Macro advances in microRNAs and myocardial regeneration

Current Opinion in Cardiology

Volumn 29, Issue 3, 2014, Pages 207-213

  Wang, Jun ^a   Martin, James F ^a,b,c  

^a Department of Molecular Physiology and Biophysics Cardiomyocyte Renewal Laboratory   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TEXAS HEART INSTITUTE   (United States)

Author keywords

cardiac injury; cardiomyocyte; microRNA; regeneration

Indexed keywords

CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 1; MICRORNA; MICRORNA 15; MICRORNA 15A; MICRORNA 16; MICRORNA 17; MICRORNA 199A; MICRORNA 19A; MICRORNA 19B; MICRORNA 20A; MICRORNA 214; MICRORNA 34A; MICRORNA 590; MICRORNA 92; MICRORNA 92A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PROTEIN HOMER 1; SERUM RESPONSE FACTOR; UNCLASSIFIED DRUG;

ANGIOGENESIS; APOPTOSIS; CELL DEATH; CELL DIFFERENTIATION; CELL METABOLISM; CELL MIGRATION; CELL PROLIFERATION; GENE OVEREXPRESSION; HEART FUNCTION; HEART INJURY; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE REGENERATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; TISSUE REGENERATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CLASSIFICATION; GENE EXPRESSION REGULATION; GENE THERAPY; GENETICS; HEART DISEASES; PATHOLOGY; PHYSIOLOGY; REGENERATION; TRENDS;

ANIMALS; CELL PHYSIOLOGICAL PROCESSES; GENE EXPRESSION REGULATION; GENETIC THERAPY; HEART DISEASES; HUMANS; MICRORNAS; MYOCYTES, CARDIAC; REGENERATION;

EID: 84899470991     PISSN: 02684705     EISSN: 15317080     Source Type: Journal    
DOI: 10.1097/HCO.0000000000000050     Document Type: Review

References (112)

