The cardiomyocyte molecular clock, regulation of Scn5a, and arrhythmia susceptibility

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 10, 2013, Pages

  Schroder, Elizabeth A ^a,b   Lefta, Mellani ^a,b   Zhang, Xiping ^a,b   Bartos, Daniel ^a,b   Feng, Han Zhong ^d   Zhao, Yihua ^c   Patwardhan, Abhijit ^a,c   Jin, Jian Ping ^d   Esser, Karyn A ^a,b   Delisle, Brian P ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac excitability; Circadian; Heart; Ion channels; Na+ cur rent; Scn5a

Indexed keywords

PROTEIN BMAL1; SODIUM CHANNEL; SODIUM CHANNEL NAV1.5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING RATE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DISEASE PREDISPOSITION; ELECTROCARDIOGRAM; ELECTROSTIMULATION; FEMALE; GENE CONSTRUCT; GENE DELETION; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART RATE; HISTOPATHOLOGY; IN VITRO STUDY; ISOLATED HEART; MECHANICAL STIMULATION; MOLECULAR CLOCK; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QRS COMPLEX; RAT; SODIUM CURRENT; TELEMETRY; TRANSACTIVATION;

CARDIAC EXCITABILITY; CIRCADIAN; HEART; ION CHANNELS; NA+ CURRENT; SCN5A;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; ARRHYTHMIAS, CARDIAC; BIOLOGICAL CLOCKS; BLOOD PRESSURE; CARDIOMYOPATHIES; CELL LINE; CIRCADIAN RHYTHM; GENE DELETION; HEART RATE; MICE; MICE, TRANSGENIC; MYOCYTES, CARDIAC; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; PROMOTER REGIONS, GENETIC; RATS; RATS, INBRED WKY;

MUS; RATTUS;

EID: 84878648007     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00383.2012     Document Type: Article

References (58)

