MicroRNAs in myocardial infarction

Nature Reviews Cardiology

Volumn 12, Issue 3, 2015, Pages 135-142

  Boon, Reinier A ^a   Dimmeler, Stefanie ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 126; MICRORNA 132; MICRORNA 210; MICRORNA 24;

ACUTE HEART INFARCTION; ANGIOGENESIS; BONE MARROW CELL; CELL COMMUNICATION; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; MESENCHYMAL STROMA CELL; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; RNA DEGRADATION; GENETICS; MYOCARDIAL INFARCTION; PATHOLOGY; PHYSIOLOGY; PROCEDURES; STEM CELL TRANSPLANTATION;

CELL COMMUNICATION; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; MICRORNAS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELL TRANSPLANTATION;

EID: 84923585184     PISSN: 17595002     EISSN: 17595010     Source Type: Journal    
DOI: 10.1038/nrcardio.2014.207     Document Type: Review

References (93)

1. Lee, R. C. &Ambros, V. An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862-864 (2001).
2. Lagos-Quintana, M. et al. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739 (2002).
3. Members, W. G. et al. Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125, e2-e220 (2012).
4. Thum, T. Noncoding RNAs and myocardial fibrosis. Nat. Rev. Cardiol. 11, 655-663 (2014).
5. Hullinger, T. G. et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circ. Res. 110, 71-81 (2012).
6. Nishi, H. et al. MicroRNA-15b modulates cellular ATP levels and degenerates mitochondria via Arl2 in neonatal rat cardiac myocytes. J. Biol. Chem. 285, 4920-4930 (2010).
7. Zhu, H. et al. MicroRNA-195 promotes palmitate-induced apoptosis in cardiomyocytes by down-regulating Sirt1. Cardiovasc. Res. 92, 75-84 (2011).
8. Hermeking, H. The miR-34 family in cancer and apoptosis. Cell Death Differ. 17, 193-199 (2010).
9. Boon, R. A. et al. MicroRNA-34a regulates cardiac ageing and function. Nature 495, 107-110 (2013).
10. Bernardo, B. C. et al. Therapeutic inhibition of the miR-34 family attenuates pathological cardiac remodeling and improves heart function. Proc. Natl Acad. Sci. USA 109, 17615-17620 (2012).
11. Bernardo, B. C. et al. Silencing of miR-34a attenuates cardiac dysfunction in a setting of moderate, but not severe, hypertrophic cardiomyopathy. PLoS ONE 9, e90337 (2014).
12. Yamakuchi, M., Ferlito, M. &Lowenstein, C. J. miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl Acad. Sci. USA 105, 13421-13426 (2008).
13. Ren, X.-P. et al. MicroRNA-320 is involved in the regulation of cardiac ischemia/reperfusion injury by targeting heat-shock protein 20 Circulation 119, 2357-2366 (2009).
14. Li, J. et al. Mitofusin 1 is negatively regulated by microRNA 140 in cardiomyocyte apoptosis. Mol. Cell. Biol. 34, 1788-1799 (2014).
15. Shan, Z.-X. et al. miR-1/miR-206 regulate Hsp60 expression contributing to glucose-mediated apoptosis in cardiomyocytes. FEBS Lett. 584, 3592-3600 (2010).
16. Zhang, B. et al. MicroRNA-92a inhibition attenuates hypoxia/reoxygenation-induced myocardiocyte apoptosis by targeting Smad7. PLoS ONE 9, e100298 (2014).
17. Hinkel, R. et al. Inhibition of microRNA-92a protects against ischemia/reperfusion injury in a large-animal model. Circulation 128, 1066-1075 (2013).
18. Huang, X. et al. Expression of microRNA-122 contributes to apoptosis in H9C2 myocytes. J. Cell. Mol. Med. 16, 2637-2646 (2012).
19. Li, X. et al. MicroRNA-150 aggravates H2O2-induced cardiac myocyte injury by down-regulating c-myb gene. Acta Biochim. Biophys. Sin. 45, 734-741 (2013).
20. Wang, L. et al. Effects of downregulation of microRNA-181a on H2O2-induced H9c2 cell apoptosis via the mitochondrial apoptotic pathway. Oxid. Med. Cell. Longev. 2014, 960362 (2014).
