Spatially discordant alternans and arrhythmias in tachypacing-induced cardiac myopathy in transgenic LQT1 rabbits: The importance of IKsand Ca2+ cycling

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Lau, Emily ^a   Kossidas, Konstantinos ^a   Kim, Tae Yun ^a   Kunitomo, Yukiko ^a   Ziv, Ohad ^a   Zhen, Song ^c   Taylor, Chantel ^a   Schofield, Lorraine ^a   Yammine, Joe ^a   Liu, Gongxin ^a   Peng, Xuwen ^b   Qu, Zhilin ^c   Koren, Gideon ^a   Choi, Bum Rak ^a  

^a BROWN UNIVERSITY   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM; VOLTAGE GATED POTASSIUM CHANNEL;

ACTION POTENTIAL DURATION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARRHYTHMOGENESIS; ARTICLE; CARDIOMYOPATHY; CARDIOVASCULAR RISK; COMPUTER SIMULATION; CONTROLLED STUDY; DOWN REGULATION; HEART ARRHYTHMIA; HEART DISEASE; HEART FAILURE; HEART PACING; HEART REPOLARIZATION; HEART VENTRICLE FIBRILLATION; HEART VENTRICLE REMODELING; IN VIVO STUDY; LONG QT SYNDROME 1; MALE; MOLECULAR PATHOLOGY; NONHUMAN; PROTEIN FUNCTION; QT INTERVAL; RISK ASSESSMENT; RR INTERVAL; SPATIALLY DISCORDANT ALTERNANS; TELEMETRY; TRANSGENIC RABBIT; ABNORMALITIES; ANIMAL; BRUGADA SYNDROME; DIAGNOSTIC IMAGING; ECHOCARDIOGRAPHY; HEART MUSCLE CONDUCTION SYSTEM; ION TRANSPORT; METABOLISM; MUSCLE DISEASE; PATHOPHYSIOLOGY; RABBIT; ROMANO-WARD SYNDROME; TRANSGENIC ANIMAL;

ORYCTOLAGUS CUNICULUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARRHYTHMIAS, CARDIAC; BRUGADA SYNDROME; CALCIUM; ECHOCARDIOGRAPHY; HEART CONDUCTION SYSTEM; HEART FAILURE; ION TRANSPORT; MALE; MUSCULAR DISEASES; POTASSIUM CHANNELS, VOLTAGE-GATED; RABBITS; ROMANO-WARD SYNDROME; VENTRICULAR FIBRILLATION;

EID: 84929340273     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122754     Document Type: Article

References (65)

1. Kjekshus J. Arrhythmias and mortality in congestive heart failure. Am J Cardiol. 1990; 65(19):42I-8I. Epub 1990/05/22. PubMed PMID: 2159694.
2. Chakko S, de Marchena E, Kessler KM, Myerburg RJ. Ventricular arrhythmias in congestive heart failure. Clin Cardiol. 1989; 12(9):525-30. Epub 1989/09/01. PubMed PMID: 2571440.
3. Rosamond W, Flegal K, Friday G, Furie K, Go A, Greenlund K, et al. Heart disease and stroke statistics - 2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2007; 115(5):e69-171. Epub 2006/12/30. CIRCULATIONAHA.106.179918 [pii] doi: 10.1161/CIRCULATIONAHA.106.179918 PubMed PMID: 17194875.
4. Ebinger MW, Krishnan S, Schuger CD. Mechanisms of ventricular arrhythmias in heart failure. Curr Heart Fail Rep. 2005; 2(3):111-7. Epub 2005/09/06. PubMed PMID: 16138946.
5. Janse MJ. Electrophysiological changes in heart failure and their relationship to arrhythmogenesis. Cardiovasc Res. 2004; 61(2):208-17. Epub 2004/01/23. S0008636303007272 [pii]. PubMed PMID: 14736537.
