MicroRNAs in Atrial Fibrillation: from Expression Signatures to Functional Implications

Nicoline W E van den Berg, Makiri Kawasaki, Wouter R Berger, Jolien Neefs, Eva Meulendijks, Anke J Tijsen, Joris R de Groot, Nicoline W E van den Berg, Makiri Kawasaki, Wouter R Berger, Jolien Neefs, Eva Meulendijks, Anke J Tijsen, Joris R de Groot

Abstract

Atrial fibrillation (AF) is the most common sustained arrhythmia and is associated with pronounced morbidity and mortality. Its prevalence, expected to further increase for the forthcoming years, and associated frequent hospitalizations turn AF into a major health problem. Structural and electrical atrial remodelling underlie the substrate for AF, but the exact mechanisms driving this remodelling remain incompletely understood. Recent studies have shown that microRNAs (miRNA), short non-coding RNAs that regulate gene expression, may be involved in the pathophysiology of AF. MiRNAs have been implicated in AF-induced ion channel remodelling and fibrosis. MiRNAs could therefore provide insight into AF pathophysiology or become novel targets for therapy with miRNA mimics or anti-miRNAs. Moreover, circulating miRNAs have been suggested as a new class of diagnostic and prognostic biomarkers of AF. However, the origin and function of miRNAs in tissue and plasma frequently remain unknown and studies investigating the role of miRNAs in AF vary in design and focus and even present contradicting results. Here, we provide a systematic review of the available clinical and functional studies investigating the tissue and plasma miRNAs in AF and will thereafter discuss the potential of miRNAs as biomarkers or novel therapeutic targets in AF.

Keywords: Atrial fibrillation; Electrical remodelling; Fibrosis; Therapy; microRNA.

Conflict of interest statement

J.R. de Groot received a grant from NWO/ZonMW(106.146.310). A.J. Tijsen received a grant from NWO/ZonMW(016.166.150). To the best of our knowledge, no conflict of interest, financial or other, exists for the co-authors. This article does not contain any original studies with human participants or animals performed by any of the authors. There were no human cases included and thus no informed consent was needed.

Figures

Fig. 1
Fig. 1
microRNAs expressed in plasma and tissue. This figure illustrates the number of miRNAs differentially expressed in tissue and in plasma in AF patients. Note the high number of upregulated miRNAs in tissue, whereas miRNAs in plasma more often have lower levels in AF. Furthermore, there is little overlap between tissue and plasma expression of the miRNAs that have lower or higher levels in AF (between the dotted lines). There is a substantial proportion of miRNAs that present contradicting results (miRNAs described to be both up- and downregulated in tissue or plasma)

References

    1. Ball J, Carrington MJ, McMurray JJV, et al. Atrial fibrillation: profile and burden of an evolving epidemic in the 21st century. Int J Cardiol. 2013;167:1807–1824. doi: 10.1016/j.ijcard.2012.12.093.
    1. Chen LY, Shen W-K. Epidemiology of atrial fibrillation: a current perspective. Hear Rhythm Off J Hear Rhythm Soc. 2007;4:S1–S6. doi: 10.1016/j.hrthm.2006.12.018.
    1. Andrade J, Khairy P, Dobrev D, et al. The clinical profile and pathophysiology of atrial fibrillation: relationships among clinical features, epidemiology, and mechanisms. Circ Res. 2014;114:1453–1468. doi: 10.1161/CIRCRESAHA.114.303211.
    1. Kirchhof P, Benussi S, Kotecha D, et al. 2016 ESC guidelines for the management of atrial fibrillation developed in collaboration with EACTS: the task force for the management of atrial fibrillation of the European Society of Cardiology (ESC)developed with the special contribution of the Europea. Eur Heart J 2016;:ehw210.
    1. Goette A, Kalman JM, Aguinaga L, et al. EHRA/HRS/APHRS/SOLAECE expert consensus on atrial cardiomyopathies: definition, characterisation, and clinical implication. 2016.
    1. Singh JP, Morady F. Patient selection and classification for atrial fibrillation ablation: thinking beyond duration. Hear Rhythm. 2009;6:1522–1525. doi: 10.1016/j.hrthm.2009.04.003.
    1. Woods CE, Olgin J. Atrial fibrillation therapy now and in the future: drugs, biologicals, and ablation. Circ Res. 2014;114:1532–1546. doi: 10.1161/CIRCRESAHA.114.302362.
