Role of microRNAs in cardiovascular disease: Therapeutic challenges and potentials

Journal of Cardiovascular Pharmacology

Volumn 56, Issue 5, 2010, Pages 444-453

  Port, J David ^a   Sucharov, Carmen ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

gene regulation; heart failure; hypertrophy; microRNA

Indexed keywords

ANGIOTENSIN 2 RECEPTOR; CONNEXIN 43; CYCLIC NUCLEOTIDE GATED CHANNEL; GELATINASE A; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; LET 7; MICRORNA; MICRORNA 1; MICRORNA 133A 1; MICRORNA 133A 2; MICRORNA 133B; MICRORNA 150; MICRORNA 195; MICRORNA 199; MICRORNA 19A; MICRORNA 19B; MICRORNA 208A; MICRORNA 208B; MICRORNA 21; MICRORNA 221; MICRORNA 23A; MICRORNA 23B; MICRORNA 29A; MICRORNA 29B; MICRORNA 30; MICRORNA 320; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; RNA POLYMERASE II; UNCLASSIFIED DRUG; UNINDEXED DRUG;

APOPTOSIS; CARDIOMYOPATHY; DNA MICROARRAY; DOWN REGULATION; FIBROBLAST; GENE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; GENE THERAPY; HEART ARRHYTHMIA; HEART EJECTION FRACTION; HEART FAILURE; HEART HYPERTROPHY; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION SYSTEM; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN POLYMORPHISM; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RNA ANALYSIS; RNA SEQUENCE; RNA SYNTHESIS; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; CARDIOVASCULAR DISEASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEART FAILURE; HUMANS; MICRORNAS; SIGNAL TRANSDUCTION;

EID: 78650179779     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3181f605b6     Document Type: Review

References (101)