1. CAST II Investigators. Effect of the antiarrhythmic agent moricizine on survival after myocardial infarction. The Cardiac Arrhythmia Suppression Trial II Investigators. N Engl J Med 327: 227-233, 1992.
2. CAST Investigators. Preliminary report: effect of encainide, and flecain-ide on mortality in a randomized trial of arrhythmia suppression after myocardial infarction. The Cardiac Arrhythmia Suppression Trial (CAST) Investigators. N Engl J Med 321: 406-412, 1989.
3. Abriel H. Roles and regulation of the cardiac sodium channel Nav1.5: recent insights from experimental studies. Cardiovasc Res 76: 381-389, 2007.
4. Agah R, Frenkel PA, French BA, Michael LH, Overbeek PA, Schneider MD. Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrange-ment in adult ventricular muscle in vivo. J Clin Invest 100: 169-179, 1997.
5. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, Gant TW, Hastings MH, Kyriacou CP. Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12: 540-550, 2002.
6. Amin AS, Asghari-Roodsari A, Tan HL. Cardiac sodium channelopa-thies. Pflügers Arch 460: 223-237, 2010.
7. Amin AS, Tan HL, Wilde AA. Cardiac ion channels in health and disease. Heart Rhythm 7: 117-126, 2010.
8. Andersson KB, Birkeland JA, Finsen AV, Louch WE, Sjaastad I, Wang Y, Chen J, Molkentin JD, Chien KR, Sejersted OM, Christensen G. Moderate heart dysfunction in mice with inducible cardiomyo-cyte-specific excision of the Serca2 gene. J Mol Cell Cardiol 47: 180-187, 2009.
9. Ballesta A, Dulong S, Abbara C, Cohen B, Okyar A, Clairambault J, Levi F. a combined experimental and mathematical approach for molec-ular-based optimization of irinotecan circadian delivery. PLoS Comput Biol 7: e1002143, 2011.
10. Banerjee I, Fuseler JW, Price RL, Borg TK, Baudino TA. Determina-tion of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 293: H1883-H1891, 2007.
11. Bezzina CR, Shimizu W, Yang P, Koopmann TT, Tanck MW, Miy-amoto Y, Kamakura S, Roden DM, Wilde AA. Common sodium channel promoter haplotype in Asian subjects underlies variability in cardiac conduction. Circulation 113: 338-344, 2006.
12. Bray MS, Shaw CA, Moore MW, Garcia RA, Zanquetta MM, Durgan DJ, Jeong WJ, Tsai JY, Bugger H, Zhang D, Rohrwasser A, Rennison JH, Dyck JR, Litwin SE, Hardin PE, Chow CW, Chandler MP, Abel ED, Young ME. Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. Am J Physiol Heart Circ Physiol 294: H1036-H1047, 2008.
13. Bray MS, Young ME. The role of cell-specific circadian clocks in metabolism and disease. Obes Rev 10: 6-13, 2009.
14. Challet E, Takahashi JS, Turek FW. Nonphotic phase-shifting in Clock mutant mice. Brain Res 859: 398-403, 2000.
15. Chen Q, Kirsch GE, Zhang D, Brugada R, Brugada J, Brugada P, Potenza D, Moya A, Borggrefe M, Breithardt G, Ortiz-Lopez R, Wang Z, Antzelevitch C, O'Brien RE, Schulze-Bahr E, Keating MT, Towbin JA, Wang Q. Genetic basis and molecular mechanism for idiopathic ventricular fibrillation. Nature 392: 293-296, 1998.
16. Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72: 517-549, 2010.
17. Dick DJ, Lab MJ. Mechanical modulation of stretch-induced premature ventricular beats: induction of a mechanoelectric adaptation period. Car-diovasc Res 38: 181-191, 1998.
18. Durgan DJ, Tsai JY, Grenett MH, Pat BM, Ratcliffe WF, Villegas-Montoya C, Garvey ME, Nagendran J, Dyck JRB, Bray MS, Gamble KL, Gimble JM, Young ME. Evidence suggesting that the cardiomyo-cyte circadian clock modulates responsiveness of the heart to hypertrophic stimuli in mice. Chronobiol Int 28: 187-203, 2011.
19. Durgan DJ, Young ME. The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res 106: 647-658, 2010.
20. Eckardt D, Theis M, Degen J, Ott T, van Rijen HV, Kirchhoff S, Kim JS, de Bakker JM, Willecke K. Functional role of connexin43 gap junction channels in adult mouse heart assessed by inducible gene deletion. J Mol Cell Cardiol 36: 101-110, 2004.