    1. Smit MD, Van Gelder IC. New treatment options for atrial fibrillation: towards patient tailored therapy. Heart. 2011;97:1796–1802. doi: 10.1136/heartjnl-2011-300276.
    1. 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 U S A. 2006;103:18255–18260. doi: 10.1073/pnas.0608791103.
    1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297. doi: 10.1016/S0092-8674(04)00045-5.
    1. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 2008;2008:102–114. doi: 10.1038/nrg2290.
    1. Luo X, Yang B, Nattel S. MicroRNAs and atrial fibrillation: mechanisms and translational potential. Nat Rev Cardiol. 2015;12:80–90. doi: 10.1038/nrcardio.2014.178.
    1. Arora P, Wu C, Khan AM, et al. Atrial natriuretic peptide is negatively regulated by microRNA-425. J Clin Invest. 2013;123:3378–3382. doi: 10.1172/JCI67383.
    1. van Rooij E, Sutherland LB, Thatcher JE, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A. 2008;105:13027–13032. doi: 10.1073/pnas.0805038105.
    1. Girmatsion Z, Biliczki P, Bonauer A, et al. Changes in microRNA-1 expression and IK1 up-regulation in human atrial fibrillation. Hear Rhythm Off J Hear Rhythm Soc. 2009;6:1802–1809. doi: 10.1016/j.hrthm.2009.08.035.
    1. Qi X-Y, Huang H, Ordog B, et al. Fibroblast inward-rectifier potassium current upregulation in profibrillatory atrial remodeling. Circ Res. 2015;116:836–845. doi: 10.1161/CIRCRESAHA.116.305326.
    1. Adam O, Löhfelm B, Thum T, et al. Role of miR-21 in the pathogenesis of atrial fibrosis. Basic Res Cardiol. 2012;107:278. doi: 10.1007/s00395-012-0278-0.
    1. Cardin S, Guasch E, Luo X, et al. Role for MicroRNA-21 in atrial profibrillatory fibrotic remodeling associated with experimental postinfarction heart failure. Circ Arrhythm Electrophysiol. 2012;5:1027–1035. doi: 10.1161/CIRCEP.112.973214.
    1. Duisters RF, Tijsen AJ, Schroen B, et al. miR-133 and miR-30 Regulate Connective Tissue Growth Factor. Circ Res 2009;104.
    1. Chen X, Ba Y, Ma L, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18282.
    1. van Rooij E, Olson EN. MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov. 2012;11.
    1. Weckbach LT, Grabmaier U, Clauss S, et al. MicroRNAs as a diagnostic tool for heart failure and atrial fibrillation. Curr Opin Pharmacol. 2016;27:24–30. doi: 10.1016/j.coph.2016.01.001.
    1. Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci. 2008;105:10513–10518. doi: 10.1073/pnas.0804549105.
    1. Weber JA, Baxter DH, Zhang S, et al. The MicroRNA Spectrum in 12 body fluids. Clin Chem. 2010;56.
    1. Tijsen AJ, Creemers EE, Moerland PD, et al. MiR423-5p as a circulating biomarker for heart failure. Circ Res. 2010;106:1035–1039. doi: 10.1161/CIRCRESAHA.110.218297.
    1. Fichtlscherer S, De Rosa S, Fox H, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res. 2010;107:677–684. doi: 10.1161/CIRCRESAHA.109.215566.
    1. D’Alessandra Y, Devanna P, Limana F, et al. Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur Heart J. 2010;31:2765–2773. doi: 10.1093/eurheartj/ehq167.
    1. Devaux Y, Mueller M, Haaf P, et al. Diagnostic and prognostic value of circulating microRNAs in patients with acute chest pain. J Intern Med. 2015;277:260–271. doi: 10.1111/joim.12183.
    1. Wang G-K, Zhu J-Q, Zhang J-T, et al. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J. 2010;31:659–666. doi: 10.1093/eurheartj/ehq013.
    1. McManus DD, Lin H, Tanriverdi K, et al. Relations between circulating microRNAs and atrial fibrillation: data from the Framingham Offspring Study. Hear Rhythm Off J Hear Rhythm Soc. 2014;11:663–669. doi: 10.1016/j.hrthm.2014.01.018.