1. Ambros V. microRNAs: tiny regulators with great potential. Cell. 2001; 107:823-826.
2. Friedman RC, Farh KK, Burge CB, et al. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19:92-105.
3. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 2008;9:102-114.
4. Filipowicz W, Jaskiewicz L, Kolb FA, et al. Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol. 2005;15: 331-341.
5. Baek D, Villen J, Shin C, et al. The impact of microRNAs on protein output. Nature. 2008;455:64-71.
6. Grosshans H, Filipowicz W. Proteomics joins the search for microRNA targets. Cell. 2008;134:560-562.
7. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843-854.
8. Griffiths-Jones S, Grocock RJ, van Dongen S, et al. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 2006;34:D140-D144.
9. Small EM, Frost RJ, Olson EN. MicroRNAs add a new dimension to cardiovascular disease. Circulation. 2010;121:1022-1032.
10. Huang JC, Babak T, Corson TW, et al. Using expression profiling data to identify human microRNA targets. Nat Methods. 2007;4:1045-1049.
11. Nam S, Li M, Choi K, et al. MicroRNA and mRNA integrated analysis (MMIA): a web tool for examining biological functions of microRNA expression. Nucleic Acids Res. 2009;37:W356-W362.
12. Chi SW, Zang JB, Mele A, et al. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature. 2009;460:479-486.
13. Hafner M, Landthaler M, Burger L, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell. 2010;141:129-141.
14. Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004;23:4051-4060.
15. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol. 2006;13:1097-1101.
16. Van Rooij E, Quiat D, Johnson BA, et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell. 2009;17:662-673.
17. 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.
18. Monteys AM, Spengler RM, Wan J, et al. Structure and activity of putative intronic miRNA promoters. RNA. 2010;16:495-505.
19. He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature. 2005;435:828-833.
20. Liu N, Williams AH, Kim Y, et al. An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc Natl Acad Sci USA. 2007;104:20844-20849.
21. Parker R, Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell. 2007;25:635-646.
22. Yi R, Qin Y, Macara IG, et al. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003;17: 3011-3016.
23. Lian SL, Li S, Abadal GX, et al. The C-terminal half of human Ago2 binds to multiple GW-rich regions of GW182 and requires GW182 to mediate silencing. RNA. 2009;15:804-813.
24. Eystathioy T, Jakymiw A, Chan EK, et al. The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA. 2003;9:1171-1173.
25. Trabucchi M, Briata P, Filipowicz W, et al. How to control miRNA maturation? RNA Biol. 2009;6:536-540.
26. Trabucchi M, Briata P, Garcia-Mayoral M, et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature. 2009;459:1010-1014.
27. Slezak-Prochazka I, Durmus S, Kroesen BJ, et al. MicroRNAs, macro-control: regulation of miRNA processing. RNA. 2010;16:1087-1095.
28. Newman MA, Thomson JM, Hammond SM. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA. 2008;14:1539-1549.
29. Gherzi R, Lee KY, Briata P, et al. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell. 2004;14:571-583.
30. Min H, Turck CW, Nikolic JM, et al. A new regulatory protein, KSRP, mediates exon inclusion through an intronic splicing enhancer. Genes Dev. 1997;11:1023-1036.
31. Briata P, Forcales SV, Ponassi M, et al. p38-dependent phosphorylation of the mRNA decay-promoting factor KSRP controls the stability of select myogenic transcripts. Mol Cell. 2005;20:891-903.
32. Bhattacharyya SN, Habermacher R, Martine U, et al. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell. 2006;125:1111-1124.
33. Kim HH, Kuwano Y, Srikantan S, et al. HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 2009;23:1743-1748.
34. Pradervand S, Weber J, Thomas J, et al. Impact of normalization on miRNA microarray expression profiling. RNA. 2009;15:493-501.
35. Bargaje R, Hariharan M, Scaria V, et al. Consensus miRNA expression profiles derived from interplatform normalization of microarray data. RNA. 2010;16:16-25.
36. Git A, Dvinge H, Salmon-Divon M, et al. Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression. RNA. 2010;16:991-1006.
37. Hafner M, Landgraf P, Ludwig J, et al. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods. 2008;44:3-12.
38. Friedlander MR, Chen W, Adamidi C, et al. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol. 2008;26: 407-415.
39. Clop A. Insights into the importance of miRNA-related polymorphisms to heart disease. Hum Mutat. 2009;30:v.
40. Zhou B, Rao L, Peng Y, et al. Common genetic polymorphisms in pre-microRNAs were associated with increased risk of dilated cardiomy-opathy. Clin Chim Acta. 2010;411:1287-1290.
41. Ryan BM, Robles AI, Harris CC. Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer. 2010;10: 389-402.
42. Chen K, Song F, Calin GA, et al. Polymorphisms in microRNA targets: a gold mine for molecular epidemiology. Carcinogenesis. 2008;29: 1306-1311.
43. Martin MM, Buckenberger JA, Jiang J, et al. The human angiotensin II type 1 receptor +1166 A/C polymorphism attenuates microrna-155 binding. J Biol Chem. 2007;282:24262-24269.
44. Martin MM, Lee EJ, Buckenberger JA, et al. MicroRNA-155 regulates human angiotensin II type 1 receptor expression in fibroblasts. J Biol Chem. 2006;281:18277-18284.
45. Rao PK, Toyama Y, Chiang HR, et al. Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ Res. 2009;105:585-594.
46. van Rooij E, Sutherland LB, Liu N, et al. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci USA. 2006;103:18255-18260.
47. Sucharov C, Bristow MR, Port JD. miRNA expression in the failing human heart: functional correlates. J Mol Cell Cardiol. 2008;45: 185-192.
48. Ikeda S, Kong SW, Lu J, et al. Altered microRNA expression in human heart disease. Physiol Genomics. 2007;31:367-373.
49. Naga Prasad SV, Duan ZH, Gupta MK, et al. Unique microRNA profile in end-stage heart failure indicates alterations in specific cardiovascular signaling networks. J Biol Chem. 2009;284:27487-27499.
50. Matkovich SJ, Van Booven DJ, Youker KA, et al. Reciprocal regulation of myocardial microRNAs and messenger RNA in human cardiomy-opathy and reversal of the microRNA signature by biomechanical support. Circulation. 2009;119:1263-1271.
51. Thum T, Galuppo P, Wolf C, et al. MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation. 2007;116: 258-267.