1. Bui AL, Horwich TB, Fonarow GC. Epidemiology and risk profile of heart failure. Nat Rev Cardiol 2011; 8:30-41.
2. Go AS, Mozaffarian D, Roger VL, et al. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 2013; 127:e6-e245.
3. Stehlik J, Edwards LB, Kucheryavaya AY, et al. The Registry of the International Society for Heart and Lung Transplantation: twenty-eighth Adult Heart Transplant Report-2011. J Heart Lung Transplant 2011; 30:1078-1094.
4. Kikuchi K, Holdway JE, Werdich AA, et al. Primary contribution to zebrafish heart regeneration by gata4(\+) cardiomyocytes. Nature 2010; 464:601-605.
5. Poss KD. Getting to the heart of regeneration in zebrafish. Semin Cell Dev Biol 2007; 18:36-45.
6. Poss KD, Wilson LG, Keating MT. Heart regeneration in zebrafish. Science 2002; 298:2188-2190.
7. Wang J, Panakova D, Kikuchi K, et al. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 2011; 138:3421-3430.
8. Jopling C, Sleep E, Raya M, et al. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010; 464:606-609.
9. Bergmann O, Bhardwaj RD, Bernard S, et al. Evidence for cardiomyocyte renewal in humans. Science 2009; 324:98-102.
10. Mollova M, Bersell K, Walsh S, et al. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc Natl Acad Sci USA 2013; 110:1446-1451.
11. Kajstura J, Rota M, Cappetta D, et al. Cardiomyogenesis in the aging and failing human heart. Circulation 2012; 126:1869-1881.
12. Senyo SE, Steinhauser ML, Pizzimenti CL, et al. Mammalian heart renewal by preexisting cardiomyocytes. Nature 2013; 493:433-436.
13. Kajstura J, Urbanek K, Perl S, et al. Cardiomyogenesis in the adult human heart. Circ Res 2010; 107:305-315.
14. Whelan RS, Kaplinskiy V, Kitsis RN. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol 2010; 72:19-44.
15. Laflamme MA, Murry CE. Heart regeneration. Nature 2011; 473:326-335.
16. Passier R, van Laake LW, Mummery CL. Stem-cell-based therapy and lessons from the heart. Nature 2008; 453:322-329.
17. Segers VF, Lee RT. Stem-cell therapy for cardiac disease. Nature 2008; 451:937-942.
18. Ptaszek LM, Mansour M, Ruskin JN, Chien KR. Towards regenerative therapy for cardiac disease. Lancet 2012; 379:933-942.
19. Elliott DA, Braam SR, Koutsis K, et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat Methods 2011; 8:1037-1040.
20. Shiba Y, Fernandes S, Zhu WZ, et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012; 489:322-325.
21. Garbern JC, Lee RT. Cardiac stem cell therapy and the promise of heart regeneration. Cell Stem Cell 2013; 12:689-698.
22. Bolli R, Chugh AR, D'Amario D, et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011; 378:1847-1857.
23. Makkar RR, Smith RR, Cheng K, et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012; 379:895-904.
24. Tohyama S, Hattori F, Sano M, et al. Distinct metabolic flow enables largescale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 2013; 12:127-137.
25. Malliaras K, Zhang Y, Seinfeld J, et al. Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med 2013; 5:191-209.
26. Zangi L, Lui KO, von Gise A, et al. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol 2013; 31:898-907.
27. Loffredo FS, Steinhauser ML, Gannon J, Lee RT. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 2011; 8:389-398.
28. Beigi F, Schmeckpeper J, Pow-Anpongkul P, et al. C3orf58, a novel paracrine protein, stimulates cardiomyocyte cell-cycle progression through the PI3K-AKT-CDK7 pathway. Circ Res 2013; 113:372-380.
29. Engel FB, Schebesta M, Duong MT, et al. p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev 2005; 19: 1175-1187.
30. Kuhn B, del Monte F, Hajjar RJ, et al. Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nat Med 2007; 13:962-969.
31. Bersell K, Arab S, Haring B, Kuhn B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 2009; 138:257-270.
32. Burridge PW, Keller G, Gold JD, Wu JC. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 2012; 10:16-28.
33. Latinkic BV, Kotecha S, Mohun TJ. Induction of cardiomyocytes by GATA4 in Xenopus ectodermal explants. Development 2003; 130:3865-3876.
34. Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009; 459:708-711.
35. Chen JX, Krane M, Deutsch MA, et al. Inefficient reprogramming of fibroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5. Circ Res 2012; 111:50-55.
36. Ieda M, Fu JD, Delgado-Olguin P, et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010; 142:375-386.
37. Srivastava D, Ieda M. Critical factors for cardiac reprogramming. Circ Res 2012; 111:5-8.
38. Inagawa K, Ieda M. Direct reprogramming of mouse fibroblasts into cardiac myocytes. J Cardiovasc Transl Res 2013; 6:37-45.
39. Song K, Nam YJ, Luo X, et al. Heart repair by reprogramming nonmyocytes with cardiac transcription factors. Nature 2012; 485:599-604.
40. Jayawardena TM, Egemnazarov B, Finch EA, et al. MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ Res 2012; 110:1465-1473.
41. Nam YJ, Song K, Luo X, et al. Reprogramming of human fibroblasts toward a cardiac fate. Proc Natl Acad Sci USA 2013; 110:5588-5593.