    1. Harling L, Lambert J, Ashrafian H, et al. Elevated serum microRNA 483-5p levels may predict patients at risk of post-operative atrial fibrillation. Eur J Cardio-Thoracic Surg Off J Eur Assoc Cardio-Thoracic Surg Published Online First: 2016.
    1. Yamac AH, Kucukbuzcu S, Ozansoy M, et al. Altered expression of micro-RNA 199a and increased levels of cardiac SIRT1 protein are associated with the occurrence of atrial fibrillation after coronary artery bypass graft surgery. Cardiovasc Pathol Off J Soc Cardiovasc Pathol. 2016;25:232–236. doi: 10.1016/j.carpath.2016.02.002.
    1. Slagsvold KH, Rognmo O, Høydal M, et al. Remote ischemic preconditioning preserves mitochondrial function and influences myocardial microRNA expression in atrial myocardium during coronary bypass surgery. Circ Res. 2014;114:851–859. doi: 10.1161/CIRCRESAHA.114.302751.
    1. Krogstad LEB, Slagsvold KH, Wahba A. Remote ischemic preconditioning and incidence of postoperative atrial fibrillation. Scand Cardiovasc J SCJ. 2015;49:117–122. doi: 10.3109/14017431.2015.1010565.
    1. Maesen B, Nijs J, Maessen J, et al. Post-operative atrial fibrillation: a maze of mechanisms. Europace. 2012;14.
    1. Goren Y, Meiri E, Hogan C, et al. Relation of reduced expression of MiR-150 in platelets to atrial fibrillation in patients with chronic systolic heart failure. Am J Cardiol. 2014;113:976–981. doi: 10.1016/j.amjcard.2013.11.060.
    1. Liu Z, Zhou C, Liu Y, et al. The expression levels of plasma micoRNAs in atrial fibrillation patients. PLoS One. 2012;7:1–9.
    1. Liu T, Zhong S, Rao F, et al. Catheter ablation restores decreased plasma miR-409-3p and miR-432 in atrial fibrillation patients. Eur Eur Pacing, Arrhythmias, Card Electrophysiol J Work Groups Card Pacing, Arrhythmias, Card Cell Electrophysiol Eur Soc Cardiol. 2016;18:92–99.
    1. Lu Y, Hou S, Huang D, et al. Expression profile analysis of circulating microRNAs and their effects on ion channels in Chinese atrial fibrillation patients. Int J Clin Exp Med. 2015;8:845–853.
    1. McManus DD, Tanriverdi K, Lin H, et al. Plasma microRNAs are associated with atrial fibrillation and change after catheter ablation (the miRhythm study) Hear Rhythm Off J Hear Rhythm Soc. 2015;12:3–10. doi: 10.1016/j.hrthm.2014.09.050.
    1. Schotten U, Verheule S, Kirchhof P, et al. Pathophysiological mechanisms of atrial fibrillation: a translational appraisal. Physiol Rev. 2011;91.
    1. Choudhury A, Chung I, Blann AD, et al. Platelet surface CD62P and CD63, mean platelet volume, and soluble/platelet P-selectin as indexes of platelet function in atrial fibrillation. J Am Coll Cardiol. 2007;49:1957–1964. doi: 10.1016/j.jacc.2007.02.038.
    1. Lu J, Guo S, Ebert BL, et al. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell. 2008;14:843–853. doi: 10.1016/j.devcel.2008.03.012.
    1. Cooley N, Cowley MJ, Lin RCY, et al. Influence of atrial fibrillation on microRNA expression profiles in left and right atria from patients with valvular heart disease. Physiol Genomics. 2012;44:211–219. doi: 10.1152/physiolgenomics.00111.2011.
    1. Lu Y, Zhang Y, Wang N, et al. MicroRNA-328 contributes to adverse electrical remodeling in atrial fibrillation. Circulation. 2010;122:2378–2387. doi: 10.1161/CIRCULATIONAHA.110.958967.
    1. Liu H, Qin H, Chen G, et al. Comparative expression profiles of microRNA in left and right atrial appendages from patients with rheumatic mitral valve disease exhibiting sinus rhythm or atrial fibrillation. J Transl Med. 2014;12:90. doi: 10.1186/1479-5876-12-90.