21. Pan, Z. et al. M3 subtype of muscarinic acetylcholine receptor promotes cardioprotection via the suppression of miR-376b-5p. PLoS ONE 7, e32571 (2012).
22. Li, R.-C. et al. In vivo suppression of microRNA-24 prevents the transition toward decompensated hypertrophy in aortic-constricted mice. Circ. Res. 112, 601-605 (2013).
23. Qian, L. et al. miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J. Exp. Med. 208, 549-560 (2011).
24. van Rooij, E. et al. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc. Natl Acad. Sci. USA 103, 18255-18260 (2006).
25. Li, D. F. et al. Induction of microRNA-24 by HIF-1 protects against ischemic injury in rat cardiomyocytes. Physiol. Res. 61, 555-565 (2012).
26. Meloni, M. et al. Local inhibition of microRNA-24 improves reparative angiogenesis and left ventricle remodeling and function in mice with myocardial infarction. Mol. Ther. 21, 1390-1402 (2013).
27. Fiedler, J. et al. MicroRNA-24 regulates vascularity after myocardial infarction. Circulation 124, 720-730 (2011).
28. Aurora, A. B. et al. MicroRNA-214 protects the mouse heart from ischemic injury by controlling Ca2+ overload and cell death. J. Clin. Invest. 122, 1222-1232 (2012).
29. Lv, G. et al. MicroRNA-214 protects cardiac myocytes against H2O2-induced injury. J. Cell. Biochem. 115, 93-101 (2014).
30. Li, B. et al. MicroRNA-7a/b protects against cardiac myocyte injury in ischemia/reperfusion by targeting poly(ADP-ribose) polymerase. PLoS ONE 9, e90096 (2014).
31. Frank, D. et al. MicroRNA-20a inhibits stress-induced cardiomyocyte apoptosis involving its novel target Egln3/PHD3. J. Mol. Cell. Cardiol. 52, 711-717 (2012).
32. He, S. et al. miR-138 protects cardiomyocytes from hypoxia-induced apoptosis via MLK3/JNK/c-jun pathway. Biochem. Biophys. Res. Comm. 441, 763-769 (2013).
33. Zhang, X. et al. Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death. J. Mol. Cell. Cardiol. 49, 841-850 (2010).
34. Hu, S. et al. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 122 (Suppl.), S124-S131 (2010).
35. Wang, J. et al. miR-499 protects cardiomyocytes from H2O2-induced apoptosis via its effects on Pdcd4 and Pacs2. RNA Biol. 11, 339-350 (2014).
36. Wang, K. et al. miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death Dis. 4, e709 (2013).
37. Porrello, E. R. &Olson, E. N. A neonatal blueprint for cardiac regeneration. Stem Cell Res. 13, 556-570 (2014).
38. Steinhauser, M. L. &Lee, R. T. Regeneration of the heart. EMBO Mol. Med. 3, 701-712 (2011).
39. Porrello, E. R. et al. Transient regenerative potential of the neonatal mouse heart. Science 331, 1078-1080 (2011).
40. Porrello, E. R. et al. miR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ. Res. 109, 670-679 (2011).
41. Porrello, E. R. et al. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl Acad. Sci. USA 110, 187-192 (2013).
42. Eulalio, A. et al. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 492, 376-381 (2012).
43. Liu, N. et al. MicroRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev. 22, 3242-3254 (2008).
44. Yin, V. P., Lepilina, A., Smith, A. &Poss, K. D. Regulation of zebrafish heart regeneration by miR-133. Dev. Biol. 365, 319-327 (2012).
45. Chen, J. et al. miR-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ. Res. 112, 1557-1566 (2013).
46. Danielson, L. S. et al. Cardiovascular dysregulation of miR-17-92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis. FASEB J. 27, 1460-1467 (2013).
47. Bonauer, A. et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 324, 1710-1713 (2009).