42. Addis RC, Ifkovits JL, Pinto F, et al. Optimization of direct fibroblast reprogramming to cardiomyocytes using calcium activity as a functional measure of success. J Mol Cell Cardiol 2013; 60:97-106.
43. Fu JD, Stone NR, Liu L, et al. Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state. Stem Cell Rep 2013; 1:235-247.
44. Qian L, Huang Y, Spencer CI, et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012; 485:593-598.
45. Qian L, Berry EC, Fu JD, et al. Reprogramming of mouse fibroblasts into cardiomyocyte-like cells in vitro. Nat Protoc 2013; 8:1204-1215.
46. Heallen T, Morikawa Y, Leach J, et al. Hippo signaling impedes adult heart regeneration. Development 2013; 140:4683-4690.
47. Heallen T, Zhang M, Wang J, et al. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 2011; 332:458-461.
48. Xin M, Kim Y, Sutherland LB, et al. Hippo pathway effector Yap promotes cardiac regeneration. Proc Natl Acad Sci USA 2013; 110:13839-13844.
49. Porrello ER, Mahmoud AI, Simpson E, et al. Transient regenerative potential of the neonatal mouse heart. Science 2011; 331:1078-1080.
50. von Gise A, Lin Z, Schlegelmilch K, et al. YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc Natl Acad Sci USA 2012; 109:2394-2399.
51. Xin M, Kim Y, Sutherland LB, et al. Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci Signal 2011; 4:ra70.
52. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136:215-233.
53. van Rooij E, Olson EN. MicroRNAs: powerful new regulators of heart disease and provocative therapeutic targets. J Clin Invest 2007; 117:2369-2376.
54. Krek A, Grun D, Poy MN, et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37:495-500.
55. 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.
56. Yin VP, Thomson JM, Thummel R, et al. Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish. Genes Dev 2008; 22:728-733.
57. Williams AH, Valdez G, Moresi V, et al. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 2009; 326:1549-1554.
58. Liu N, Williams AH, Maxeiner JM, et al. microRNA-206 promotes skeletal muscle regeneration and delays progression of Duchenne muscular dystrophy in mice. J Clin Invest 2012; 122:2054-2065.
59. Xin M, Olson EN, Bassel-Duby R. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat Rev Mol Cell Biol 2013; 14:529-541.
60. Seeger FH, Zeiher AM, Dimmeler S. MicroRNAs in stem cell function and regenerative therapy of the heart. Arterioscler Thromb Vasc Biol 2013; 33:1739-1746.
61. Chen J, Wang DZ. microRNAs in cardiovascular development. J Mol Cell Cardiol 2012; 52:949-957.
62. Boettger T, Braun T. A new level of complexity: the role of microRNAs in cardiovascular development. Circ Res 2012; 110:1000-1013.
63. Ounzain S, Crippa S, Pedrazzini T. Small and long noncoding RNAs in cardiac homeostasis and regeneration. Biochim Biophys Acta 2013; 1833:923-933.
64. Addis RC, Epstein JA. Induced regeneration: the progress and promise of direct reprogramming for heart repair. Nat Med 2013; 19:829-836.
65. Christoffels VM, Pu WT. Developing insights into cardiac regeneration. Development 2013; 140:3933-3937.
66. Zhu H, Fan GC. Role of microRNAs in the reperfused myocardium towards postinfarct remodelling. Cardiovasc Res 2012; 94:284-292.
67. Quiat D, Olson EN. MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment. J Clin Invest 2013; 123:11-18.
68. van Rooij E, Olson EN. MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov 2012; 11:860-872.
69. Small EM,Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature 2011; 469:336-342.
70. Eulalio A, Mano M, Dal Ferro M, et al. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 2012; 492:376-381.
71. Cirera-Salinas D, Pauta M, Allen RM, et al. Mir-33 regulates cell proliferation and cell cycle progression. Cell Cycle 2012; 11:922-933.
72. Davalos A, Goedeke L, Smibert P, et al. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci USA 2011; 108:9232-9237.
73. Goedeke L, Vales-Lara FM, Fenstermaker M, et al. A regulatory role for microRNA 33-in controlling lipid metabolism gene expression. Mol Cell Biol 2013; 33:2339-2352.
74. Shiraishi-Yamaguchi Y, Furuichi T. The Homer family proteins. Genome Biol 2007; 8:206.
75. Rong R, Ahn JY, Huang H, et al. PI3 kinase enhancer-Homer complex couples mGluRI to PI3 kinase, preventing neuronal apoptosis. Nat Neurosci 2003; 6:1153-1161.
76. Hwang SY, Wei J, Westhoff JH, et al. Differential functional interaction of two Vesl/Homer protein isoforms with ryanodine receptor type 1: a novel mechanism for control of intracellular calcium signaling. Cell Calcium 2003; 34:177-184.
77. Feng W, Tu J, Yang T, et al. Homer regulates gain of ryanodine receptor type 1 channel complex. J Biol Chem 2002; 277:44722-44730.
78. Shin CH, Liu ZP, Passier R, et al. Modulation of cardiac growth and development by HOP, an unusual homeodomain protein. Cell 2002; 110:725-735.
79. Kook H, Epstein JA. Hopping to the beat. Hop regulation of cardiac gene expression. Trends Cardiovasc Med 2003; 13:261-264.