    1. Schotten U, Dobrev D, Platonov PG, et al. Current controversies in determining the main mechanisms of atrial fibrillation. J Intern Med. 2016;279:428–438. doi: 10.1111/joim.12492.
    1. Andrade J, Khairy P, Dobrev D, et al. The clinical profile and pathophysiology of atrial fibrillation: relationships among clinical features, epidemiology, and mechanisms. Circ Res. 2014;114:1453–1468. doi: 10.1161/CIRCRESAHA.114.303211.
    1. Nattel S, Harada M. Atrial remodeling and atrial fibrillation: recent advances and translational perspectives. J Am Coll Cardiol. 2014;63:2335–2345. doi: 10.1016/j.jacc.2014.02.555.
    1. Heijman J, Voigt N, Nattel S, et al. Cellular and molecular electrophysiology of atrial fibrillation initiation, maintenance, and progression. Circ Res. 2014;114
    1. Tamargo J, Caballero R, Gomez R, et al. Cardiac electrophysiological effects of nitric oxide. Cardiovasc Res. 2010;87:593–600. doi: 10.1093/cvr/cvq214.
    1. Reilly SN, Liu X, Carnicer R, et al. Up-regulation of miR-31 in human atrial fibrillation begets the arrhythmia by depleting dystrophin and neuronal nitric oxide synthase. Sci Transl Med. 2016;8:340ra74. doi: 10.1126/scitranslmed.aac4296.
    1. Nishi H, Sakaguchi T, Miyagawa S, et al. Impact of microRNA expression in human atrial tissue in patients with atrial fibrillation undergoing cardiac surgery. PLoS One. 2013;8 doi: 10.1371/journal.pone.0073397.
    1. Morishima M, Iwata E, Nakada C, et al. Atrial fibrillation-mediated upregulation of miR-30d regulates myocardial electrical remodeling of the G-protein-gated K(+) channel, IK.ACh. Circ J Off J Japanese Circ Soc. 2016;80:1346–1355.
    1. Watson CJ, Gupta SK, O’Connell E, et al. MicroRNA signatures differentiate preserved from reduced ejection fraction heart failure. Eur J Heart Fail. 2015;17:405–415. doi: 10.1002/ejhf.244.
    1. Liu H, Chen G, Liang M, et al. Atrial fibrillation alters the microRNA expression profiles of the left atria of patients with mitral stenosis. BMC Cardiovasc Disord. 2014;14:10. doi: 10.1186/1471-2261-14-10.
    1. Soeki T, Matsuura T, Bando S, et al. Relationship between local production of microRNA-328 and atrial substrate remodeling in atrial fibrillation: J Cardiol Published Online First; 2016.
    1. Cañón S, Caballero R, Herraiz-Martínez A, et al. miR-208b upregulation interferes with calcium handling in HL-1 atrial myocytes: implications win human chronic atrial fibrillation. J Mol Cell Cardiol. 2016;99:162–173. doi: 10.1016/j.yjmcc.2016.08.012.
    1. Barana A, Matamoros M, Dolz-Gaitón P, et al. Chronic atrial fibrillation increases microRNA-21 in human atrial myocytes decreasing L-type calcium current. Circ Arrhythm Electrophysiol. 2014;7:861–868. doi: 10.1161/CIRCEP.114.001709.
    1. Pandit SV, Berenfeld O, Anumonwo JMB, et al. Ionic determinants of functional reentry in a 2-D model of human atrial cells during simulated chronic atrial fibrillation. Biophys J. 2005;88:3806–3821. doi: 10.1529/biophysj.105.060459.
    1. Dobrev D, Graf E, Wettwer E, et al. Molecular basis of downregulation of G-protein-coupled inward rectifying K+ current (IK,ACh) in chronic human atrial fibrillation: decrease in GIRK4 mRNA correlates with reduced IK,ACh and muscarinic receptor-mediated shortening of action potentials. Circulation. 2001;104:2551–2557. doi: 10.1161/hc4601.099466.
    1. Kakimoto Y, Tanaka M, Kamiguchi H, et al. MicroRNA deep sequencing reveals chamber-specific miR-208 family expression patterns in the human heart. Int J Cardiol. 2016;211:43–48. doi: 10.1016/j.ijcard.2016.02.145.
