Role of microRNAs in cardiac development and disease (Review)

Tian,Jing; An,Xinjiang; Niu,Ling

doi:10.3892/etm.2016.3932

Role of microRNAs in cardiac development and disease (Review)

Authors:
- Jing Tian
- Xinjiang An
- Ling Niu
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Affiliations: Department of Cardiology, Xuzhou Children's Hospital, Xuzhou, Jiangsu 221002, P.R. China
Published online on: November 28, 2016 https://doi.org/10.3892/etm.2016.3932
Pages: 3-8
Copyright: © Tian et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Heart disease-related deaths are the highest in most societies and congenital heart diseases account for approximately 40% of prenatal deaths and over 20% of mortality in the first few months after birth. Congenital heart disease affects approximately 1% of all newborns and is the causative factor for more deaths within the first year of life as compared to all other genetic defects. Advances in treatment approaches increased life expectancy and led to an expansion of adult population with clinical manifestation of congenital heart defects in up to 90% of the children born with congenital heart diseases. Regulation of cardiac gene expression involves multiple independent enhancers that play a critical role in maintaining a restricted and specific pattern of gene expression in the heart. Cardiac transcriptional pathways are intimately regulated by microRNAs (miRNAs), which are small, regulatory RNAs, approximately 22 nucleotides in length, also coded by specific genes. These miRNAs act as suppressors of gene expression by inhibiting translation and/or promoting degradation of target protein‑coding mRNAs. There are several miRNAs involved in the development of heart and dysregulation of specific miRNAs is associated with congenital and other cardiac defects. Stress responsive cardiac hypertrophy is orchestrated among other factors, by specific miRNAs. miRNAs such as miR‑499 are considered useful as biomarkers of a given heart disease. Therapeutic application of miRNAs is also envisaged considering the small size and specific effects of these molecules. In this review, we addressed different roles of miRNAs in the development and diseases of the heart.

