. Zhou X, Mao A,Wang X, Duan X, Yao Y, Zhang C. Urine and serum microRNA-1 as novel biomarkers for myocardial injury in open-heart surgeries with cardiopulmonary bypass. PLoS One 2013; 8: e62245
159. van Mil A, Vrijsen KR, Goumans MJ, Metz CH, Doevendans PA, Sluijter JP. MicroRNA-1 enhances the angiogenic differentiation of human cardiomyocyte progenitor cells. J Mol Med (Berl) 2013; 91: 1001-1012
160. Willimott S, Wagner SD. Post-transcriptional and post-translational regulation of Bcl2. Biochem Soc Trans 2010; 38: 1571-1575
161. Liu LF, Liang Z, Lv ZR, Liu XH, Bai J, Chen J et al. MicroRNA-15a/b are up-regulated in response to myocardial ischemia/reperfusion injury. J Geriatr Cardiol 2012; 9: 28-32.
162. Hullinger TG, Montgomery RL, Seto AG, Dickinson BA, Semus HM, Lynch JM et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res 2012; 110: 71-81
163. Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernandez-Hernando C, Suarez Y. MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol 2011; 31: 2595-2606
164. Eitel I, Adams V, Dieterich P, Fuernau G, de Waha S, Desch S et al. Relation of circulating MicroRNA-133a concentrations with myocardial damage and clinical prognosis in ST-elevation myocardial infarction. Am Heart J 2012; 164: 706-714
165. Zhang L, Wu Y, Li Y, Xu C, Li X, Zhu D et al. Tanshinone IIA improves miR-133 expression through MAPK ERK1/2 pathway in hypoxic cardiac myocytes. Cell Physiol Biochem 2012; 30: 843-852
166. Danielson LS, Park DS, Rotllan N, Chamorro-Jorganes A, Guijarro MV, Fernandez-Hernando C et al. Cardiovascular dysregulation of miR-17-92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis. FASEB J 2013; 27: 1460-1467
167. van Almen GC, Verhesen W, van Leeuwen RE, van de Vrie M, Eurlings C, Schellings MW et al. MicroRNA-18 and microRNA-19 regulate CTGF and TSP-1 expression in age-related heart failure. Aging Cell 2011; 10: 769-779
168. Frank D, Gantenberg J, Boomgaarden I, Kuhn C, Will R, Jarr KU et al. MicroRNA-20a inhibits stress-induced cardiomyocyte apoptosis involving its novel target Egln3/PHD3. J Mol Cell Cardiol 2012; 52: 711-717
169. Qin DN, Qian L, Hu DL, Yu ZB, Han SP, Zhu C et al. Effects of miR-19b overexpression on proliferation, differentiation, apoptosis and Wnt/beta-catenin signaling pathway in P19 cell model of cardiac differentiation in vitro. Cell Biochem Biophys 2013; 66: 709-722
170. Qin Y, Yu Y, Dong H, Bian X, Guo X, Dong S. 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 2012; 9: 413-423
171. Sayed D, He M, Hong C, Gao S, Rane S, Yang Z et al. MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J Biol Chem 2010; 285: 20281-20290
172. Cheng Y, Liu X, Zhang S, Lin Y, Yang J, Zhang C. MicroRNA-21 protects against the H(2)O(2)-induced injury on cardiac myocytes via its target gene PDCD4. J Mol Cell Cardiol 2009; 47: 5-14
173. Cheng Y, Zhu P, Yang J, Liu X, Dong S, Wang X et al. Ischaemic preconditioningregulated miR-21 protects heart against ischaemia/reperfusion injury via anti-apoptosis through its target PDCD4. Cardiovasc Res 2010; 87: 431-439
174. Zeng J, Xiong Y, Li G, Liu M, He T, Tang Y et al. MiR-21 is overexpressed in response to high glucose and protects endothelial cells from apoptosis. Exp Clin Endocrinol Diabetes 2013; 121: 425-430
175. He J, Yue Y, Dong C, Xiong S. MiR-21 confers resistance against CVB3-induced myocarditis by inhibiting PDCD4-mediated apoptosis. Clin Invest Med 2013; 36: E103-E111
