Electrical remodeling in dyssynchrony and resynchronization

Journal of Cardiovascular Translational Research

Volumn 5, Issue 2, 2012, Pages 170-179

  Aiba, Takeshi ^a   Tomaselli, Gordon ^b  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac resynchronization therapy; Dyssynchrony; Electrophysiology; Heart failure; Ion channels

Indexed keywords

BETA ADRENERGIC RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; POTASSIUM ION; RYANODINE RECEPTOR; SODIUM ION;

ADRENERGIC ACTIVITY; ARTICLE; CALCIUM CURRENT; CALCIUM HOMEOSTASIS; CARDIAC RESYNCHRONIZATION THERAPY; CHANNEL GATING; DEFIBRILLATION; DOWN REGULATION; DYSSYNCHRONOUS HEART FAILURE; ENZYME ACTIVITY; ENZYME INHIBITION; EXCITATION CONTRACTION COUPLING; HEART ARRHYTHMIA; HEART CONDUCTION; HEART DEPOLARIZATION; HEART ELECTROPHYSIOLOGY; HEART FAILURE; HEART LEFT VENTRICLE CONTRACTION; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE POTENTIAL; HEART PERFORMANCE; HEART VENTRICLE ARRHYTHMIA; HEART VENTRICLE REMODELING; HUMAN; MORTALITY; MUSCLE CELL; NONHUMAN; OUTCOME ASSESSMENT; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QT PROLONGATION; SIGNAL TRANSDUCTION; SODIUM CURRENT; THERAPY EFFECT;

ACTION POTENTIALS; ANIMALS; BUNDLE-BRANCH BLOCK; CARDIAC RESYNCHRONIZATION THERAPY; EXCITATION CONTRACTION COUPLING; HEART FAILURE; HUMANS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

ANIMALIA;

EID: 84866085303     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-012-9348-9     Document Type: Article

References (77)

