The role of microRNA in cardiac excitability

Journal of Cardiovascular Pharmacology

Volumn 56, Issue 5, 2010, Pages 460-470

  Wang, Zhiguo ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

action potential; arrhythmia; cardiac excitability; gene expression; ion channel; miRNA

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; ANTISENSE OLIGONUCLEOTIDE; CHLORIDE CHANNEL; CONNEXIN 43; GAP JUNCTION PROTEIN; ION CHANNEL; MICRORNA; MICRORNA 21; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM CHANNEL; TANSHINONE IIA; TRANSFORMING GROWTH FACTOR BETA; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

APOPTOSIS; ARRHYTHMOGENESIS; BIOGENESIS; CALCIUM CELL LEVEL; GAP JUNCTION; HEART AUTOMATICITY; HEART CONDUCTION; HEART DEPOLARIZATION; HEART FAILURE; HEART INFARCTION; HEART MUSCLE EXCITABILITY; HEART MUSCLE POTENTIAL; HEART REPOLARIZATION; HEART VENTRICLE SEPTUM DEFECT; HUMAN; ISCHEMIC HEART DISEASE; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LONG QT SYNDROME; NONHUMAN; PRIORITY JOURNAL; REVIEW; STROKE;

ACTION POTENTIALS; ARRHYTHMIAS, CARDIAC; GENE EXPRESSION REGULATION; HEART CONDUCTION SYSTEM; HEART FAILURE; HUMANS; ION CHANNELS; MICRORNAS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC;

EID: 78650174737     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3181edb22c     Document Type: Review

References (96)