6. Li GR, Lau CP, Ducharme A, Tardif JC, Nattel S. Transmural action potential and ionic current remodeling in ventricles of failing canine hearts. Am J Physiol Heart Circ Physiol. 2002; 283(3):H1031-41. Epub 2002/08/16. doi: 10.1152/ajpheart.00105.2002 PubMed PMID: 12181133.
7. Nuss HB, Kaab S, Kass DA, Tomaselli GF, Marban E. Cellular basis of ventricular arrhythmias and abnormal automaticity in heart failure. Am J Physiol. 1999; 277(1 Pt 2):H80-91. Epub 1999/07/17. PubMed PMID: 10409185.
8. Harada M, Tsuji Y, Ishiguro YS, Takanari H, Okuno Y, Inden Y, et al. Rate-dependent shortening of action potential duration increases ventricular vulnerability in failing rabbit heart. Am J Physiol Heart Circ Physiol. 2011; 300(2):H565-73. Epub 2010/12/15. ajpheart.00209.2010 [pii] doi: 10.1152/ajpheart.00209.2010 PubMed PMID: 21148762.
9. Akar FG, Rosenbaum DS. Transmural electrophysiological heterogeneities underlying arrhythmogenesis in heart failure. Circ Res. 2003; 93(7):638-45. Epub 2003/08/23. doi: 10.1161/01.RES. 0000092248.59479.AE 01.RES.0000092248.59479.AE [pii]. PubMed PMID: 12933704.
10. Kaab S, Nuss HB, Chiamvimonvat N, O'Rourke B, Pak PH, Kass DA, et al. Ionic mechanism of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circ Res. 1996; 78(2):262-73. Epub 1996/02/01. PubMed PMID: 8575070.
11. Li GR, Lau CP, Leung TK, Nattel S. Ionic current abnormalities associated with prolonged action potentials in cardiomyocytes from diseased human right ventricles. Heart Rhythm. 2004; 1(4):460-8. Epub 2005/04/27. S1547-5271(04)00292-9 [pii] doi: 10.1016/j.hrthm.2004.06.003 PubMed PMID: 15851200.
12. Tsuji Y, Opthof T, Kamiya K, Yasui K, Liu W, Lu Z, et al. Pacing-induced heart failure causes a reduction of delayed rectifier potassium currents along with decreases in calcium and transient outward currents in rabbit ventricle. Cardiovasc Res. 2000; 48(2):300-9. Epub 2000/10/31. S0008-6363(00)00180-2 [pii]. PubMed PMID: 11054476.
13. Wang Y, Hill JA. Electrophysiological remodeling in heart failure. J Mol Cell Cardiol. 2010; 48(4):619-32. doi: 10.1016/j.yjmcc.2010.01.009 PubMed PMID: 20096285; PubMed Central PMCID: PMC2879059.
14. Tomaselli GF, Marban E. Electrophysiological remodeling in hypertrophy and heart failure. Cardiovasc Res. 1999; 42(2):270-83. PubMed PMID: 10533566.
15. Roden DM, Yang T. Protecting the heart against arrhythmias: potassium current physiology and repolarization reserve. Circulation. 2005; 112(10):1376-8. Epub 2005/09/08. 112/10/1376 [pii] doi: 10.1161/CIRCULATIONAHA.105.562777 PubMed PMID: 16145010.
16. Roden DM. Long QT syndrome: reduced repolarization reserve and the genetic link. J Intern Med. 2006; 259(1):59-69. Epub 2005/12/13. JIM1589 [pii] doi: 10.1111/j.1365-2796.2005.01589.x PubMed PMID: 16336514.
17. Roden DM. Repolarization reserve: a moving target. Circulation. 2008; 118(10):981-2. Epub 2008/09/ 04. 118/10/981 [pii] doi: 10.1161/CIRCULATIONAHA.108.798918 PubMed PMID: 18765386.
18. Roden DM. Taking the "idio" out of "idiosyncratic": predicting torsades de pointes. Pacing Clin Electrophysiol. 1998; 21(5):1029-34. PubMed PMID: 9604234.