    1. Jia X, Zheng S, Xie X, et al. MicroRNA-1 accelerates the shortening of atrial effective refractory period by regulating KCNE1 and KCNB2 expression: an atrial tachypacing rabbit model. PLoS One. 2013;8:e85639. doi: 10.1371/journal.pone.0085639.
    1. Christ T, Wettwer E, Ravens U. Letter by Christ et al regarding article, "Angiotensin II potentiates the slow component of delayed rectifier K+ current via the AT1 receptor in Guinea pig atrial Myocytes&quot. Circulation. 2006;114:e565. doi: 10.1161/CIRCULATIONAHA.106.639377.
    1. Yang B, Lin H, Xiao J, et al. The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med. 2007;13:486–491. doi: 10.1038/nm1569.
    1. 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. doi: 10.1016/j.cell.2007.03.030.
    1. Terentyev D, Belevych AE, Terentyeva R, et al. miR-1 overexpression enhances Ca2+ release and promotes cardiac Arrhythmogenesis by targeting PP2A regulatory subunit B56 and causing CaMKII-dependent hyperphosphorylation of RyR2. Circ Res. 2009;104:514–521. doi: 10.1161/CIRCRESAHA.108.181651.
    1. Luo X, Pan Z, Shan H, et al. MicroRNA-26 governs profibrillatory inward-rectifier potassium current changes in atrial fibrillation. J Clin Invest. 2013;123:1939–1951. doi: 10.1172/JCI62185.
    1. Chiang DY, Zhang M, Voigt N, et al. Identification of microRNA-mRNA dysregulations in paroxysmal atrial fibrillation. Int J Cardiol. 2015;184:190–197. doi: 10.1016/j.ijcard.2015.01.075.
    1. Xiao J, Liang D, Zhang Y, et al. MicroRNA expression signature in atrial fibrillation with mitral stenosis. Physiol Genomics. 2011;43:655–664. doi: 10.1152/physiolgenomics.00139.2010.
    1. Morishima M, Iwata E, Nakada C, et al. Atrial fibrillation-mediated upregulation of miR-30d regulates myocardial electrical remodeling of the G-protein-gated K(+) channel, IK.ACh. Circ J. 2016;80:1346–1355. doi: 10.1253/circj.CJ-15-1276.
    1. Voigt N, Trausch A, Knaut M, et al. Left-to-right atrial inward rectifier potassium current gradients in patients with paroxysmal versus chronic atrial fibrillation. Circ Arrhythmia Electrophysiol. 2010;3:472–480. doi: 10.1161/CIRCEP.110.954636.
    1. Dobrev D, Friedrich A, Voigt N, et al. The G protein-gated potassium current IK,ACh Is constitutively active in patients with chronic atrial fibrillation. Circulation. 2005;112:3697–3706. doi: 10.1161/CIRCULATIONAHA.105.575332.
    1. Ling T-Y, Wang X-L, Chai Q, et al. Regulation of the SK3 channel by microRNA-499--potential role in atrial fibrillation. Hear Rhythm Off J Hear Rhythm Soc. 2013;10:1001–1009. doi: 10.1016/j.hrthm.2013.03.005.
    1. Corsten MF, Dennert R, Jochems S, et al. Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet. 2010;3:499–506. doi: 10.1161/CIRCGENETICS.110.957415.
    1. Sossalla S, Kallmeyer B, Wagner S, et al. Altered Na(+) currents in atrial fibrillation effects of ranolazine on arrhythmias and contractility in human atrial myocardium. J Am Coll Cardiol. 2010;55:2330–2342. doi: 10.1016/j.jacc.2009.12.055.
    1. Gaspo R, Bosch RF, Bou-Abboud E, et al. Tachycardia-induced changes in Na+ current in a chronic dog model of atrial fibrillation. Circ Res. 1997;81:1045–1052. doi: 10.1161/01.RES.81.6.1045.
    1. Ellinor PT, Nam EG, Shea MA, et al. Cardiac sodium channel mutation in atrial fibrillation. Hear Rhythm. 2008;5:99–105. doi: 10.1016/j.hrthm.2007.09.015.
    1. Zhao Y, Huang Y, Li W, et al. Post-transcriptional regulation of cardiac sodium channel gene SCN5A expression and function by miR-192-5p. Biochim Biophys Acta. 1852;2015:2024–2034.