48. Iaconetti, C. et al. Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury. Basic Res. Cardiol. 107, 1-14 (2012).
49. Urbich, C., Walter, D. H., Zeiher, A. M. &Dimmeler, S. Laminar shear stress upregulates integrin expression: role in endothelial cell adhesion and apoptosis. Circ. Res. 87, 683-689 (2000).
50. Wu, W. et al. Flow-dependent regulation of Krüppel-like factor 2 is mediated by microRNA-92a. Circulation 124, 633-641 (2011).
51. Doebele, C. et al. Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells. Blood 115, 4944-4950 (2010).
52. Pin, A.-L. et al. miR-20a represses endothelial cell migration by targeting MKK3 and inhibiting p38 MAP kinase activation in response to VEGF. Angiogenesis 15, 593-608 (2012).
53. Suarez, Y. et al. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc. Natl Acad. Sci. USA 105, 14082-14087 (2008).
54. Semo, J. et al. The 106b~25 microRNA cluster is essential for neovascularization after hindlimb ischaemia in mice. Eur. Heart J. http://dx.doi.org/ 10.1093/eurheartj/eht041.
55. Icli, B. et al. MicroRNA-26a regulates pathological and physiological angiogenesis by targeting BMP/SMAD1 signaling. Circ. Res. 113, 1231-1241 (2013).
56. Yin, K.-J. et al. Vascular endothelial cell-specific microRNA-15a inhibits angiogenesis in hindlimb ischemia. J. Biol. Chem. 287, 27055-27064 (2012).
57. Spinetti, G. et al. MicroRNA-15a and microRNA-16 impair human circulating proangiogenic cell functions and are increased in the proangiogenic cells and serum of patients with critical limb ischemia. Circ. Res. 112, 335-346 (2013).
58. Fasanaro, P. et al. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand ephrin-A3. J. Biol. Chem. 283, 15878-15883 (2008).
59. Matsa, E., Sallam, K. &Wu, J. C. Cardiac stem cell biology: glimpse of the past, present, and future. Circ. Res. 114, 21-27 (2014).
60. Dimmeler, S., Ding, S., Rando, T. A. &Trounson, A. Translational strategies and challenges in regenerative medicine. Nat. Med. 20, 814-821 (2014).
61. Jakob, P. et al. Loss of angiomiR-126 and 130a in angiogenic early outgrowth cells from patients with chronic heart failure: role for impaired in vivo neovascularization and cardiac repair capacity. Circulation 126, 2962-2975 (2012).
62. Jansen, F. et al. Endothelial microparticle-mediated transfer of microRNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucose-damaged endothelial microparticles. Circulation 128, 2026-2038 (2013).
63. Chen, J. J. &Zhou, S. H. Mesenchymal stem cells overexpressing miR-126 enhance ischemic angiogenesis via the AKT/ERK-related pathway. Cardiol. J. 18, 675-681 (2011).
64. Huang, F. et al. Mesenchymal stem cells modified with miR-126 release angiogenic factors and activate Notch ligand Delta-like-4, enhancing ischemic angiogenesis and cell survival. Int. J. Mol. Med. 31, 484-492 (2013).
65. Liu, J. et al. MicroRNA-155 prevents necrotic cell death in human cardiomyocyte progenitor cells via targeting RIP1. J. Cell. Mol. Med. 15, 1474-1482 (2011).
66. Xu, Q. et al. MicroRNA-34a contributes to the impaired function of bone marrow-derived mononuclear cells from patients with cardiovascular disease. J. Am. Coll. Cardiol. 59, 2107-2117 (2012).
67. Hu, S. et al. Novel MicroRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation. Circulation 124 (Suppl.), S27-S34 (2011).
68. Heinrich, E.-M. &Dimmeler, S. MicroRNAs and stem cells: control of pluripotency, reprogramming, and lineage commitment. Circ. Res. 110, 1014-1022 (2012).
69. Jayawardena, T. M. et al. MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ. Res. 110, 1465-1473 (2012).