80. Obarzanek-Fojt M, Favre B, Kypriotou M, et al. Homeodomain-only protein HOP is a novel modulator of late differentiation in keratinocytes. Eur J Cell Biol 2011; 90:279-290.
81. Trivedi CM, Zhu W, Wang Q, et al. Hopx and Hdac2 interact to modulate Gata4 acetylation and embryonic cardiac myocyte proliferation. Dev Cell 2010; 19:450-459.
82. Yang JM, Sim SM, Kim HY, Park GT. Expression of the homeobox gene, HOPX, is modulated by cell differentiation in human keratinocytes and is involved in the expression of differentiation markers. Eur J Cell Biol 2010; 89:537-546.
83. Trivedi CM, Cappola TP, Margulies KB, Epstein JA. Homeodomain only protein x is down-regulated in human heart failure. J Mol Cell Cardiol 2011; 50:1056-1058.
84. 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.
85. Haghikia A, Missol-Kolka E, Tsikas D, et al. Signal transducer and activator of transcription 3-mediated regulation of miR-199a-5p links cardiomyocyte and endothelial cell function in the heart: a key role for ubiquitin-conjugating enzymes. Eur Heart J 2011; 32:1287-1297.
86. Greco S, Fasanaro P, Castelvecchio S, et al. MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes 2012; 61:1633-1641.
87. Baumgarten A, Bang C, Tschirner A, et al. TWIST1 regulates the activity of ubiquitin proteasome system via the miR-199/214 cluster in human endstage dilated cardiomyopathy. Int J Cardiol 2013; 168:1447-1452.
88. el Azzouzi H, Leptidis S, Dirkx E, et al. The hypoxia-inducible microRNA cluster miR-199a approximately 214 targets myocardial PPARdelta and impairs mitochondrial fatty acid oxidation. Cell Metab 2013; 18:341-354.
89. Wang J, Greene SB, Bonilla-Claudio M, et al. Bmp signaling regulates myocardial differentiation from cardiac progenitors through a MicroRNAmediated mechanism. Dev Cell 2010; 19:903-912.
90. Wang J, Bai Y, Li H, et al. MicroRNA-17-92, a direct Ap-2alpha transcriptional target, modulates T-box factor activity in orofacial clefting. PLoS Genet 2013; 9:e1003785.
91. Iaconetti C, Polimeni A, Sorrentino S, 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 2012; 107:296.
92. Bonauer A, Carmona G, Iwasaki M, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 2009; 324:1710-1713.
93. Chen J, Huang ZP, Seok HY, et al. mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ Res 2013; 112:1557-1566.
94. Olive V, Bennett MJ, Walker JC, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev 2009; 23:2839-2849.
95. Lakatta EG. Age-associated cardiovascular changes in health: impact on cardiovascular disease in older persons. Heart Fail Rev 2002; 7:29-49.
96. Boon RA, Iekushi K, Lechner S, et al. MicroRNA-34a regulates cardiac ageing and function. Nature 2013; 495:107-110.
97. Christoffersen NR, Shalgi R, Frankel LB, et al. p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ 2010; 17:236-245.
98. He L, He X, Lim LP, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447:1130-1134.
99. Hermeking H. MicroRNAs in the p53 network: micromanagement of tumour suppression. Nat Rev Cancer 2012; 12:613-626.
100. Xu Q, Seeger FH, Castillo J, et al. Micro-RNA-34a contributes to the impaired function of bone marrow-derived mononuclear cells from patients with cardiovascular disease. J Am Coll Cardiol 2012; 59:2107-2117.
101. Zhao T, Li J, Chen AF. MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am J Physiol Endocrinol Metab 2010; 299:E110-E116.
102. De Leon G, Sherry TC, Krucher NA. Reduced expression of PNUTS leads to activation of Rb-phosphatase and caspase-mediated apoptosis. Cancer Biol Ther 2008; 7:833-841.
103. Porrello ER, Johnson BA, Aurora AB, et al. MiR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ Res 2011; 109:670-679.
104. Small EM, Frost RJ, Olson EN. MicroRNAs add a new dimension to cardiovascular disease. Circulation 2010; 121:1022-1032.
105. Hullinger TG, Montgomery RL, Seto AG, et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res 2012; 110:71-81.
106. Porrello ER, Mahmoud AI, Simpson E, et al. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc Natl Acad Sci USA 2013; 110:187-192.
107. Zandi E, Rothwarf DM, Delhase M, et al. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 1997; 91:243-252.
108. Jin G, Klika A, Callahan M, et al. Identification of a human NF-kappaBactivating protein, TAB3. Proc Natl Acad Sci USA 2004; 101:2028-2033.
109. Ding J, Huang S, Wang Y, et al. Genome-wide screening reveals that miR-195 targets the TNF-alpha/NF-kappaB pathway by down-regulating IkappaB kinase alpha and TAB3 in hepatocellular carcinoma. Hepatology 2013; 58:654-666.
110. He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature 2005; 435:828-833.
111. O'Donnell KA, Wentzel EA, Zeller KI, et al. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435:839-843.
112. Li T, Morgan MJ, Choksi S, et al. MicroRNAs modulate the noncanonical transcription factor NF-kappaB pathway by regulating expression of the kinase IKKalpha during macrophage differentiation. Nat Immunol 2010; 11:799-805.