21. Feng HZ, Biesiadecki BJ, Yu ZB, Hossain MM, Jin JP. Restricted N-terminal truncation of cardiac troponin T: a novel mechanism for functional adaptation to energetic crisis. J Physiol 586: 3537-3550, 2008.
22. Fukuda K, Davies SS, Nakajima T, Ong BH, Kupershmidt S, Fessel J, Amarnath V, Anderson ME, Boyden PA, Viswanathan PC, Roberts LJ 2nd, Balser JR. Oxidative mediated lipid peroxidation recapitulates proarrhythmic effects on cardiac sodium channels. Circ Res 97: 1262-1269, 2005.
23. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ. Role of the CLOCK protein in the mammalian circadian mechanism. Science 280: 1564-1569, 1998.
24. Hall ME, Smith G, Hall JE, Stec DE. Systolic dysfunction in cardiac-specific ligand-inducible MerCreMer transgenic mice. Am J Physiol Heart Circ Physiol 301: H253-H260, 2011.
25. Herrmann S, Fabritz L, Layh B, Kirchhof P, Ludwig A. Insights into sick sinus syndrome from an inducible mouse model. Cardiovasc Res 90: 38-48, 2011.
26. Hughes ME, Hogenesch JB, Kornacker K. JTK_CYCLE: an efficient non-parametric algorithm for detecting rhythmic components in genome-scale datasets. J Biol Rhythms 25: 372-380, 2010.
27. Janse M, Vermeulen J, Opthof T, Coronel R, Wilms-Schopman F, Rademaker H, Baartscheer A, Dekker L. Arrhythmogenesis in heart failure. J Cardiovasc Electrophysiol 4: 496-499, 2001.
28. Jeyaraj D, Haldar SM, Wan X, McCauley MD, Ripperger JA, Hu K, Lu Y, Eapen BL, Sharma N, Ficker E, Cutler MJ, Gulick J, Sanbe A, Robbins J, Demolombe S, Kondratov RV, Shea SA, Albrecht U, Wehrens XH, Rosenbaum DS, Jain MK. Circadian rhythms govern cardiac repolarization and arrhythmogenesis. Nature 483: 96-99, 2012.
29. Jin X, Shearman LP, Weaver DR, Zylka MJ, De Vries GJ, Reppert SM. A molecular mechanism regulating rhythmic output from the supra-chiasmatic circadian clock. Cell 96: 57-68, 1999.
30. Kamkin A, Kiseleva I, Wagner KD, Leiterer KP, Theres H, Scholz H, Günther J, Lab MJ. Mechano-electric feedback in right atrium after left ventricular infarction in rats. J Mol Cell Cardiol 32: 465-477, 2000.
31. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, Maywood ES, Hastings MH, Reppert SM. mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98: 193-205, 1999.
32. Lakatta EG, Yaniv Y, Maltsev VA. Minding the gaps that link intrinsic circadian clock within the heart to its intrinsic ultradian pacemaker clocks. Focus on "The cardiomyocyte molecular clock, regulation of Scn5a, and arrhythmia susceptibility." Am J Physiol Cell Physiol (March 13, 2013). doi:10.1152/ajpcell.00072.2013.
33. Lefta M, Campbell KS, Feng HZ, Jin JP, Esser KA. Development of dilated cardiomyopathy in Bmal1-deficient mice. Am J Physiol Heart Circ Physiol 303: H475-H485, 2012.
34. Lowrey PL, Takahashi JS. Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet 5: 407-441, 2004.
35. Lowrey PL, Takahashi JS. Genetics of circadian rhythms in mammalian model organisms. Adv Genet 74: 175-230, 2011.
36. Maltsev VA, Kyle JW, Mishra S, Undrovinas A. Molecular identity of the late sodium current in adult dog cardiomyocytes identified by Nav1.5 antisense inhibition. Am J Physiol Heart Circ Physiol 295: H667-H676, 2008.
37. Martino TA, Oudit GY, Herzenberg AM, Tata N, Koletar MM, Kabir GM, Belsham DD, Backx PH, Ralph MR, Sole MJ. Circadian rhythm disorganization produces profound cardiovascular and renal disease in hamsters. Am J Physiol Regul Integr Comp Physiol 294: R1675-R1683, 2008.
38. Martino TA, Tata N, Belsham DD, Chalmers J, Straume M, Lee P, Pribiag H, Khaper N, Liu PP, Dawood F, Backx PH, Ralph MR, Sole MJ. Disturbed diurnal rhythm alters gene expression and exacerbates cardiovascular disease with rescue by resynchronization. Hypertension 49: 1104-1113, 2007.
39. Menaker M, Takahashi JS, Eskin A. The physiology of circadian pacemakers. Annu Rev Physiol 40: 501-526, 1978.