1. Nattel S, Maguy A, Le Bouter S, et al. Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev. 2007;87:425-456. (Pubitemid 47084677)
2. Carmeliet E. Cardiac ionic currents and acute ischemia: from channels to arrhythmias. Physiol Rev. 1999;79:917-1017.
3. Morita H, Wu J, Zipes DP. The QT syndromes: long and short. Lancet. 2008;372:750-763.
4. Viskin S. The QT interval: too long, too short or just right. Heart Rhythm. 2009;6:711-715.
5. Zaugg CE, Buser PT. When calcium turns arrhythmogenic: intracellular calcium handling during the development of hypertrophy and heart failure. Croat Med J. 2001;42:24-32.
6. Sipido KR, Bito V, Antoons G, et al. Na/Ca exchange and cardiac ventricular arrhythmias. Ann N Y Acad Sci. 2007;1099:339-348.
7. Tribulova N, Seki S, Radosinska J, et al. Myocardial Ca2+ handling and cell-to-cell coupling, key factors in prevention of sudden cardiac death. Can J Physiol Pharmacol. 2009;87:1120-1129.
8. Antoons G, Sipido KR. Targeting calcium handling in arrhythmias. Europace. 2008;10:1364-1369.
9. Day CP, McComb JM, Campbell RWF. QT dispersion: an indication of arrhythmia risk in patients with long QT intervals. Br Heart J. 1990;63: 342-344.
10. Gintant GA. Regional differences in IK density in canine left ventricle: role of IKs in electrical heterogeneity. Am J Physiol. 1995;268:H604-H613.
11. Liu DW, Gintant GA, Antzelevitch C. Ionic bases for electrophysiological distinctions among epicardial, midmyocardial, and endocardial myocytes from the free wall of the canine left ventricle. Circ Res. 1993;72:671-687.
12. Szentadrassy N, Banyasz T, Biro T, et al. Apico-basal inhomogeneity in distribution of ion channels in canine and human ventricular myocardium. Cardiovasc Res. 2005;65:851-860. (Pubitemid 40249729)
13. Verduyn SC, Vos MA, van der Zande J, et al. Role of interventricular dispersion of repolarization in acquired torsade-de-pointes arrhythmias: reversal by magnesium. Cardiovasc Res. 1997;34:453-463.
14. Verduyn SC, Vos MA, van der Zande J, et al. Further observations to elucidate the role of interventricular dispersion of repolarization and early after depolarizations in the genesis of acquired torsade de pointes arrhythmias: a comparison between almokalant and d-sotalol using the dog as its own control. J Am Coll Cardiol. 1997;30:1575-1584.
15. Volders PG, Sipido KR, Carmeliet E, et al. Repolarizing K+ currents ITO1 and IKs are larger in right than left canine ventricular midmyocardium. Circulation. 1999;99:206-210.
16. Volders PG, Sipido KR, Vos MA, et al. Downregulation of delayed rectifier K+ currents in dogs with chronic complete atrioventricular block and acquired torsades de pointes. Circulation. 1999;100:2455-2461.
17. James TN. Normal and abnormal consequences of apoptosis in the human heart. From postnatal morphogenesis to paroxysmal arrhythmias. Circulation. 1994;90:556-573.
18. Nerheim P, Krishnan SC, Olshansky B, et al. Apoptosis in the genesis of cardiac rhythm disorders. Cardiol Clin. 2001;19:155-163.
19. Mallat Z, Tedgui A, Fontaliran F, et al. Evidence of apoptosis in arrhythmogenic right ventricular dysplasia. N Engl J Med. 1996;335: 1190-1196. (Pubitemid 26339773)
20. Hamilton RM. Arrhythmogenic right ventricular cardiomyopathy. Pacing Clin Electrophysiol. 2009;32:S44-S51.
21. Pellman J, Lyon RC, Sheikh F. Extracellular matrix remodeling in atrial fibrosis: mechanisms and implications in atrial fibrillation. J Mol Cell Cardiol. 2010;48:461-467.
22. Rohr S. Myofibroblasts in diseased hearts: new players in cardiac arrhythmias? Heart Rhythm. 2009;6:848-856.
23. Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol. 2005;6:376-385.
24. Lee Y, Jeon K, Lee JT, et al. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 2002;21:4663-4670.
25. Hutvagner G, Simard MJ. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol. 2008;9:22-32.
26. Lewis BP, Shih IH, Jones-Rhoades MW, et al. Prediction of mammalian microRNA targets. Cell. 2003;115:787-798.
27. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120:15-20.
28. Luo X, Zhang H, Xiao J, et al. Regulation of human cardiac ion channel genes by microRNAs: theoretical perspective and pathophysiological implications. Cell Physiol Biochem. 2010;25:571-586.
29. Lagos-Quintana M, Rauhut R, Yalcin A, et al. Identification of tissue-specific miRNAs from mouse. Curr Biol. 2002;12:735-739.
30. Liang Y, Ridzon D, Wong L, et al. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics. 2007;8:166.
31. Yang B, Lu Y, Wang Z. Control of cardiac excitability by microRNAs. Cardiovasc Res. 2008;79:571-580.
32. Wang Z, Luo X, Lu Y, et al. miRNAs at the heart of the matter. J Mol Med. 2008;86:772-783.
33. Yang B, Lin H, Xiao J, et al. The muscle-specific microRNA miR-1 causes cardiac arrhythmias by targeting GJA1 and KCNJ2 genes. Nat Med. 2007; 13:486-491
34. Bostjancic E, Zidar N, Stajer D, et al. MicroRNA miR-1 is up-regulated in remote myocardium in patients with myocardial infarction. Folia Biol (Praha). 2010;56:27-31.
35. Tang Y, Zheng J, Sun Y, et al. MicroRNA-1 regulates cardiomyocyte apoptosis by targeting Bcl-2. Int Heart J. 2009;50:377-387.