176. Kolpa HJ, Peal DS, Lynch SN, Giokas AC, Ghatak S, Misra S et al. miR-21 represses Pdcd4 during cardiac valvulogenesis. Development 2013; 140: 2172-2180
177. Qian L, Van Laake LW, Huang Y, Liu S, Wendland MF, Srivastava D. miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J Exp Med 2011; 208: 549-560
178. Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet 2010; 6: e1000795
179. Li X, Kong M, Jiang D, Qian J, Duan Q, Dong A. MicroRNA-150 aggravates H2O2-induced cardiac myocyte injury by down-regulating c-myb gene. Acta Biochim Biophys Sin (Shanghai) 2013; 45: 734-741
180. Mutharasan RK, Nagpal V, Ichikawa Y, Ardehali H. microRNA-210 is upregulated in hypoxic cardiomyocytes through Akt- and p53-dependent pathways and exerts cytoprotective effects. Am J Physiol Heart Circ Physiol 2011; 301: H1519-H1530
181. Rane S, He M, Sayed D, Vashistha H, Malhotra A, Sadoshima J et al. Downregulation of miR-199a derepresses hypoxia-inducible factor-1alpha and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res 2009; 104: 879-886
182. Ren XP, Wu J, Wang X, Sartor MA, Qian J, Jones K et al. MicroRNA-320 is
183. Ding SL, Wang JX, Jiao JQ, Tu X, Wang Q, Liu F et al. 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 2013; 288: 26865-26877
184. Wang JX, Jiao JQ, Li Q, Long B, Wang K, Liu JP et al. miR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat Med 2011; 17: 71-78
185. Lv G, Shao S, Dong H, Bian X, Yang X, Dong S. MicroRNA-214 protects cardiac myocytes against H O -induced injury. J Cell Biochem 2013
186. Aurora AB, Mahmoud AI, Luo X, Johnson BA, van Rooij E, Matsuzaki S et al. MicroRNA- 214 protects the mouse heart from ischemic injury by controlling Ca(2)(+) overload and cell death. J Clin Invest 2012; 122: 1222-1232
187. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C et al. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010; 107: 677-684
188. Fang J, Song XW, Tian J, Chen HY, Li DF, Wang JF et al. Overexpression of microRNA- 378 attenuates ischemia-induced apoptosis by inhibiting caspase-3 expression in cardiac myocytes. Apoptosis 2012; 17: 410-423
189. Zhu H, Yang Y, Wang Y, Li J, Schiller PW, Peng T. MicroRNA-195 promotes palmitateinduced apoptosis in cardiomyocytes by down-regulating Sirt1. Cardiovasc Res 2011; 92: 75-84
190. Tabuchi T, Satoh M, Itoh T, Nakamura M. MicroRNA-34a regulates the longevityassociated protein SIRT1 in coronary artery disease: effect of statins on SIRT1 and microRNA-34a expression. Clin Sci (Lond) 2012; 123: 161-171
191. Ito T, Yagi S, Yamakuchi M. MicroRNA-34a regulation of endothelial senescence. Biochem Biophys Res Commun 2010; 398: 735-740
192. 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: e53950
193. Jian X, Xiao-yan Z, Bin H, Yu-feng Z, Bo K, Zhi-nong W et al. MiR-204 regulate cardiomyocyte autophagy induced by hypoxia-reoxygenation through LC3-II. Int J Cardiol 2011; 148: 110-112
194. Courboulin A, Paulin R, Giguere NJ, Saksouk N, Perreault T, Meloche J et al. Role for miR-204 in human pulmonary arterial hypertension. J Exp Med 2011; 208: 535-548
195. Xiao J, Zhu X, He B, Zhang Y, Kang B, Wang Z et al. MiR-204 regulates cardiomyocyte autophagy induced by ischemia-reperfusion through LC3-II. J Biomed Sci 2011; 18: 35
196. Ucar A, Gupta SK, 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
197. Seca H, Lima RT, Lopes-Rodrigues V, Guimaraes JE, Almeida GM, Vasconcelos MH. Targeting miR-21 induces autophagy and chemosensitivity of leukemia cells. Curr Drug Targets 2013; 14: 1135-1143