40. Miyazaki M, Schroder E, Edelmann SE, Hughes ME, Kornacker K, Balke CW, Esser KA. Age-associated disruption of molecular clock expression in skeletal muscle of the spontaneously hypertensive rat. PLos One 6: e27168, 2011.
41. Molnar J, Zhang F, Weiss J, Ehlert FA, Rosenthal JE. Diurnal pattern of QTc interval: how long is prolonged?: possible relation to circadian triggers of cardiovascular events. J Am Coll Cardiol 27: 76-83, 1996.
42. Okutucu S, Karakulak UN, Sahiner L, Aytemir K, Demiri E, Evranos B, Fatihoglu SG, Kaya EB, Kabakci G, Tokgozoglu L, Ozkutlu H, Oto A. The relationship between circadian blood pressure pattern and ventric-ular repolarization dynamics assessed by QT dynamicity. Blood Press Monit 17: 14-19, 2012.
43. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB. Coordinated tran-scription of key pathways in the mouse by the circadian clock. Cell 109: 307-320, 2002.
44. Papadatos GA, Wallerstein PM, Head CE, Ratcliff R, Brady PA, Benndorf K, Saumarez RC, Trezise AE, Huang CL, Vandenberg JI, Colledge WH, Grace AA. Slowed conduction and ventricular tachycardia after targeted disruption of the cardiac sodium channel gene Scn5a. Proc Natl Acad Sci USA 99: 6210-6215, 2002.
45. Park JK, Martin LJ, Zhang X, Jegga AG, Benson DW. Genetic variants in SCN5A promoter are associated with arrhythmia phenotype severity in patients with heterozygous loss-of-function mutation. Heart Rhythm 9: 1090-1096, 2012.
46. Schroder E, Magyar J, Burgess D, Andres D, Satin J. Chronic vera-pamil treatment remodels ICa, L in mouse ventricle. Am J Physiol Heart Circ Physiol 292: H1906-H1916, 2007.
47. Shaw RM, Rudy Y. Electrophysiologic effects of acute myocardial ischemia: a theoretical study of altered cell excitability and action potential duration. Cardiovasc Res 35: 256-272, 1997.
48. Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, Tymitz KM, Penninger JM, Molkentin JD. Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res 89: 20-25, 2001.
49. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ. Extensive and divergent circadian gene expression in liver and heart. Nature 417: 78-83, 2002.
50. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz Charles J. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130: 730-741, 2007.
51. Tamanini F. Manipulation of mammalian cell lines for circadian studies. Methods Mol Biol 362: 443-453, 2007.
52. Tong X, Muchnik M, Chen Z, Patel M, Wu N, Joshi S, Rui L, Lazar MA, Yin L. Transcriptional repressor E4-binding protein 4 (E4BP4) regulates metabolic hormone fibroblast growth factor 21 (FGF21) during circadian cycles and feeding. J Biol Chem 285: 36401-36409, 2010.
53. Wilsbacher LD, Yamazaki S, Herzog ED, Song EJ, Radcliffe LA, Abe M, Block G, Spitznagel E, Menaker M, Takahashi JS. Photic and circadian expression of luciferase in mPeriod1-luc transgenic mice in vivo. Proc Natl Acad Sci USA 99: 489-494, 2002.
54. Yamazaki S, Takahashi JS. Real-time luminescence reporting of circadian gene expression in mammals. Methods Enzymol 393: 288-301, 2005.
55. Yang P, Koopmann TT, Pfeufer A, Jalilzadeh S, Schulze-Bahr E, Kaab S, Wilde AA, Roden DM, Bezzina CR. Polymorphisms in the cardiac sodium channel promoter displaying variant in vitro expression activity. Eur J Hum Genet 16: 350-357, 2008.
56. Yang P, Kupershmidt S, Roden DM. Cloning and initial characterization of the human cardiac sodium channel (SCN5A) promoter. Cardiovasc Res 61: 56-65, 2004.
57. Zambon A, McDearmon E, Salomonis N, Vranizan K, Johansen K, Adey D, Takahashi J, Schambelan M, Conklin B. Time-and exercise-dependent gene regulation in human skeletal muscle. Genome Biol 4: R61, 2003.
58. Zhang X, Patel SP, McCarthy JJ, Rabchevsky AG, Goldhamer DJ, Esser KA. A non-canonical E-box within the MyoD core enhancer is necessary for circadian expression in skeletal muscle. Nucleic Acids Res 40: 3419-3430, 2012.