    1. Hove-Madsen L, Llach A, Bayes-Genís A, et al. Atrial fibrillation is associated with increased spontaneous calcium release from the sarcoplasmic reticulum in human atrial myocytes. Circulation. 2004;110:1358–1363. doi: 10.1161/01.CIR.0000141296.59876.87.
    1. Voigt N, Li N, Wang Q, et al. Enhanced sarcoplasmic reticulum Ca2+ leak and increased Na+−Ca2+ exchanger function underlie delayed afterdepolarizations in patients with chronic atrial fibrillation. Circulation. 2012;125:2059–2070. doi: 10.1161/CIRCULATIONAHA.111.067306.
    1. Li N, Chiang DY, Wang S, et al. Ryanodine receptor-mediated calcium leak drives progressive development of an atrial fibrillation substrate in a transgenic mouse model. Circulation. 2014;129:1276–1285. doi: 10.1161/CIRCULATIONAHA.113.006611.
    1. Harada M, Luo X, Murohara T, et al. MicroRNA regulation and cardiac calcium signaling: role in cardiac disease and therapeutic potential. Circ Res. 2014;114:689–705. doi: 10.1161/CIRCRESAHA.114.301798.
    1. Nattel S, Dobrev D. The multidimensional role of calcium in atrial fibrillation pathophysiology: mechanistic insights and therapeutic opportunities. Eur Heart J. 2012;33.
    1. Vest JA, Wehrens XHT, Reiken SR, et al. Defective cardiac ryanodine receptor regulation during atrial fibrillation. Circulation. 2005;111.
    1. Harada M, Luo X, Qi XY, et al. Transient receptor potential canonical-3 channel-dependent fibroblast regulation in atrial fibrillation. Circulation. 2012;126:2051–2064. doi: 10.1161/CIRCULATIONAHA.112.121830.
    1. Chiang DY, Kongchan N, Beavers DL, et al. Loss of microRNA-106b-25 cluster promotes atrial fibrillation by enhancing ryanodine receptor type-2 expression and calcium release. Circ Arrhythm Electrophysiol. 2014;7:1214–1222. doi: 10.1161/CIRCEP.114.001973.
    1. Burstein B, Nattel S. Atrial fibrosis: mechanisms and clinical relevance in atrial fibrillation. J Am Coll Cardiol. 2008;51:802–809. doi: 10.1016/j.jacc.2007.09.064.
    1. Krul SPJ, Berger WR, Smit NW, et al. Atrial fibrosis and conduction slowing in the left atrial appendage of patients undergoing thoracoscopic surgical pulmonary vein isolation for atrial fibrillation. Circ Arrhythmia Electrophysiol. 2015;8.
    1. Frustaci A, Chimenti C, Bellocci F, et al. Histological substrate of atrial biopsies in patients with lone atrial fibrillation. Circulation. 1997;96.
    1. Boldt A, Wetzel U, Lauschke J, et al. Fibrosis in left atrial tissue of patients with atrial fibrillation with and without underlying mitral valve disease. Heart. 2004;90:400–405. doi: 10.1136/hrt.2003.015347.
    1. Xu J, Cui G, Esmailian F, et al. Atrial extracellular matrix remodeling and the maintenance of atrial fibrillation. Circulation. 2004;109.
    1. Souders CA, Bowers SLK, Baudino TA. Cardiac fibroblast: the renaissance cell. Circ Res. 2009;105:1164–1176. doi: 10.1161/CIRCRESAHA.109.209809.
    1. Lin CS, Pan CH. Regulatory mechanisms of atrial fibrotic remodeling in atrial fibrillation. Cell Mol Life Sci. 2008;65:1489–1508. doi: 10.1007/s00018-008-7408-8.
    1. 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. doi: 10.1038/nature07511.
    1. Adam O, Zimmer C, Hanke N, et al. Inhibition of aldosterone synthase (CYP11B2) by torasemide prevents atrial fibrosis and atrial fibrillation in mice. J Mol Cell Cardiol. 2015;85:140–150. doi: 10.1016/j.yjmcc.2015.05.019.
    1. He X, Zhang K, Gao X, et al. Rapid atrial pacing induces myocardial fibrosis by down-regulating Smad7 via microRNA-21 in rabbit. Heart Vessels Published Online First: 2016.
