Arrhythmia mechanisms in the failing heart

PACE - Pacing and Clinical Electrophysiology

Volumn 31, Issue 8, 2008, Pages 1048-1056

  Jin, Hongwei ^b   Lyon, Alexander R ^b   Akar, Fadi G ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

Arrhythmias; Conduction; Gap junctions; Heart failure; Repolarization

Indexed keywords

ION CHANNEL;

ACTION POTENTIAL; CARDIOMYOPATHY; EXCITATION CONTRACTION COUPLING; GAP JUNCTION; HEART ARRHYTHMIA; HEART CONDUCTION; HEART ELECTROPHYSIOLOGY; HEART FAILURE; HEART MUSCLE CONDUCTION DISTURBANCE; HEART REPOLARIZATION; HUMAN; NONHUMAN; REVIEW;

ARRHYTHMIAS, CARDIAC; HEART CONDUCTION SYSTEM; HEART FAILURE; HUMANS; MODELS, CARDIOVASCULAR;

EID: 48249126816     PISSN: 01478389     EISSN: 15408159     Source Type: Journal    
DOI: 10.1111/j.1540-8159.2008.01134.x     Document Type: Review

References (76)

1. Kaab S, Nuss HB, Chiamvimonvat N, O'Rourke B, Pak PH, Kass DA, Marban E, et al. Ionic mechanism of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circ Res 1996 78 : 262 273.
2. O'Rourke B, Kass DA, Tomaselli GF, Kaab S, Tunin R, Marban E. Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, I: Experimental studies. Circ Res 1999 84 : 562 570.
3. Rosenbaum DS, Jackson LE, Smith JM, Garan H, Ruskin JN, Cohen RJ. Electrical alternans and vulnerability to ventricular arrhythmias. N Engl J Med 1994 330 : 235 241.
4. Berger RD, Kasper EK, Baughman KL, Marban E, Calkins H, Tomaselli GF. Beat-to-beat QT interval variability: Novel evidence for repolarization lability in ischemic and nonischemic dilated cardiomyopathy. Circulation 1997 96 : 1557 1565.
5. Atiga WL, Calkins H, Lawrence JH, Tomaselli GF, Smith JM, Berger RD. Beat-to-beat repolarization lability identifies patients at risk for sudden cardiac death. J Cardiovasc Electrophysiol 1998 9 : 899 908.
6. Pham Q, Quan KJ, Rosenbaum DS. T-wave alternans: Marker, mechanism, and methodology for predicting sudden cardiac death. J Electrocardiol 2003 36 (Suppl 75 81.
7. Antzelevitch C. Role of spatial dispersion of repolarization in inherited and acquired sudden cardiac death syndromes. Am J Physiol 2007 293 : H2024 H2038.
8. Antzelevitch C, Shimizu W, Yan GX, Sicouri S, Weissenburger J, Nesterenko VV, Burashnikov A, et al. The M cell: Its contribution to the ECG and to normal and abnormal electrical function of the heart. J Cardiovasc Electrophysiol 1999 10 : 1124 1152.
9. Akar FG, Rosenbaum DS. Transmural electrophysiological heterogeneities underlying arrhythmogenesis in heart failure. Circ Res 2003 93 : 638 645.
10. Yan GX, Rials SJ, Wu Y, Liu T, Xu X, Marinchak RA, Kowey PR. Ventricular hypertrophy amplifies transmural repolarization dispersion and induces early afterdepolarization. Am J Physiol 2001 281 : H1968 H1975.
11. Poelzing S, Rosenbaum DS. Altered connexin43 expression produces arrhythmia substrate in heart failure. Am J Physiol 2004 287 : H1762 H1770.
12. Stevenson WG, Sweeney MO. Arrhythmias and sudden death in heart failure. Jpn Circ J 1997 61 : 727 740.
13. Tomaselli GF, Zipes DP. What causes sudden death in heart failure? Circ Res 2004 95 : 754 763.
14. Hall DG, Morley GE, Vaidya D, Ard M, Kimball TR, Witt SA, Colbert MC. Early onset heart failure in transgenic mice with dilated cardiomyopathy. Pediatr Res 2000 48 : 36 42.
15. Laurita KR, Chuck ET, Yang T, Dong WQ, Kuryshev YA, Brittenham GM, Rosenbaum DS, et al. Optical mapping reveals conduction slowing and impulse block in iron-overload cardiomyopathy. J Lab Clin Med 2003 142 : 83 89.
16. Akar FG, Spragg DD, Tunin RS, Kass DA, Tomaselli GF. Mechanisms underlying conduction slowing and arrhythmogenesis in nonischemic dilated cardiomyopathy. Circ Res 2004 95 : 717 725.
17. Akar FG, Nass RD, Hahn S, Cingolani E, Shah M, Hesketh GG, DiSilvestre D, et al. Dynamic changes in conduction velocity and gap junction properties during development of pacing-induced heart failure. Am J Physiol Heart Circ Physiol 2007 293 : H1223 H1230.