19. Jost N, Papp JG, Varro A. Slow delayed rectifier potassium current (IKs) and the repolarization reserve. Ann Noninvasive Electrocardiol. 2007; 12(1):64-78. Epub 2007/02/09. ANEC140 [pii] doi: 10.1111/j.1542-474X.2007.00140.x PubMed PMID: 17286653.
20. Jost N, Virag L, Bitay M, Takacs J, Lengyel C, Biliczki P, et al. Restricting excessive cardiac action potential and QT prolongation: a vital role for IKs in human ventricular muscle. Circulation. 2005; 112 (10):1392-9. Epub 2005/09/01. CIRCULATIONAHA.105.550111 [pii] doi: 10.1161/ CIRCULATIONAHA.105.550111 PubMed PMID: 16129791.
21. Silva J, Rudy Y. Subunit interaction determines IKs participation in cardiac repolarization and repolarization reserve. Circulation. 2005; 112(10):1384-91. Epub 2005/09/01. CIRCULATIONAHA.105.543306 [pii] doi: 10.1161/CIRCULATIONAHA.105.543306 PubMed PMID: 16129795; PubMed Central PMCID: PMC1820744.
22. Maltsev VA, Sabbah HN, Undrovinas AI. Late sodium current is a novel target for amiodarone: studies in failing human myocardium. J Mol Cell Cardiol. 2001; 33(5):923-32. doi: 10.1006/jmcc.2001.1355 PubMed PMID: 11343415.
23. Undrovinas AI, Maltsev VA, Kyle JW, Silverman N, Sabbah HN. Gating of the late Na+ channel in normal and failing human myocardium. J Mol Cell Cardiol. 2002; 34(11):1477-89. PubMed PMID: 12431447.
24. Valdivia CR, Chu WW, Pu J, Foell JD, Haworth RA, Wolff MR, et al. Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. J Mol Cell Cardiol. 2005; 38 (3):475-83. doi: 10.1016/j.yjmcc.2004.12.012 PubMed PMID: 15733907.
25. Bers DM, Pogwizd SM, Schlotthauer K. Upregulated Na/Ca exchange is involved in both contractile dysfunction and arrhythmogenesis in heart failure. Basic Res Cardiol. 2002; 97 Suppl 1:I36-42. Epub 2002/12/14. PubMed PMID: 12479232.
26. Pogwizd SM, Schlotthauer K, Li L, Yuan W, Bers DM. Arrhythmogenesis and contractile dysfunction in heart failure: Roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circ Res. 2001; 88(11):1159-67. PubMed PMID: 11397782.
27. Reinecke H, Studer R, Vetter R, Holtz J, Drexler H. Cardiac Na+/Ca2+ exchange activity in patients with end-stage heart failure. Cardiovasc Res. 1996; 31(1):48-54. PubMed PMID: 8849588.
28. Studer R, Reinecke H, Bilger J, Eschenhagen T, Bohm M, Hasenfuss G, et al. Gene expression of the cardiac Na(+)-Ca2+ exchanger in end-stage human heart failure. Circ Res. 1994; 75(3):443-53. PubMed PMID: 8062418.
29. Sanguinetti MC, Jurkiewicz NK. Two components of cardiac delayed rectifier K+ current. Differential sensitivity to block by class III antiarrhythmic agents. J Gen Physiol. 1990; 96(1):195-215. PubMed PMID: 2170562; PubMed Central PMCID: PMC2228985.
30. Viswanathan PC, Shaw RM, Rudy Y. Effects of IKr and IKs heterogeneity on action potential duration and its rate dependence: a simulation study. Circulation. 1999; 99(18):2466-74. Epub 1999/05/11. PubMed PMID: 10318671.
31. Zeng J, Laurita KR, Rosenbaum DS, Rudy Y. Two components of the delayed rectifier K+ current in ventricular myocytes of the guinea pig type. Theoretical formulation and their role in repolarization. Circ Res. 1995; 77(1):140-52. Epub 1995/07/01. PubMed PMID: 7788872.