52. Condorelli G, Latronico MV, Dorn GW II. microRNAs in heart disease: putative novel therapeutic targets? Eur Heart J. 2010;31:649-658.
53. Bauersachs J, Thum T. MicroRNAs in the broken heart. Eur J Clin Invest. 2007;37:829-833.
54. Tatsuguchi M, Seok HY, Callis TE, et al. Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy. J Mol Cell Cardiol. 2007;42:1137-1141.
55. Sayed D, He M, Hong C, 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.
56. Roy S, Khanna S, Hussain SR, et al. MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metal-loprotease-2 via phosphatase and tensin homologue. Cardiovasc Res. 2009;82:21-29.
57. 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.
58. Dong S, Cheng Y, Yang J, et al. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem. 2009;284:29514-29525.
59. Sayed D, Rane S, Lypowy J, et al. MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol Biol Cell. 2008;19:3272-3282.
60. 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.
61. Cheng Y, Zhang C. MicroRNA-21 in cardiovascular disease. J Cardiovasc Transl Res. 2010;3:251-255.
62. 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;CIRCRESAHA.108.193250:572-575.
63. 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.
64. Yang B, Lin H, Xiao J, et al. The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2.[see comment]. Nat Med. 2007;13:486-491.
65. Luo X, Lin H, Pan Z, et al. Down-regulation of miR-1/miR-133 contributes to re-expression of pacemaker channel genes HCN2 and HCN4 in hypertrophic heart. J Biol Chem. 2008;283:20045-20052.
66. Terentyev D, Belevych AE, Terentyeva R, et al. miR-1 overexpression enhances Ca(2+) release and promotes cardiac arrhythmogenesis by targeting PP2A regulatory subunit B56alpha and causing CaMKII-dependent hyperphosphorylation of RyR2. Circ Res. 2009;104: 514-521.
67. Ikeda S, He A, Kong SW, et al. MicroRNA-1 negatively regulates expression of the hypertrophy-associated calmodulin and Mef2a genes. Mol Cell Biol. 2009;29:2193-2204.
68. 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(pt 17): 3045-3052.
69. Elia L, Contu R, Quintavalle M, et al. Reciprocal regulation of microRNA-1 and insulin-like growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions. Circulation. 2009;120:2377-2385.
70. Care A, Catalucci D, Felicetti F, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med. 2007;13:613-618.
71. Tang Y, Zheng J, Sun Y, et al. MicroRNA-1 regulates cardiomyocyte apoptosis by targeting Bcl-2. Int Heart J. 2009;50:377-387.
72. Beuvink I, Kolb FA, Budach W, et al. A novel microarray approach reveals new tissue-specific signatures of known and predicted mammalian microRNAs. Nucleic Acids Res. 2007;35:e52.
73. Dong DL, Chen C, Huo R, et al. Reciprocal repression between microRNA-133 and calcineurin regulates cardiac hypertrophy: a novel mechanism for progressive cardiac hypertrophy. Hypertension. 2010;55: 946-952.
74. 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.
75. Schipper ME, van Kuik J, de Jonge N, et al. Changes in regulatory microRNA expression in myocardium of heart failure patients on left ventricular assist device support. J Heart Lung Transplant. 2008;27: 1282-1285.
76. Bostjancic E, Zidar N, Stajer D, et al. MicroRNAs miR-1, miR-133a, miR-133b and miR-208 are dysregulated in human myocardial infarction. Cardiology. 2010;115:163-169.
77. 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.
78. 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.
79. 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.
80. Chen JF, Mandel EM, Thomson JM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006;38:228-233.
81. Callis TE, Pandya K, Seok HY, et al. MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest. 2009;119: 2772-2786.
82. Sluijter JP, van Mil A, van Vliet P, et al. MicroRNA-1 and-499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells. Arterioscler Thromb Vasc Biol. 2010;30:859-868.
83. Lin Z, Murtaza I, Wang K, et al. miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc Natl Acad Sci USA. 2009;106:12103-12108.
84. 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.
85. Adams V, Mobius-Winkler S, Schuler G. Basic and translational research: from molecule, to mouse, to man. Eur J Cardiovasc Prev Rehabil. 2009;16(Suppl 2):S48-S52.
86. Song XW, Li Q, Lin L, et al. MicroRNAs are dynamically regulated in hypertrophic hearts, and miR-199a is essential for the maintenance of cell size in cardiomyocytes. J Cell Physiol. 2010;225:437-443.
87. Rane S, He M, Sayed D, et al. Downregulation of MiR-199a derepresses hypoxia-inducible factor-1{alpha} andsirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res. 2009;CIRCRESAHA. 108.193102:879-886.
88. Rane S, He M, Sayed D, et al. An antagonism between the AKT and beta-adrenergic signaling pathways mediated through their reciprocal effects on miR-199a-5p. Cell Signal. 2010;22:1054-1062.
89. van Rooij E, Olson EN. MicroRNAs: powerful new regulators of heart disease and provocative therapeutic targets. J Clin Invest. 2007;117: 2369-2376.
90. van Rooij E, Marshall WS, Olson EN. Toward microRNA-based therapeutics for heart disease: the sense in antisense. Circ Res. 2008;103: 919-928.
91. Dorn GW II. Therapeutic potential of microRNAs in heart failure. Curr Cardiol Rep. 2010;12:209-215.
92. Fasanaro P, Greco S, Ivan M, et al. microRNA: emerging therapeutic targets in acute ischemic diseases. Pharmacol Ther. 2010;125: 92-104.
93. Soifer HS, Rossi JJ, Saetrom P. MicroRNAs in disease and potential therapeutic applications. Mol Ther. 2007;15:2070-2079.
94. Sibley CR, Seow Y, Wood MJ. Novel RNA-based strategies for therapeutic gene silencing. Mol Ther. 2010;18:466-476.
95. Krutzfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438:685-689.
96. Esau CC Inhibition of microRNA with antisense oligonucleotides. Methods. 2008;44:55-60.
97. Esau CC, Monia BP Therapeutic potential for microRNAs. Adv Drug Deliv Rev. 2007;59:101-114.
98. Davis S, Propp S, Freier SM, et al. Potent inhibition of microRNA in vivo without degradation. Nucleic Acids Res. 2009;37:70-77.
99. Lennox KA, Behlke MA. A direct comparison of anti-microRNA oligonucleotide potency. Pharm Res. 2010;27:1788-1799.
100. Voellenkle C, van Rooij J, Cappuzzello C, et al. microRNA signatures in peripheral blood mononuclear cells of chronic heart failure patients. Physiol Genomics. 2010;42:420-426.
101. Satoh M, Minami Y, Takahashi Y, et al. Expression of microRNA-208 is associated with adverse clinical outcomes in human dilated cardiomyopathy. J Card Fail. 2010;16:404-410.