MiRNA-1/133a clusters regulate adrenergic control of cardiac repolarization

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Besser, Johannes ^a   Malan, Daniela ^b   Wystub, Katharina ^a   Bachmann, Angela ^a   Wietelmann, Astrid ^a   Sasse, Philipp ^b   Fleischmann, Bernd K ^b   Braun, Thomas ^a   Boettger, Thomas ^a  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL L TYPE; MICRORNA; MICRORNA 1; PROTEIN MIR 133A; UNCLASSIFIED DRUG; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; ISOPRENALINE; MIRN1 MICRORNA, MOUSE; MIRN133 MICRORNA, MOUSE;

ADRENERGIC SYSTEM; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLUSTER ANALYSIS; HEART DEPOLARIZATION; HEART ELECTROPHYSIOLOGY; HEART MUSCLE FIBER MEMBRANE POTENTIAL; HEART RATE; HEART REPOLARIZATION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; QT PROLONGATION; SIGNAL TRANSDUCTION; ACTION POTENTIAL; ANIMAL; ANTIBODY SPECIFICITY; CELL CULTURE; DRUG EFFECTS; ELECTROCARDIOGRAPHY; GENE INACTIVATION; GENETICS; HEART MUSCLE CELL; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY; PROCEDURES;

ACTION POTENTIALS; ADRENERGIC BETA-AGONISTS; ANIMALS; CALCIUM CHANNELS, L-TYPE; CELLS, CULTURED; ELECTROCARDIOGRAPHY; GENE KNOCKOUT TECHNIQUES; ISOPROTERENOL; MICE; MICRORNAS; MULTIGENE FAMILY; MYOCYTES, CARDIAC; ORGAN SPECIFICITY;

EID: 84913550674     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113449     Document Type: Article

References (39)