32. Decker KF, Heijman J, Silva JR, Hund TJ, Rudy Y. Properties and ionic mechanisms of action potential adaptation, restitution, and accommodation in canine epicardium. Am J Physiol Heart Circ Physiol. 2009; 296(4):H1017-26. doi: 10.1152/ajpheart.01216.2008 PubMed PMID: 19168720; PubMed Central PMCID: PMC2670702.
33. Karma A. Electrical alternans and spiral wave breakup in cardiac tissue. Chaos. 1994; 4(3):461-72. PubMed PMID: 12780121.
34. Weiss JN, Karma A, Shiferaw Y, Chen PS, Garfinkel A, Qu Z. From pulsus to pulseless: the saga of cardiac alternans. Circ Res. 2006; 98(10):1244-53. Epub 2006/05/27. 98/10/1244 [pii] doi: 10.1161/01.RES.0000224540.97431.f0 PubMed PMID: 16728670.
35. Weiss JN, Qu Z, Chen PS, Lin SF, Karagueuzian HS, Hayashi H, et al. The dynamics of cardiac fibrillation. Circulation. 2005; 112(8):1232-40. Epub 2005/08/24. 112/8/1232 [pii] doi: 10.1161/CIRCULATIONAHA.104.529545 PubMed PMID: 16116073.
36. Gilmour RF Jr, Chialvo DR. Electrical restitution, critical mass, and the riddle of fibrillation. J Cardiovasc Electrophysiol. 1999; 10(8):1087-9. PubMed PMID: 10466489.
37. Islam MA. Pharmacological modulations of cardiac ultra-rapid and slowly activating delayed rectifier currents: potential antiarrhythmic approaches. Recent patents on cardiovascular drug discovery. 2010; 5(1):33-46. PubMed PMID: 19929823.
38. Varro A, Biliczki P, Iost N, Virag L, Hala O, Kovacs P, et al. Theoretical possibilities for the development of novel antiarrhythmic drugs. Curr Med Chem. 2004; 11(1):1-11. PubMed PMID: 14754422.
39. Munoz V, Grzeda KR, Desplantez T, Pandit SV, Mironov S, Taffet SM, et al. Adenoviral expression of IKs contributes to wavebreak and fibrillatory conduction in neonatal rat ventricular cardiomyocyte monolayers. Circ Res. 2007; 101(5):475-83. Epub 2007/07/14. CIRCRESAHA.107.149617 [pii] doi: 10.1161/CIRCRESAHA.107.149617 PubMed PMID: 17626898.
40. Tohse N. Calcium-sensitive delayed rectifier potassium current in guinea pig ventricular cells. Am J Physiol. 1990; 258(4 Pt 2):H1200-7. PubMed PMID: 2331008.
41. Shinbane JS, Wood MA, Jensen DN, Ellenbogen KA, Fitzpatrick AP, Scheinman MM. Tachycardia-induced cardiomyopathy: a review of animal models and clinical studies. J Am Coll Cardiol. 1997; 29 (4):709-15. Epub 1997/03/15. S073510979600592X [pii]. PubMed PMID: 9091514.
42. Brunner M, Peng X, Liu GX, Ren XQ, Ziv O, Choi BR, et al. Mechanisms of cardiac arrhythmias and sudden death in transgenic rabbits with long QT syndrome. J Clin Invest. 2008; 118(6):2246-59. PubMed PMID: 18464931. doi: 10.1172/JCI33578
43. Tsuji Y, Zicha S, Qi XY, Kodama I, Nattel S. Potassium channel subunit remodeling in rabbits exposed to long-term bradycardia or tachycardia: discrete arrhythmogenic consequences related to differential delayed-rectifier changes. Circulation. 2006; 113(3):345-55. doi: 10.1161/CIRCULATIONAHA.105.552968 PubMed PMID: 16432066.