70. Nam, Y.-J. et al. Reprogramming of human fibroblasts toward a cardiac fate. Proc. Natl Acad. Sci. USA 110, 5588-5593 (2013).
71. Jayawardena, T. M. et al. MicroRNA induced cardiac reprogramming in vivo: evidence for mature cardiac myocaytes and improved cardiac function. Circ. Res. http://dx.doi.org/10.1161/CIRCRESAHA.116.304510.
72. Qian, L. et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485, 593-598 (2012).
73. Boon, R. A. &Vickers, K. C. Intercellular transport of microRNAs. Arterioscler. Thromb. Vasc. Biol. 33, 186-192 (2013).
74. Hosoda, T. et al. Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation 123, 1287-1296 (2011).
75. Hergenreider, E. et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol. 14, 249-256 (2012).
76. Zhou, J. et al. Regulation of vascular smooth muscle cell turnover by endothelial cell-secreted microRNA-126: role of shear stress. Circ. Res. 113, 40-51 (2013).
77. Losordo, D. W. et al. Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circ. Res. 109, 428-436 (2011).
78. Mocharla, P. et al. AngiomiR-126 expression and secretion from circulating CD34+ and CD14+ PBMCs: role for proangiogenic effects and alterations in type 2 diabetics. Blood 121, 226-236 (2013).
79. Barile, L. et al. Extracellular vesicles from human cardiac progenitor cells inhibit cardiomyocyte apoptosis and improve cardiac function after myocardial infarction. Cardiovasc. Res. 103, 530-541 (2014).
80. Ong, S.-G. et al. Cross talk of combined gene and cell therapy in ischemic heart disease: role of exosomal microRNA transfer. Circulation 130 (Suppl. 1), S60-S69 (2014).
81. Katare, R. et al. Transplantation of human pericyte progenitor cells improves the repair of infarcted heart through activation of an angiogenic program involving microRNA-132. Circ. Res. 109, 894-906 (2011).
82. Ibrahim, A. G.-E., Cheng, K. &Marbán, E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports 2, 606-619 (2014).
83. Cheng, H. S. et al. MicroRNA-146 represses endothelial activation by inhibiting pro-inflammatory pathways. EMBO Mol. Med. 5, 949-966 (2013).
84. Chen, L. et al. Cardiac progenitor-derived exosomes protect ischemic myocardium from acute ischemia/reperfusion injury. Biochem. Biophys. Res. Comm. 431, 566-571 (2013).
85. Yu, B. et al. Cardiomyocyte protection by GATA-4 gene engineered mesenchymal stem cells is partially mediated by translocation of miR-221 in microvesicles. PLoS ONE 8, e73304 (2013).
86. Bang, C. et al. Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J. Clin. Invest. 124, 2136-2146 (2014).
87. Bellera, N. et al. Single intracoronary injection of encapsulated antagomir-92a promotes angiogenesis and prevents adverse infarct remodeling. J. Am. Heart Assoc. 3, e000946 (2014).
88. van Rooij, E. &Kauppinen, S. Development of microRNA therapeutics is coming of age. EMBO Mol. Med. 6, 851-864 (2014).
89. Kota, J. et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137, 1005-1017 (2009).
90. US National Library of Medicine. ClinicalTrial.gov [online], http://clinicaltrials.gov/ct2/show/NCT01829971 (2014).
91. Bonci, D. et al. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat. Med. 14, 1271-1277 (2008).
92. Schäfer, F., Wagner, J., Knau, A., Dimmeler, S. &Heckel, A. Regulating angiogenesis with light-inducible antimiRs. Angew. Chem. Int. Ed. Engl. 52, 13558-13561 (2013).
93. Bish, L. T. et al. Adeno-associated virus (AAV) serotype 9 provides global cardiac gene transfer superior to AAV1, AAV6, AAV7, and AAV8 in the mouse and rat. Hum. Gene Ther. 19, 1359-1368 (2008).