36. Yin C, Wang X, Kukreja RC. Endogenous microRNAs induced by heat-shock reduce myocardial infarction following ischemia-reperfusion in mice. FEBS Lett. 2008;582:4137-4142.
37. Ai J, Zhang R, Li Y, et al. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun. 2010;391:73-77.
38. Wang GK, Zhu JQ, Zhang JT, et al. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J. 2010;31:659-666.
39. Xu C, Lu Y, Pan Z, 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: 3045-3052.
40. Shan H, Li X, Pan Z, 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.
41. Zhao Y, Ransom JF, Li A, et al. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell. 2007;129: 303-317.
42. Desai AD, Yaw TS, Yamazaki T, et al. Prognostic significance of quantitative QRS duration. Am J Med. 2006;119:600-606.
43. Costantini DL, Arruda EP, Agarwal P, et al. The homeodomain transcription factor Irx5 establishes the mouse cardiac ventricular repolarization gradient. Cell. 2005;123:347-358.
44. Sanguinetti MC, Curran ME, Zou A, et al. Coassembly of KVLQT1 and minK (IsK) proteins to form cardiac IKs potassium channel. Nature. 1996; 384:80-83.
45. Roden DM, Yang T. Protecting the heart against arrhythmias: potassium current physiology and repolarization reserve. Circulation. 2005;112: 1376-1378.
46. Roden DM. Long QT syndrome: reduced repolarization reserve and the genetic link. J Intern Med. 2006;259:59-69.
47. Sanguinetti MC, Jiang C, Curran ME, et al. A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell. 1995;81:299-307.
48. Sanguinetti MC, Tristani-Firouzi M. HERG potassium channels and cardiac arrhythmia. Nature. 2006;440:463-469.
49. Luo X, Lin H, Lu Y, et al. Transcriptional activation by stimulating protein 1 and post-transcriptional repression by muscle-specific microRNAs of IKs-encoding genes and potential implications in regional heterogeneity of their expressions. J Cell Physiol. 2007;212:358-367.
50. Xiao J, Luo X, Lin H, et al. MicroRNA miR-133 represses HERG K+ channel expression contributing to QT prolongation in diabetic hearts. J Biol Chem. 2007;282:12363-12367.
51. Xiao L, Xiao J, Luo X, et al. Feedback remodeling of cardiac potassium current expression: a novel potential mechanism for control of repolarization reserve. Circulation. 2008;118:983-992.
52. Guo W, Xu H, London B, et al. Molecular basis of transient outward K+ current diversity in mouse ventricular myocytes. J Physiol. 1999;521:587-599.
53. Guo W, Li H, London B, et al. Functional consequences of elimination of ito, f and ito, s: early afterdepolarizations, atrioventricular block, and ventricular arrhythmias in mice lacking Kv1.4 and expressing a dominant-negative Kv4 alpha subunit. Circ Res. 2000;87:73-79.
54. Zhou J, Kodirov S, Murata M, et al. Regional upregulation of Kv2.1-encoded current, IK, slow2, in Kv1DN mice is abolished by crossbreeding with Kv2DN mice. Am J Physiol Heart Circ Physiol. 2003;284: H491-H500.
55. Zhang Y, Xiao J, Wang H, et al. Restoring depressed HERG K+ channel function as a mechanism for insulin treatment of the abnormal QT prolongation and the associated arrhythmias in diabetic rabbits. Am J Physiol. 2006;291:1446-1455.
56. Matkovich SJ, Wang W, Tu Y, et al. MicroRNA-133a protects against myocardial fibrosis and modulates electrical repolarization without affecting hypertrophy in pressure-overloaded adult hearts. Circ Res. 2010;106:166-175.
57. Babij P, Askew GR, Nieuwenhuijsen B, et al. Inhibition of cardiac delayed rectifier K+ current by overexpression of the long-QT syndrome HERG G628S mutation in transgenic mice. Circ Res. 1998;83:668-678.
58. Dhamoon AS, Jalife J. The inward rectifier current (IK1) controls cardiac excitability and is involved in arrhythmogenesis. Heart Rhythm. 2005;2: 316-324.
59. Li J, McLerie M, Lopatin AN. Transgenic upregulation of IK1 in the mouse heart leads to multiple abnormalities of cardiac excitability. Am J Physiol Heart Circ Physiol. 2004;287:H2790-H2802.
60. Girmatsion Z, Biliczki P, Bonauer A, et al. Changes in microRNA-1 expression and IK1 up-regulation in human atrial fibrillation. Heart Rhythm. 2009;6:1802-1809.
61. Fernandez-Velasco M, Goren N, et al. Regional distribution of hyperpolarization-activated current If and hyperpolarization-activated cyclic nucleotide-gated channel mRNA expression in ventricular cells from control and hypertrophied rat hearts. J Physiol. 2003;553:395-405.
62. Stilli D, Sgoifo A, Macchi E, et al. Myocardial remodeling and arrhythmogenesis in moderate cardiac hypertrophy in rats. Am J Physiol Heart Circ Physiol. 2001;280:H142-H150.
63. Yasui K, Liu W, Opthof T, et al. If current and spontaneous activity in mouse embryonic ventricular myocytes. Circ Res. 2001;88:536-542.
64. Robinson RB, Yu H, Chang F, et al. Developmental change in the voltage-dependence of the pacemaker current, if, in rat ventricle cells. Pflugers Arch. 1997;433:533-535.
65. Cerbai E, Sartiani L, DePaoli P, et al. The properties of the pacemaker current if in human ventricular myocytes are modulated by cardiac disease. J Mol Cell Cardiol. 2001;3:441-448.
66. Hoppe UC, Jansen E, Sudkamp M, et al. Hyperpolarization activated inward current in ventricular myocytes from normal and failing human hearts. Circulation. 1998;97:55-65.