44. Odening KE, Hyder O, Chaves L, Schofield L, Brunner M, Kirk M, et al. Pharmacogenomics of anesthetic drugs in transgenic LQT1 and LQT2 rabbits reveal genotype-specific differential effects on cardiac repolarization. Am J Physiol Heart Circ Physiol. 2008; 295(6):H2264-72. Epub 2008/10/07. 00680.2008 [pii] doi: 10.1152/ajpheart.00680.2008 PubMed PMID: 18835916; PubMed Central PMCID: PMC2614544.
45. Choi B-R, Salama G. Simultaneous optical maps of early afterdepolarizations (EADs) and intracellular Ca2+ (Cai) in drug-induced long QT syndrome (LQTS). Circulation. 1999; 100:I51.
46. Salama G, Choi BR, Azour G, Lavasani M, Tumbev V, Salzberg BM, et al. Properties of new, long-wavelength, voltage-sensitive dyes in the heart. J Membr Biol. 2005; 208(2):125-40. Epub 2006/04/29. doi: 10.1007/s00232-005-0826-8 PubMed PMID: 16645742; PubMed Central PMCID: PMC3018276.
47. Hayashi H, Kamanu SD, Ono N, Kawase A, Chou CC, Weiss JN, et al. Calcium transient dynamics and the mechanisms of ventricular vulnerability to single premature electrical stimulation in Langendorff-perfused rabbit ventricles. Heart Rhythm. 2008; 5(1):116-23. Epub 2008/01/09. S1547-5271(07) 00877-6 [pii] doi: 10.1016/j.hrthm.2007.08.020 PubMed PMID: 18180025; PubMed Central PMCID: PMC2756777.
48. Choi BR, Jang W, Salama G. Spatially discordant voltage alternans cause wavebreaks in ventricular fibrillation. Heart Rhythm. 2007; 4(8):1057-68. PubMed PMID: 17675081.
49. Choi BR, Salama G. Simultaneous maps of optical action potentials and calcium transients in guinea-pig hearts: mechanisms underlying concordant alternans. J Physiol. 2000; 529(Pt 1):171-88.
50. Ziv O, Morales E, Song YK, Peng X, Odening KE, Buxton AE, et al. Origin of complex behaviour of spatially discordant alternans in a transgenic rabbit model of type 2 long QT syndrome. J Physiol. 2009; 587(Pt 19):4661-80. Epub 2009/08/14. jphysiol.2009.175018 [pii] doi: 10.1113/jphysiol.2009.175018 PubMed PMID: 19675070; PubMed Central PMCID: PMC2768020.
51. Kim TY, Woo SJ, Hwang SM, Hong JH, Lee KJ. Cardiac beat-to-beat alternations driven by unusual spiral waves. Proc Natl Acad Sci U S A. 2007; 104(28):11639-42. Epub 2007/07/04. doi: 10.1073/pnas.0704204104 PubMed PMID: 17606916; PubMed Central PMCID: PMC1913880.
52. Restrepo JG, Weiss JN, Karma A. Calsequestrin-mediated mechanism for cellular calcium transient alternans. Biophys J. 2008; 95(8):3767-89. PubMed PMID: 18676655. doi: 10.1529/biophysj.108.130419
53. Mahajan A, Shiferaw Y, Sato D, Baher A, Olcese R, Xie L-H, et al. A rabbit ventricular action potential model replicating cardiac dynamics at rapid heart rates. Biophys J. 2008; 94(2):392-410. doi: 10.1529/biophysj.106.98160 PMID: 18160660
54. Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM. Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res. 2005; 97(12):1314-22. doi: 10.1161/01.RES.0000194329.41863.89 PubMed PMID: 16269653.
55. Shannon TR, Wang F, Bers DM. Regulation of cardiac sarcoplasmic reticulum Ca release by luminal [Ca] and altered gating assessed with a mathematical model. Biophys J. 2005; 89(6):4096-110. doi: 10.1529/biophysj.105.068734 PubMed PMID: 16169970; PubMed Central PMCID: PMC1366975.