18. Cabo C, Yao J, Boyden PA, Chen S, Hussain W, Duffy HS, Ciaccio EJ, et al. Heterogeneous gap junction remodeling in reentrant circuits in the epicardial border zone of the healing canine infarct. Cardiovasc Res 2006 72 : 241 249.
19. Yao JA, Hussain W, Patel P, Peters NS, Boyden PA, Wit AL. Remodeling of gap junctional channel function in epicardial border zone of healing canine infarcts. Circ Res 2003 92 : 437 443.
20. Peters NS, Coromilas J, Severs NJ, Wit AL. Disturbed connexin43 gap junction distribution correlates with the location of reentrant circuits in the epicardial border zone of healing canine infarcts that cause ventricular tachycardia. Circulation 1997 95 : 988 996.
21. Pu J, Boyden PA. Alterations of Na+ currents in myocytes from epicardial border zone of the infarcted heart. A possible ionic mechanism for reduced excitability and postrepolarization refractoriness. Circ Res 1997 81 : 110 119.
22. Shaw RM, Rudy Y. Electrophysiologic effects of acute myocardial ischemia. A mechanistic investigation of action potential conduction and conduction failure. Circ Res 1997 80 : 124 138.
23. Kucera JP, Kleber AG, Rohr S. Slow conduction in cardiac tissue: Insights from optical mapping at the cellular level. J Electrocardiol 2001 34 (Suppl 57 64.
24. Shah MHHG, Guo Y, Akar FG, Kass DA, Tomaselli GF, Van Eyk JE. Membrane localization and novel phosphorylation of Connexin43 in heart failure. Circulation 2006 114 : 202 202.
25. Brooksby P, Levi AJ, Jones JV. The electrophysiological characteristics of hypertrophied ventricular myocytes from the spontaneously hypertensive rat. J Hypertens 1993 11 : 611 622.
26. Cerbai E, Barbieri M, Li Q, Mugelli A. Ionic basis of action potential prolongation of hypertrophied cardiac myocytes isolated from hypertensive rats of different ages. Cardiovasc Res 1994 28 : 1180 1187.
27. Richard S, Leclercq F, Lemaire S, Piot C, Nargeot J. Ca2+ currents in compensated hypertrophy and heart failure. Cardiovasc Res 1998 37 : 300 311.
28. Hill JA. Electrical remodeling in cardiac hypertrophy. Trends Cardiovasc Med 2003 13 : 316 322.
29. Ouadid H, Albat B, Nargeot J. Calcium currents in diseased human cardiac cells. J Cardiovasc Pharmacol 1995 25 : 282 291.
30. Ryder KO, Bryant SM, Hart G. Membrane current changes in left ventricular myocytes isolated from guinea pigs after abdominal aortic coarctation. Cardiovasc Res 1993 27 : 1278 1287.
31. Schroder F, Handrock R, Beuckelmann DJ, Hirt S, Hullin R, Priebe L, Schwinger RH, et al. Increased availability and open probability of single L-type calcium channels from failing compared with nonfailing human ventricle. Circulation 1998 98 : 969 976.
32. Sipido KR, Stankovicova T, Vanhaecke J, Flameng W, Verdonck F. A critical role for L-type Ca2+ current in the regulation of Ca2+ release from the sarcoplasmic reticulum in human ventricular myocytes from dilated cardiomyopathy. Ann NY Acad Sci 1998 853 : 353 356.
33. Cingolani E, Ramirez Correa GA, Kizana E, Murata M, Cheol Cho H, Marbán E. Gene therapy to inhibit the calcium channel {beta} subunit. Physiological consequences and pathophysiological effects in models of cardiac hypertrophy. Circ Res 2007 10 : 166 175.
34. Samie FH, Mandapati R, Gray RA, Watanabe Y, Zuur C, Beaumont J, Jalife J. A mechanism of transition from ventricular fibrillation to tachycardia: Effect of calcium channel blockade on the dynamics of rotating waves. Circ Res 2000 86 : 684 691.
35. Catterall WA. Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 2000 16 : 521 555.
36. Clozel JP, Ertel EA, Ertel SI. Voltage-gated T-type Ca2+ channels and heart failure. Proc Assoc Am Physicians 1999 111 : 429 437.