    1. Huang Z, Chen X-J, Qian C, et al. Signal transducer and activator of transcription 3/MicroRNA-21 feedback loop contributes to atrial fibrillation by promoting atrial fibrosis in a rat sterile pericarditis model. Circ Arrhythm Electrophysiol. 2016;9.
    1. 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. doi: 10.1038/nature07511.
    1. Patrick DM, Montgomery RL, Qi X, et al. Stress-dependent cardiac remodeling occurs in the absence of microRNA-21 in mice. J Clin Invest. 2010;120:3912–3916. doi: 10.1172/JCI43604.
    1. Tijsen AJ, Pinto YM, Creemers EE. Non-cardiomyocyte microRNAs in heart failure. Cardiovasc Res. 2012;93:573–582. doi: 10.1093/cvr/cvr344.
    1. Xiong Q, Zhong Q, Zhang J, et al. Identification of novel miR-21 target proteins in multiple myeloma cells by quantitative proteomics. J Proteome Res. 2012;11:2078–2090. doi: 10.1021/pr201079y.
    1. Dawson K, Wakili R, Ordög B, et al. MicroRNA29: a mechanistic contributor and potential biomarker in atrial fibrillation. Circulation. 2013;127:1466–1475. doi: 10.1161/CIRCULATIONAHA.112.001207.
    1. Yuan C-T, Li X-X, Cheng Q-J, et al. MiR-30a regulates the atrial fibrillation-induced myocardial fibrosis by targeting snail 1. Int J Clin Exp Pathol. 2015;8:15527–15536.
    1. Li H, Li S, Yu B, et al. Expression of miR-133 and miR-30 in chronic atrial fibrillation in canines. Mol Med Rep. 2012;5:1457–1460.
    1. Slagsvold KH, Johnsen AB, Rognmo O, et al. Comparison of left versus right atrial myocardium in patients with sinus rhythm or atrial fibrillation - an assessment of mitochondrial function and microRNA expression. Physiol Rep 2014;2.
    1. Shan H, Zhang Y, Lu Y, et al. Downregulation of miR-133 and miR-590 contributes to nicotine-induced atrial remodelling in canines. Cardiovasc Res. 2009;83:465–472. doi: 10.1093/cvr/cvp130.
    1. Wang J, Wang Y, Han J, et al. Integrated analysis of microRNA and mRNA expression profiles in the left atrium of patients with nonvalvular paroxysmal atrial fibrillation: role of miR-146b-5p in atrial fibrosis. Hear Rhythm Off J Hear Rhythm Soc. 2015;12:1018–1026. doi: 10.1016/j.hrthm.2015.01.026.
    1. Wang J, Song S, Xie C, et al. MicroRNA profiling in the left atrium in patients with non-valvular paroxysmal atrial fibrillation. BMC Cardiovasc Disord. 2015;15:97. doi: 10.1186/s12872-015-0085-2.
    1. 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. doi: 10.1126/science.1139089.
    1. 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. doi: 10.1172/JCI36154.
    1. Morissette MR, Cook SA, Foo S, et al. Myostatin regulates cardiomyocyte growth through modulation of Akt signaling. Circ Res. 2006;99:15–24. doi: 10.1161/01.RES.0000231290.45676.d4.
    1. Montgomery RL, Hullinger TG, Semus HM, et al. Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation. 2011;124:1537–1547. doi: 10.1161/CIRCULATIONAHA.111.030932.
    1. Slagsvold KH, Johnsen AB, Rognmo O, et al. Mitochondrial respiration and microRNA expression in right and left atrium of patients with atrial fibrillation. Physiol Genomics. 2014;46:505–511. doi: 10.1152/physiolgenomics.00042.2014.
    1. Shen MJ, Choi E-K, Tan AY, et al. Neural mechanisms of atrial arrhythmias. Nat Rev Cardiol. 2012;9:30–39. doi: 10.1038/nrcardio.2011.139.
    1. Kovoor P, Wickman K, Maguire CT, et al. Evaluation of the role of I(KACh) in atrial fibrillation using a mouse knockout model. J Am Coll Cardiol. 2001;37:2136–2143. doi: 10.1016/S0735-1097(01)01304-3.
    1. Chen P-S, Chen LS, Fishbein MC, et al. Role of the autonomic nervous system in atrial fibrillation: pathophysiology and therapy. Circ Res. 2014;114:1500–1515. doi: 10.1161/CIRCRESAHA.114.303772.