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1	Trojnarska O, Grajek S, Katarzyński S and Kramer L: Predictors of mortality in adult patients with congenital heart disease. Cardiol J. 16:341–347. 2009.PubMed/NCBI
2	Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N, Hailpern SM, Ho M, Howard V, Kissela B, et al: American Heart Association Statistics Committee and Stroke Statistics Subcommittee: Heart disease and stroke statistics - 2008 update: A report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 117:e25–e146. 2008. View Article : Google Scholar : PubMed/NCBI
3	Khairy P, Ionescu-Ittu R, Mackie AS, Abrahamowicz M, Pilote L and Marelli AJ: Changing mortality in congenital heart disease. J Am Coll Cardiol. 56:1149–1157. 2010. View Article : Google Scholar : PubMed/NCBI
4	Bruneau BG: The developmental genetics of congenital heart disease. Nature. 451:943–948. 2008. View Article : Google Scholar : PubMed/NCBI
5	Olson EN: Gene regulatory networks in the evolution and development of the heart. Science. 313:1922–1927. 2006. View Article : Google Scholar : PubMed/NCBI
6	Olson EN: A decade of discoveries in cardiac biology. Nat Med. 10:467–474. 2004. View Article : Google Scholar : PubMed/NCBI
7	Wang DZ: MicroRNAs in cardiac development and remodeling. Pediatr Cardiol. 31:357–362. 2010. View Article : Google Scholar : PubMed/NCBI
8	Kiriakidou M, Tan GS, Lamprinaki S, De Planell-Saguer M, Nelson PT and Mourelatos Z: An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell. 129:1141–1151. 2007. View Article : Google Scholar : PubMed/NCBI
9	Humphreys DT, Westman BJ, Martin DI and Preiss T: MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc Natl Acad Sci USA. 102:16961–16966. 2005. View Article : Google Scholar : PubMed/NCBI
10	Liu N and Olson EN: MicroRNA regulatory networks in cardiovascular development. Dev Cell. 18:510–525. 2010. View Article : Google Scholar : PubMed/NCBI
11	Cai B, Pan Z and Lu Y: The roles of microRNAs in heart diseases: A novel important regulator. Curr Med Chem. 17:407–411. 2010. View Article : Google Scholar : PubMed/NCBI
12	Rota R, Ciarapica R, Giordano A, Miele L and Locatelli F: MicroRNAs in rhabdomyosarcoma: Pathogenetic implications and translational potentiality. Mol Cancer. 10:1202011. View Article : Google Scholar : PubMed/NCBI
13	Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell. 136:215–233. 2009. View Article : Google Scholar : PubMed/NCBI
14	Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, Doevendans PA, Mummery CL, Borlak J, Haverich A, et al: MicroRNAs in the human heart: A clue to fetal gene reprogramming in heart failure. Circulation. 116:258–267. 2007. View Article : Google Scholar : PubMed/NCBI
15	Zhao Y, Ransom JF, Li A, Vedantham V, von Drehle M, Muth AN, Tsuchihashi T, McManus MT, Schwartz RJ and Srivastava D: Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell. 129:303–317. 2007. View Article : Google Scholar : PubMed/NCBI
16	van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J and Olson EN: Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 316:575–579. 2007. View Article : Google Scholar : PubMed/NCBI
17	Carè A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, Bang ML, Segnalini P, Gu Y, Dalton ND, et al: MicroRNA-133 controls cardiac hypertrophy. Nat Med. 13:613–618. 2007. View Article : Google Scholar : PubMed/NCBI
18	Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI
19	Yi R, Qin Y, Macara IG and Cullen BR: Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17:3011–3016. 2003. View Article : Google Scholar : PubMed/NCBI
20	Filipowicz W, Bhattacharyya SN and Sonenberg N: Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet. 9:102–114. 2008. View Article : Google Scholar : PubMed/NCBI
21	Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, Li MZ, Mills AA, Elledge SJ, Anderson KV and Hannon GJ: Dicer is essential for mouse development. Nat Genet. 35:215–217. 2003. View Article : Google Scholar : PubMed/NCBI
22	Wienholds E, Koudijs MJ, van Eeden FJ, Cuppen E and Plasterk RH: The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat Genet. 35:217–218. 2003. View Article : Google Scholar : PubMed/NCBI
23	Chen JF, Murchison EP, Tang R, Callis TE, Tatsuguchi M, Deng Z, Rojas M, Hammond SM, Schneider MD, Selzman CH, et al: Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci USA. 105:2111–2116. 2008. View Article : Google Scholar : PubMed/NCBI
24	Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL and Wang DZ: The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 38:228–233. 2006. View Article : Google Scholar : PubMed/NCBI
25	Zhao Y, Samal E and Srivastava D: Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature. 436:214–220. 2005. View Article : Google Scholar : PubMed/NCBI
26	Srivastava D, Thomas T, Lin Q, Kirby ML, Brown D and Olson EN: Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat Genet. 16:154–160. 1997. View Article : Google Scholar : PubMed/NCBI