1. Boettger T, Braun T (2012) A new level of complexity: the role of microRNAs in cardiovascular development. Circulation research 110: 1000-1013.
2. Zhao Y, Ransom JF, Li A, Vedantham V, von Drehle M, et al. (2007) Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 129: 303-317.
3. Costantini DL, Arruda EP, Agarwal P, Kim KH, Zhu Y, et al. (2005) The homeodomain transcription factor Irx5 establishes the mouse cardiac ventricular repolarization gradient. Cell 123: 347-358.
4. Guo W, Jung WE, Marionneau C, Aimond F, Xu H, et al. (2005) Targeted deletion of Kv4.2 eliminates I(to,f) and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circ Res 97: 1342-1350.
5. Heidersbach A, Saxby C, Carver-Moore K, Huang Y, Ang YS, et al. (2013) microRNA-1 regulates sarcomere formation and suppresses smooth muscle gene expression in the mammalian heart. Elife 2: e01323.
6. Liu N, Bezprozvannaya S, Williams AH, Qi X, Richardson JA, et al. (2008) microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev 22: 3242-3254.
7. Wystub K, Besser J, Bachmann A, Boettger T, Braun T (2013) miR-1/133a clusters cooperatively specify the cardiomyogenic lineage by adjustment of myocardin levels during embryonic heart development. PLoS Genet 9: e1003793.
8. Terentyev D, Belevych AE, Terentyeva R, Martin MM, Malana GE, et al. (2009) miR-1 overexpression enhances Ca(2+) release and promotes cardiac arrhythmogenesis by targeting PP2A regulatory subunit B56alpha and causing CaMKII-dependent hyperphosphorylation of RyR2. Circulation research 104: 514-521.
9. Belevych AE, Sansom SE, Terentyeva R, Ho HT, Nishijima Y, et al. (2011) MicroRNA-1 and -133 increase arrhythmogenesis in heart failure by dissociating phosphatase activity from RyR2 complex. PLoS One 6: e28324.
10. Su H, Mills AA, Wang X, Bradley A (2002) A targeted X-linked CMV-Cre line. Genesis 32: 187-188.
11. O'Connell TD, Rodrigo MC, Simpson PC (2007) Isolation and culture of adult mouse cardiac myocytes. Methods Mol Biol 357: 271-296.
12. Morris SA, Weiss LM, Factor S, Bilezikian JP, Tanowitz H, et al. (1989) Verapamil ameliorates clinical, pathologic and biochemical manifestations of experimental chagasic cardiomyopathy in mice. J Am Coll Cardiol 14: 782-789.
13. Larson AC, White RD, Laub G, McVeigh ER, Li D, et al. (2004) Self-gated cardiac cine MRI. Magn Reson Med 51: 93-102.
14. Bruegmann T, Malan D, Hesse M, Beiert T, Fuegemann CJ, et al. (2010) Optogenetic control of heart muscle in vitro and in vivo. Nat Methods 7: 897-900.
15. Knollmann BC, Casimiro MC, Katchman AN, Sirenko SG, Schober T, et al. (2004) Isoproterenol exacerbates a long QT phenotype in Kcnq1-deficient neonatal mice: possible roles for human-like Kcnq1 isoform 1 and slow delayed rectifier K+ current. J Pharmacol Exp Ther 310: 311-318.
16. Drici MD, Arrighi I, Chouabe C, Mann JR, Lazdunski M, et al. (1998) Involvement of IsK-associated K+ channel in heart rate control of repolarizationin a murine engineered model of Jervell and Lange-Nielsen syndrome. Circulation research 83: 95-102.
17. Rau F, Freyermuth F, Fugier C, Villemin JP, Fischer MC, et al. (2011) Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nature structural & molecular biology 18: 840-845.
18. Jia XM, Zheng SH, Xie XX, Zhang YJ, Wang WZ, et al. (2013) MicroRNA-1 Accelerates the Shortening of Atrial Effective Refractory Period by Regulating KCNE1 and KCNB2 Expression: An Atrial Tachypacing Rabbit Model. Plos One 8.
19. Wang L, Feng ZP, Kondo CS, Sheldon RS, Duff HJ (1996) Developmental changes in the delayed rectifier K+ channels in mouse heart. Circ Res 79: 79-85.
20. Fiset C, Clark RB, Larsen TS, Giles WR (1997) A rapidly activating sustained K+ current modulates repolarization and excitation-contraction coupling in adult mouse ventricle. J Physiol 504 (Pt 3): 557-563.
21. Ridley JM, Milnes JT, Zhang YH, Witchel HJ, Hancox JC (2003) Inhibition of HERG K+ current and prolongation of the guinea-pig ventricular action potential by 4-aminopyridine. J Physiol 549: 667-672.
22. Splawski I, Timothy KW, Sharpe LM, Decher N, Kumar P, et al. (2004)Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119: 19-31.
23. Drum BM, Dixon RE, Yuan C, Cheng EP, Santana LF (2014) Cellular mechanisms of ventricular arrhythmias in a mouse model of Timothy syndrome (long QT syndrome 8). J Mol Cell Cardiol 66: 63-71.
24. Nuyens D, Stengl M, Dugarmaa S, Rossenbacker T, Compernolle V, et al. (2001) Abrupt rate accelerations or premature beats cause life-threatening arrhythmias in mice with long-QT3 syndrome. Nat Med 7: 1021-1027.
25. Schwartz PJ, Priori SG, Locati EH, Napolitano C, Cantu F, et al. (1995) Long QT syndrome patients with mutations of the SCN5A and HERG genes have differential responses to Na+ channel blockade and to increases in heart rate. Implications for gene-specific therapy. Circulation 92: 3381-3386.
26. Priori SG, Napolitano C, Cantu F, Brown AM, Schwartz PJ (1996) Differential response to Na+ channel blockade, beta-adrenergic stimulation, and rapid pacing in a cellular model mimicking the SCN5A and HERG defects present in the long-QT syndrome. Circ Res 78: 1009-1015.
27. Tranquillo JV, Hlavacek J, Henriquez CS (2005) An integrative model of mouse cardiac electrophysiology from cell to torso. Europace 7 Suppl 2: 56-70.
28. Grimm M, Brown JH (2010) Beta-adrenergic receptor signaling in the heart: role of CaMKII. Journal of molecular and cellular cardiology 48: 322-330.
29. Webster G, Berul CI (2013) An update on channelopathies: from mechanisms to management. Circulation 127: 126-140.
30. Takenaka K, Ai T, Shimizu W, Kobori A, Ninomiya T, et al. (2003) Exercise stress test amplifies genotype-phenotype correlation in the LQT1 and LQT2 forms of the long-QT syndrome. Circulation 107: 838-844.
31. Hedley PL, Jorgensen P, Schlamowitz S, Wangari R, Moolman-Smook J, et al. (2009) The genetic basis of long QT and short QT syndromes: a mutation update. Human mutation 30: 1486-1511.
32. Harvey RD, Hell JW (2013) CaV1.2 signaling complexes in the heart. J Mol Cell Cardiol 58: 143-152.
33. Hofmann F, Flockerzi V, Kahl S, Wegener JW (2014) L-type CaV1.2 calcium channels: from in vitro findings to in vivo function. Physiol Rev 94: 303-326.
34. Castaldi A, Zaglia T, Di Mauro V, Carullo P, Viggiani G, Borile G, Di Stefano B, Schiattarella GG, Gualazzi MG, Elia L, Stirparo GG, Colorito ML, Pironti G, Kunderfranco P, Esposito G, Bang ML, Mongillo M, Condorelli G and Catalucci D. MicroRNA-133 modulates the beta1-adrenergic receptor transduction cascade. Circulation research. 2014;115:273-83.
35. Fischer TH, Neef S, Maier LS (2013) The Ca-calmodulin dependent kinase II: a promising target for future antiarrhythmic therapies? J Mol Cell Cardiol 58: 182-187.
36. Ali R, Huang Y, Maher SE, Kim RW, Giordano FJ, et al. (2012) miR-1 mediated suppression of Sorcin regulates myocardial contractility through modulation of Ca2+ signaling. J Mol Cell Cardiol 52: 1027-1037.
37. Fowler MR, Colotti G, Chiancone E, Higuchi Y, Seidler T, et al. (2009) Complex modulation of L-type Ca(2+) current inactivation by sorcin in isolated rabbit cardiomyocytes. Pflugers Arch 457: 1049-1060.
38. Care A, Catalucci D, Felicetti F, Bonci D, Addario A, et al. (2007) MicroRNA- 133 controls cardiac hypertrophy. Nat Med 13: 613-618.
39. Yang B, Lin H, Xiao J, Lu Y, Luo X, et al. (2007) The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nature medicine 13: 486-491.