37. Nuss HB, Houser SR. T-type Ca2+ current is expressed in hypertrophied adult feline left ventricular myocytes. Circ Res 1993 73 : 777 782.
38. Wang HS, Cohen IS. Calcium channel heterogeneity in canine left ventricular myocytes. J Physiol 2003 547 (Pt 3 825 833.
39. Winslow RL, Rice J, Jafri S, Marban E, O'Rourke B. Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, II: Model studies. Circ Res 1999 84 : 571 586.
40. Ohizumi Y, Sasaki S, Shibusawa K, Ishikawa K, Ikemoto F. Stimulation of sarcoplasmic reticulum Ca(2+)-ATPase by gingerol analogues. Biol Pharm Bull 1996 19 : 1377 1379.
41. del Monte F, Hajjar RJ, Harding SE. Overwhelming evidence of the beneficial effects of SERCA gene transfer in heart failure. Circ Res 2001 88 : E66 67.
42. Sakata S, Liang L, Sakata N, Sakata Y, Chemaly ER, Lebeche D, Takewa Y, et al. Preservation of mechanical and energetic function after adenoviral gene transfer in normal rat hearts. Clin Exp Pharmacol Physiol 2007 34 : 1300 1306.
43. Sakata S, Lebeche D, Sakata N, Sakata Y, Chemaly ER, Liang LF, Tsuji T, et al. Restoration of mechanical and energetic function in failing aortic-banded rat hearts by gene transfer of calcium cycling proteins. J Mol Cell Cardiol 2007 42 : 852 861.
44. Laurita KR, Katra R, Wible B, Wan X, Koo MH. Transmural heterogeneity of calcium handling in canine. Circ Res 2003 92 : 668 675.
45. Cerrone M, Noujaim SF, Tolkacheva EG, Talkachou A, O'Connell R, Berenfeld O, Anumonwo J, et al. Arrhythmogenic mechanisms in a mouse model of catecholaminergic polymorphic ventricular tachycardia. Circ Res 2007 101 : 1039 1048.
46. Levine BA, Patchell VB, Sharma P, Gao Y, Bigelow DJ, Yao Q, Goh S, et al. Sites on the cytoplasmic region of phospholamban involved in interaction with the calcium-activated ATPase of the sarcoplasmic reticulum. Eur J Biochem 1999 264 : 905 913.
47. Hasenfuss G, Meyer M, Schillinger W, Preuss M, Pieske B, Just H. Calcium handling proteins in the failing human heart. Basic Res Cardiol 1997 92 (Suppl 1 87 93.
48. Kaprielian RDMF, Hajjar RJ. Targeting Ca2+ cycling proteins and the action potential in heart failure by gene transfer. Basic Res Cardiol 2002 97 (Suppl 1 I136 I145.
49. Janczewski AM, Zahid M, Lemster BH, Frye CS, Gibson G, Higuchi Y, Kranias EG, et al. Phospholamban gene ablation improves calcium transients but not cardiac function in a heart failure model. Cardiovasc Res 2004 62 : 468 480.
50. McKenna E, Smith JS, Coll KE, Mazack EK, Mayer EJ, Antanavage J, Wiedmann RT, et al. Dissociation of phospholamban regulation of cardiac sarcoplasmic reticulum Ca2+ATPase by quercetin. J Biol Chem 1996 271 : 24517 24525.
51. 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 I42.
52. Mattiello JA, Margulies KB, Jeevanandam V, Houser SR. Contribution of reverse-mode sodium-calcium exchange to contractions in failing human left ventricular myocytes. Cardiovasc Res 1998 37 : 424 431.
53. Houser SR, Piacentino V, III., Mattiello J, Weisser J, Gaughan JP. Functional properties of failing human ventricular myocytes. Trends Cardiovasc Med 2000 10 : 101 107.
54. Sipido KR, Volders PG, Vos MA, Verdonck F. Altered Na/Ca exchange activity in cardiac hypertrophy and heart failure: A new target for therapy? Cardiovasc Res 2002 53 : 782 805.
55. Arai M, Alpert NR, MacLennan DH, Barton P, Periasamy M. Alterations in sarcoplasmic reticulum gene expression in human heart failure. A possible mechanism for alterations in systolic and diastolic properties of the failing myocardium. Circ Res 1993 72 : 463 469.
56. Hobai IA, Maack C, O'Rourke B. Partial inhibition of sodium/calcium exchange restores cellular calcium handling in canine heart failure. Circ Res 2004 95 : 292 299.
57. Meyer M, Schillinger W, Pieske B, Holubarsch C, Heilmann C, Posival H, Kuwajima G, et al. Alterations of sarcoplasmic reticulum proteins in failing human dilated cardiomyopathy. Circulation 1995 92 : 778 784.