    1. Deneke T, Chaar H, de Groot JR, et al. Shift in the pattern of autonomic atrial innervation in subjects with persistent atrial fibrillation. Hear Rhythm. 2011;8:1357–1363. doi: 10.1016/j.hrthm.2011.04.013.
    1. Zhang Y, Zheng S, Geng Y, et al. MicroRNA profiling of atrial fibrillation in canines: miR-206 modulates intrinsic cardiac autonomic nerve remodeling by regulating SOD1. PLoS One. 2015;10:e0122674. doi: 10.1371/journal.pone.0122674.
    1. Cioffi DL, Hubler TR, Scammell JG. Organization and function of the FKBP52 and FKBP51 genes. Curr Opin Pharmacol. 2011;11:308–313. doi: 10.1016/j.coph.2011.03.013.
    1. Kim D-J, Linnstaedt S, Palma J, et al. Plasma components affect accuracy of circulating cancer-related microRNA quantitation. J Mol Diagn. 2012;14:71–80. doi: 10.1016/j.jmoldx.2011.09.002.
    1. Cummins JM, Velculescu VE. Implications of micro-RNA profiling for cancer diagnosis. Oncogene. 2006;25:6220–6227. doi: 10.1038/sj.onc.1209914.
    1. Masè M, Grasso M, Avogaro L, et al. Selection of reference genes is critical for miRNA expression analysis in human cardiac tissue. A focus on atrial fibrillation. Sci Rep. 2017;7:41127. doi: 10.1038/srep41127.
    1. Creemers EE, Tijsen AJ, Pinto YM. Circulating MicroRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res. 2012;110:483–495. doi: 10.1161/CIRCRESAHA.111.247452.
    1. Rayner KJ, Hennessy EJ. Extracellular communication via microRNA: lipid particles have a new message. J Lipid Res. 2013;54:1174–1181. doi: 10.1194/jlr.R034991.
    1. Bang C, Batkai S, Dangwal S, et al. Cardiac fibroblast–derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest. 2014;124:2136–2146. doi: 10.1172/JCI70577.
    1. Arroyo JD, Chevillet JR, Kroh EM, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A. 2011;108:5003–5008. doi: 10.1073/pnas.1019055108.
    1. Turchinovich A, Tonevitsky AG, Cho WC, et al. Check and mate to exosomal extracellular miRNA: new lesson from a new approach. Front Mol Biosci. 2015;2:11. doi: 10.3389/fmolb.2015.00011.
    1. van Rooij E, Purcell AL, Levin AA. Developing microRNA therapeutics. Circ Res. 2012;110:496–507. doi: 10.1161/CIRCRESAHA.111.247916.
    1. Asokan A, Samulski RJ. An emerging adeno-associated viral vector pipeline for cardiac Gene therapy. Hum Gene Ther. 2013;24:906–913. doi: 10.1089/hum.2013.2515.
    1. Laurence J, Van Beusekom M. Translating MicroRNAs to the clinic. Academic Press 2017. chemical modifications are applied&f=false. Accessed 15 Mar 2017.
    1. Janssen HLA, Reesink HW, Lawitz EJ, et al. Treatment of HCV infection by targeting MicroRNA. N Engl J Med. 2013;368:1685–1694. doi: 10.1056/NEJMoa1209026.
    1. Elmén J, Lindow M, Schütz S, et al. LNA-mediated microRNA silencing in non-human primates. Nature. 2008;452:896–899. doi: 10.1038/nature06783.
    1. Grimm D, Streetz KL, Jopling CL, et al. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature. 2006;441:537–541. doi: 10.1038/nature04791.
    1. Li Y-D, Hong Y-F, Yusufuaji Y, et al. Altered expression of hyperpolarization-activated cyclic nucleotide-gated channels and microRNA-1 and -133 in patients with age-associated atrial fibrillation. Mol Med Rep. 2015;12:3243–3248.
    1. Torrado M, Franco D, Lozano-Velasco E, et al. A MicroRNA-transcription factor blueprint for early atrial Arrhythmogenic remodeling. Biomed Res Int. 2015;2015:263151. doi: 10.1155/2015/263151.
    1. Li H, Li S, Yu B, et al. Expression of miR-133 and miR-30 in chronic atrial fibrillation in canines. Mol Med Rep. 2012;5:1457–1460.

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