27	Liu N, Williams AH, Kim Y, McAnally J, Bezprozvannaya S, Sutherland LB, Richardson JA, Bassel-Duby R and Olson EN: An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc Natl Acad Sci USA. 104:20844–20849. 2007. View Article : Google Scholar : PubMed/NCBI
28	Liu N, Bezprozvannaya S, Williams AH, Qi X, Richardson JA, Bassel-Duby R and Olson EN: microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev. 22:3242–3254. 2008. View Article : Google Scholar : PubMed/NCBI
29	Goddeeris MM, Rho S, Petiet A, Davenport CL, Johnson GA, Meyers EN and Klingensmith J: Intracardiac septation requires hedgehog-dependent cellular contributions from outside the heart. Development. 135:1887–1895. 2008. View Article : Google Scholar : PubMed/NCBI
30	Latronico MV, Catalucci D and Condorelli G: MicroRNA and cardiac pathologies. Physiol Genomics. 34:239–242. 2008. View Article : Google Scholar : PubMed/NCBI
31	O'Brien JE Jr, Kibiryeva N, Zhou XG, Marshall JA, Lofland GK, Artman M, Chen J and Bittel DC: Noncoding RNA expression in myocardium from infants with tetralogy of Fallot. Circ Cardiovasc Genet. 5:279–286. 2012. View Article : Google Scholar : PubMed/NCBI
32	Yu ZB, Han SP, Bai YF, Zhu C, Pan Y and Guo XR: microRNA expression profiling in fetal single ventricle malformation identified by deep sequencing. Int J Mol Med. 29:53–60. 2012.PubMed/NCBI
33	Omran A, Elimam D, Webster KA, Shehadeh LA and Yin F: MicroRNAs: A new piece in the paediatric cardiovascular disease puzzle. Cardiol Young. 23:642–655. 2013. View Article : Google Scholar : PubMed/NCBI
34	Ikeda S, Kong SW, Lu J, Bisping E, Zhang H, Allen PD, Golub TR, Pieske B and Pu WT: Altered microRNA expression in human heart disease. Physiol Genomics. 31:367–373. 2007. View Article : Google Scholar : PubMed/NCBI
35	Tatsuguchi M, Seok HY, Callis TE, Thomson JM, Chen JF, Newman M, Rojas M, Hammond SM and Wang DZ: Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy. J Mol Cell Cardiol. 42:1137–1141. 2007. View Article : Google Scholar : PubMed/NCBI
36	van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA and Olson EN: Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA. 105:13027–13032. 2008. View Article : Google Scholar : PubMed/NCBI
37	Fichtlscherer S, Zeiher AM, Dimmeler S and Sessa WC: Circulating microRNAs: Biomarkers or mediators of cardiovascular diseases? Arterioscler Thromb Vasc Biol. 31:2383–2390. 2011. View Article : Google Scholar : PubMed/NCBI
38	Tijsen AJ, Pinto YM and Creemers EE: Circulating microRNAs as diagnostic biomarkers for cardiovascular diseases. Am J Physiol Heart Circ Physiol. 303:H1085–H1095. 2012. View Article : Google Scholar : PubMed/NCBI
39	Hunter JJ and Chien KR: Signaling pathways for cardiac hypertrophy and failure. N Engl J Med. 341:1276–1283. 1999. View Article : Google Scholar : PubMed/NCBI
40	van Rooij E, Sutherland LB, Liu N, Williams AH, McAnally J, Gerard RD, Richardson JA and Olson EN: A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci USA. 103:18255–18260. 2006. View Article : Google Scholar : PubMed/NCBI
41	Callis TE, Pandya K, Seok HY, Tang RH, Tatsuguchi M, Huang ZP, Chen JF, Deng Z, Gunn B, Shumate J, et al: MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest. 119:2772–2786. 2009. View Article : Google Scholar : PubMed/NCBI
42	Sayed D, Hong C, Chen IY, Lypowy J and Abdellatif M: MicroRNAs play an essential role in the development of cardiac hypertrophy. Circ Res. 100:416–424. 2007. View Article : Google Scholar : PubMed/NCBI
43	Matkovich SJ, Hu Y, Eschenbacher WH, Dorn LE and Dorn GW II: Direct and indirect involvement of microRNA-499 in clinical and experimental cardiomyopathy. Circ Res. 111:521–531. 2012. View Article : Google Scholar : PubMed/NCBI
44	Li C, Fang Z, Jiang T, Zhang Q, Liu C, Zhang C and Xiang Y: Serum microRNAs profile from genome-wide serves as a fingerprint for diagnosis of acute myocardial infarction and angina pectoris. BMC Med Genomics. 6:162013. View Article : Google Scholar : PubMed/NCBI
45	Kuwabara Y, Ono K, Horie T, Nishi H, Nagao K, Kinoshita M, Watanabe S, Baba O, Kojima Y, Shizuta S, et al: Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ Cardiovasc Genet. 4:446–454. 2011. View Article : Google Scholar : PubMed/NCBI
46	Ai X, Curran JW, Shannon TR, Bers DM and Pogwizd SM: Ca²⁺/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca²⁺ leak in heart failure. Circ Res. 97:1314–1322. 2005. View Article : Google Scholar : PubMed/NCBI
47	Wang GK, Zhu JQ, Zhang JT, Li Q, Li Y, He J, Qin YW and Jing Q: Circulating microRNA: A novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J. 31:659–666. 2010. View Article : Google Scholar : PubMed/NCBI
48	Zhang L, Chen X, Su T, Li H, Huang Q, Wu D, Yang C and Han Z: Circulating miR-499 are novel and sensitive biomarker of acute myocardial infarction. J Thorac Dis. 7:303–308. 2015.PubMed/NCBI
49	Hosoda T, Zheng H, Cabral-da-Silva M, Sanada F, Ide-Iwata N, Ogórek B, Ferreira-Martins J, Arranto C, D'Amario D, del Monte F, et al: Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation. 123:1287–1296. 2011. View Article : Google Scholar : PubMed/NCBI