58. Heerdt PM, Holmes JW, Cai B, Barbone A, Madigan JD, Reiken S, Lee DL, et al. Chronic unloading by left ventricular assist device reverses contractile dysfunction and alters gene expression in end-stage heart failure. Circulation 2000 102 : 2713 2719.
59. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): Defective regulation in failing hearts. Cell 2000 101 : 365 376.
60. Curran J, Hinton MJ, Rios E, Bers DM, Shannon TR. Beta-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ Res 2007 100 : 391 398.
61. Marks AR. Novel therapy for heart failure and exercise-induced ventricular tachycardia based on 'fixing' the leak in ryanodine receptors. Novartis Found Symp 2006 274 : 132 147 discussion 147-155, 272-136.
62. Benkusky NA, Weber CS, Scherman JA, Farrell EF, Hacker TA, John MC, Powers PA, et al. Intact {beta}-adrenergic response and unmodified progression toward heart failure in mice with genetic ablation of a major protein kinase A phosphorylation site in the cardiac ryanodine receptor. Circ Res 2007 101 : 819 829.
63. Xiao B, Zhong G, Obayashi M, Yang D, Chen K, Walsh MP, Shimoni Y, et al. Ser-2030, but not Ser-2808, is the major phosphorylation site in cardiac ryanodine receptors responding to protein kinase A activation upon beta-adrenergic stimulation in normal and failing hearts. Biochem J. 2006 396 : 7 16.
64. Xiao B, Sutherland C, Walsh MP, Chen SR. Protein kinase A phosphorylation at serine-2808 of the cardiac Ca2+-release channel (ryanodine receptor) does not dissociate 12.6-kDa FK506-binding protein (FKBP12.6). Circ Res 2004 94 : 487 495.
65. Xiao B, Jiang MT, Zhao M, Yang D, Sutherland C, Lai FA, Walsh MP, et al. Characterization of a novel PKA phosphorylation site, serine-2030, reveals no PKA hyperphosphorylation of the cardiac ryanodine receptor in canine heart failure. Circ Res 2005 96 : 847 855.
66. 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 : 1314 1322.
67. Guo T, Zhang T, Mestril R, Bers DM. Ca2+/Calmodulin-dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes. Circ Res 2006 99 : 398 406.
68. Liu N, Colombi B, Memmi M, Zissimopoulos S, Rizzi N, Negri S, Imbriani M, et al. Arrhythmogenesis in catecholaminergic polymorphic ventricular tachycardia: insights from a RyR2 R4496C knock-in mouse model. Circ Res 2006 99 : 292 298.
69. Lehnart SE, Terrenoire C, Reiken S, Wehrens XH, Song LS, Tillman EJ, Mancarella S, et al. Stabilization of cardiac ryanodine receptor prevents intracellular calcium leak and arrhythmias. Proc Nat Acad Sci o USA 2006 103 : 7906 7910.
70. Akar FG. The perfect storm: Defective calcium cycling in insulated fibers with reduced repolarization reserve. Circ Res 2007 101 : 968 970.
71. Nam GB, Burashnikov A, Antzelevitch C. Cellular mechanisms underlying the development of catecholaminergic ventricular tachycardia. Circulation 2005 111 : 2727 2733.
72. Kirchhefer U, Schmitz W, Scholz H, Neumann J. Activity of cAMP-dependent protein Kinase and Ca2+/Calmodulin-dependent protein kinase in failing and nonfailing human hearts. Cardiovasc Res 1999 42 : 254 261.
73. Maier LS, Bers DM. Calcium, calmodulin, and calcium-calmodulin kinase II: Heartbeat to heartbeat and beyond. J Mol Cell Cardiol 2002 34 : 919 939.
74. Lokuta AJ, Rogers TB, Lederer WJ, Valdivia HH. Modulation of cardiac ryanodine receptors of swine and rabbit by a phosphorylation-dephosphorylation mechanism. J Physiol 1995 487 (Pt 3 609 622.
75. Kohlhaas M, Zhang T, Seidler T, Zibrova D, Dybkova N, Steen A, Wagner S, et al. Increased sarcoplasmic reticulum calcium leak but unaltered contractility by acute CaMKII overexpression in isolated rabbit cardiac myocytes. Circ Res 2006 98 : 235 244.
76. Anderson ME. Multiple downstream proarrhythmic targets for calmodulin kinase II: Moving beyond an ion channel-centric focus. Cardiovasc Res 2007 73 : 657 666.