67. Cerbai E, Pino R, Porciatti F, et al. Characterization of the hyperpolar-ization-activated current, if, in ventricular myocytes from human failing heart. Circulation. 1997;95:568-571.
68. Luo X, Lin H, Xiao J, et al. Downregulation of miRNA-1/miRNA-133 contributes to re-expression of pacemaker channel genes HCN2 and HCN4 in hypertrophic heart. J Biol Chem. 2008;283:20045-20052.
69. Lu Y, Xiao J, Lin H, et al. A single anti-microRNA antisense oligodeoxyribonucleotide (AMO) targeting multiple microRNAs offers an improved approach for microRNA interference. Nucleic Acids Res. 2009;37:e24.
70. Terentyev D, Belevych AE, Terentyeva R, et al. miR-1 overexpression enhances Ca2+ release and promotes cardiac arrhythmogenesis by targeting PP2A regulatory subunit B56alpha and causing CaMKII-dependent hyperphosphorylation of RyR2. Circ Res. 2009;104:514-521.
71. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415: 198-205.
72. Wehrens XH, Marks AR. Novel therapeutic approaches for heart failure by normalizing calcium cycling. Nat Rev Drug Discov. 2004;3:565-573.
73. Maier LS, Bers DM. Role of Ca2+/calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc Res. 2007;73:631-640.
74. Grueter CE, Colbran RJ, Anderson ME. CaMKII, an emerging molecular driver for calcium homeostasis, arrhythmias, and cardiac dysfunction. J Mol Med. 2007;85:5-14.
75. Davare MA, Horne MC, Hell JW. Protein phosphatase 2A is associated with class C L-type calcium channels (Cav1.2) and antagonizes channel phosphorylation by cAMP-dependent protein kinase. J Biol Chem. 2000; 275:39710-39717.
76. Marx SO, Reiken S, Hisamatsu Y, et al. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell. 2000;101:365-376.
77. Steenaart NAE, Ganim JR, DiSalvo J, et al. The phospholamban phosphatase associated with cardiac sarcoplasmic reticulum is a type 1 enzyme. Arch Biochem Biophys. 1992;293:17-24.
78. Hall DD, Feekes JA, Arachchige Don AS, et al. Binding of protein phosphatase 2A to the L-type calcium channel Cav1.2 next to Ser1928, its main PKA site, is critical for Ser1928 dephosphorylation. Biochemistry. 2006;45:3448-3459.
79. Liu DW, Antzelevitch C. Characteristics of the delayed rectifier current (IKr and IKs) in canine ventricular epicardial, midmyocardial, and endocardial myocytes. A weaker IKs contributes to the longer action potential of the M cell. Circ Res. 1995;76:351-365.
80. Szabo G, Szentandrassy N, Biro T, et al. Asymmetrical distribution of ion channels in canine and human leftventricular wall: epicardium versus midmyocardium. Pflugers Arch. 2005;450:307-316.
81. Ramakers C, Vos MA, Doevendans PA, et al. Coordinated down-regulation of KCNQ1 and KCNE1 expression contributes to reduction of IKs in canine hypertrophied hearts. Cardiovasc Res. 2003;57:486-496.
82. Ramakers C, Stengl M, Spatjens RL, et al. Molecular and electrical characterization of the canine cardiac ventricular septum. J Mol Cell Cardiol. 2005;38:153-161.
83. Tsuji Y, Opthof T, Yasui K, et al. Ionic mechanisms of acquired QT prolongation and torsades de pointes in rabbits with chronic complete atrioventricular block. Circulation. 2002;106:2012-2018.
84. Tsuji Y, Zicha S, Qi XY, et al. Potassium channel subunit remodeling in rabbits exposed to long-term bradycardia or tachycardia: discrete arrhythmogenic consequences related to differential delayed-rectifier changes. Circulation. 2006;113:345-355.
85. Yang B, Lu Y, Wang Z. MicroRNAs and apoptosis: implications for molecular therapy of human disease. Clin Exp Pharmacol Physiol. 2009; 36:951-960.
86. Wang Z. microRNAs: a matter of life or death. World J Biol Chem. 2010; 1:41-54.
87. Ye Y, Hu Z, Lin Y, et al. Down-regulation of microRNA-29 by antisense inhibitors and a PPAR-{gamma} agonist protects against myocardial ischemia-reperfusion injury. Cardiovasc Res. 2010;87:535-544.
88. Ren XP, Wu J, Wang X, et al. MicroRNA-320 is involved in the regulation of cardiac ischemia/reperfusion injury by targeting heat-shock protein 20. Circulation. 2009;119:2357-2366.
89. Yin C, Salloum FN, Kukreja RC. A novel role of microRNA in late preconditioning: upregulation of endothelial nitric oxide synthase and heat shock protein 70. Circ Res. 2009;104:572-575.
90. Rane S, He M, Sayed D, 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.
91. van Rooij E, Sutherland LB, Qi X, et al. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007;316: 575-579.
92. Thum T, Gross C, Fiedler J, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature. 2008; 456:980-984.
93. Roy S, Khanna S, Hussain SR, et al. MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res. 2009;82:21-29.
94. van Rooij E, Sutherland LB, Thatcher JE, et al. Dysregulation of microRNAs following myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA. 2008;105:13027-13032.
95. Duisters RF, Tijsen AJ, Schroen B, et al. mir-133 and mir-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ Res. 2009;104:170-178.
96. Liu N, Bezprozvannaya S, Williams AH, et al. microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev. 2008;22:3242-3254.