56. Lammers WJ, Allessie M, Rensma PL, Schalij MJ. The use of fibrillation cycle length to determine spatial dispersion in electrophysiological properties and to characterise the underlying mechanism of fibirllation. New Trends in Arrhythmias. 1986; II.
57. Hayashi H, Shiferaw Y, Sato D, Nihei M, Lin SF, Chen PS, et al. Dynamic origin of spatially discordant alternans in cardiac tissue. Biophys J. 2007; 92(2):448-60. Epub 2006/10/31. S0006-3495(07)70845-7 [pii] doi: 10.1529/biophysj.106.091009 PubMed PMID: 17071663; PubMed Central PMCID: PMC1751420.
58. Qu Z, Nivala M, Weiss JN. Calcium alternans in cardiac myocytes: Order from disorder. J Mol Cell Cardiol. 2013; 58(0):100-9. http://dx.doi.org/10.1016/j.yjmcc.2012.10.007. doi: 10.1016/j.yjmcc.2012.10.007 PMID: 23104004
59. Benoist D, Stones R, Drinkhill MJ, Benson AP, Yang Z, Cassan C, et al. Cardiac arrhythmia mechanisms in rats with heart failure induced by pulmonary hypertension. Am J Physiol Heart Circ Physiol. 2012; 302(11):H2381-95. doi: 10.1152/ajpheart.01084.2011 PubMed PMID: 22427523; PubMed Central PMCID: PMC3378302.
60. Lou Q, Janks DL, Holzem KM, Lang D, Onal B, Ambrosi CM, et al. Right ventricular arrhythmogenesis in failing human heart: the role of conduction and repolarization remodeling. Am J Physiol Heart Circ Physiol. 2012; 303(12):H1426-34. doi: 10.1152/ajpheart.00457.2012 PubMed PMID: 23042951; PubMed Central PMCID: PMC4116390.
61. Watanabe T, Yamaki M, Yamauchi S, Minamihaba O, Miyashita T, Kubota I, et al. Regional prolongation of ARI and altered restitution properties cause ventricular arrhythmia in heart failure. Am J Physiol Heart Circ Physiol. 2002; 282(1):H212-8. PubMed PMID: 11748065.
62. Tomaselli GF, Zipes DP. What causes sudden death in heart failure? Circ Res. 2004; 95(8):754-63. Epub 2004/10/16. 95/8/754 [pii] doi: 10.1161/01.RES.0000145047.14691.db PubMed PMID: 15486322.
63. Hoeker GS, Katra RP, Wilson LD, Plummer BN, Laurita KR. Spontaneous calcium release in tissue from the failing canine heart. Am J Physiol Heart Circ Physiol. 2009; 297(4):H1235-42. Epub 2009/08/04. 01320.2008 [pii] doi: 10.1152/ajpheart.01320.2008 PubMed PMID: 19648256; PubMed Central PMCID: PMC2770773.
64. Wilson LD, Jeyaraj D, Wan X, Hoeker GS, Said TH, Gittinger M, et al. Heart failure enhances susceptibility to arrhythmogenic cardiac alternans. Heart Rhythm. 2009; 6(2):251-9. Epub 2009/02/04. S1547-5271(08)01091-6 [pii] doi: 10.1016/j.hrthm.2008.11.008 PubMed PMID: 19187920; PubMed Central PMCID: PMC2764250.
65. Jeong EM, Liu M, Sturdy M, Gao G, Varghese ST, Sovari AA, et al. Metabolic stress, reactive oxygen species, and arrhythmia. J Mol Cell Cardiol. 2012; 52(2):454-63. Epub 2011/10/08. S0022-2828(11)00420-2 [pii] doi: 10.1016/j.yjmcc.2011.09.018 PubMed PMID: 21978629; PubMed Central PMCID: PMC3264827.