1. American Heart Association. (2002). Heart disease and stroke statistics -2003 update. Dallas, Texas.
2. Tsuchihashi-Makaya, M., Hamaguchi, S., Kinugawa, S., et al. (2009). Characteristics and outcomes of hospitalized patients with heart failure and reduced vs preserved ejection fraction. Report from the Japanese Cardiac Registry of Heart Failure in Cardiology (JCARE-CARD). Circulation Journal, 73(10), 1893-1900.
3. Cleland, J. G., Daubert, J. C., Erdmann, E., et al. (2005). The effect of cardiac resynchronization onmorbidity and mortality in heart failure. The New England Journal of Medicine, 352(15), 1539-1549. (Pubitemid 40517094)
4. Medina-Ravell, V. A., Lankipalli, R. S., Yan, G. X., et al. (2003). Effect of epicardial or biventricular pacing to prolong QT interval and increase transmural dispersion of repolarization: Does resynchronization therapy pose a risk for patients predisposed to long QT or torsade de pointes? Circulation, 107(5), 740-746. (Pubitemid 36222603)
5. Harada, M., Osaka, T., Yokoyama, E., et al. (2006). Biventricular pacing has an advantage over left ventricular epicardial pacing alone to minimize proarrhythmic perturbation of repolarization. Journal of Cardiovascular Electrophysiology, 17(2), 151-156. (Pubitemid 43344865)
6. Fish, J. M., Di Diego, J. M., Nesterenko, V., et al. (2004). Epicardial activation of left ventricular wall prolongsQT interval and transmural dispersion of repolarization: Implications for biventricular pacing. Circulation, 109(17), 2136-2142. (Pubitemid 38620224)
7. Chalil, S., Yousef, Z. R., Muyhaldeen, S. A., et al. (2006). Pacinginduced increase in QT dispersion predicts sudden cardiac death following cardiac resynchronization therapy. Journal of the American College of Cardiology, 47(12), 2486-2492. (Pubitemid 43866366)
8. Young, J. B., Abraham,W. T., Smith, A. L., et al. (2003). Combined cardiac resynchronization and implantable cardioversion defibrillation in advanced chronic heart failure: The MIRACLE ICD Trial. Journal of the American Medical Association, 289(20), 2685-2694. (Pubitemid 37430139)
9. McSwain, R. L., Schwartz, R. A., DeLurgio, D. B., et al. (2005). The impact of cardiac resynchronization therapy on ventricular tachycardia/ fibrillation: An analysis from the combined Contak-CD and InSync-ICD studies. Journal of Cardiovascular Electrophysiology, 16(11), 1168-1171.
10. Bristow, M. R., Saxon, L. A., Boehmer, J., et al. (2004). Cardiacresynchronization therapy with or without an implantable defibrillator in advanced chronic heart failure. The New England Journal of Medicine, 350(21), 2140-2150.
11. Arya, A., Haghjoo, M., Dehghani, M. R., et al. (2005). Effect of cardiac resynchronization therapy on the incidence of ventricular arrhythmias in patients with an implantable cardioverter-defibrillator. Heart Rhythm, 2(10), 1094-1098. (Pubitemid 41472158)
12. Moss, A. J., Hall, W. J., Cannom, D. S., et al. (2009). Cardiacresynchronization therapy for the prevention of heart-failure events. The New England Journal of Medicine, 361(14), 1329-1338.
13. Yu, C. M., Chan, J. Y., Zhang, Q., et al. (2009). Biventricular pacing in patients with bradycardia and normal ejection fraction. The New England Journal of Medicine, 361(22), 2123-2134.
14. Bai, R., Di Biase, L., Elayi, C., et al. (2008). Mortality of heart failure patients after cardiac resynchronization therapy: Identification of predictors. Journal of Cardiovascular Electrophysiology, 19(12), 1259-1265.
15. Higgins, S. L., Yong, P., Sheck, D., et al. (2000). Biventricular pacing diminishes the need for implantable cardioverter defibrillator therapy. Ventak CHF Investigators. J Am Coll Cardiol. Sep, 36(3), 824-827.
16. Di Biase, L., Gasparini, M., Lunati, M., et al. (2008). Antiarrhythmic effect of reverse ventricular remodeling induced by cardiac resynchronization therapy: The InSync ICD (Implantable Cardioverter-Defibrillator) Italian Registry. Journal of the American College of Cardiology, 52(18), 1442-1449.
17. Markowitz, S. M., Lewen, J. M., Wiggenhorn, C. J., et al. (2009). Relationship of reverse anatomical remodeling and ventricular arrhythmias after cardiac resynchronization. Journal of Cardiovascular Electrophysiology, 20(3), 293-298.
18. Kies, P., Bax, J. J., Molhoek, S. G., et al. (2005). Effect of cardiac resynchronization therapy on inducibility of ventricular tachyarrhythmias in cardiac arrest survivors with either ischemic or idiopathic dilated cardiomyopathy. The American Journal of Cardiology, 95(9), 1111-1114. (Pubitemid 40544323)
19. Cleland, J. G., Daubert, J. C., Erdmann, E., et al. (2006). Longerterm effects of cardiac resynchronization therapy on mortality in heart failure [the CArdiac REsynchronization-Heart Failure (CARE-HF) trial extension phase]. European Heart Journal, 27 (16), 1928-1932. (Pubitemid 44297365)
20. Rose, J., Armoundas, A. A., Tian, Y., et al. (2005). Molecular correlates of altered expression of potassium currents in failing rabbit myocardium. American Journal of Physiology. Heart and Circulatory Physiology, 288(5), H2077-H2087. (Pubitemid 40604090)
21. Beuckelmann, D. J., Nabauer, M., & Erdmann, E. (1993). Alterations of K+ currents in isolated human ventricular myocytes from patients with terminal heart failure. Circulation Research, 73(2), 379-385. (Pubitemid 23212118)
22. Akar, F. G., & Rosenbaum, D. S. (2003). Transmural electrophysiological heterogeneities underlying arrhythmogenesis in heart failure. Circulation Research, 93(7), 638-645. (Pubitemid 37222160)
23. Kaab, S., Nuss, H. B., Chiamvimonvat, N., et al. (1996). Ionic mechanism of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circulation Research, 78(2), 262-273. (Pubitemid 26040856)
24. Kaab, S., Dixon, J., Duc, J., et al. (1998). Molecular basis of transient outward potassium current downregulation in human heart failure: A decrease in Kv4.3 mRNA correlates with a reduction in current density. Circulation, 98(14), 1383-1393. (Pubitemid 28462798)
25. Tsuji, Y., Zicha, S., Qi, X. Y., et al. (2006). Potassium channel subunit remodeling in rabbits exposed to long-term bradycardia or tachycardia: Discrete arrhythmogenic consequences related to differential delayed-rectifier changes. Circulation, 113(3), 345-355. (Pubitemid 43803195)
26. Nattel, S., Maguy, A., Le Bouter, S., et al. (2007). Arrhythmogenic ion-channel remodeling in the heart: Heart failure, myocardial infarction, and atrial fibrillation. Physiological Reviews, 87(2), 425-456. (Pubitemid 47084677)
27. Li, G. R., Lau, C. P., Ducharme, A., et al. (2002). Transmural action potential and ionic current remodeling in ventricles of failing canine hearts. American Journal of Physiology. Heart and Circulatory Physiology, 283(3), H1031-H1041.
28. Aiba, T., Hesketh, G. G., Barth, A. S., et al. (2009). Electrophysiological consequences of dyssynchronous heart failure and its restoration by resynchronization therapy. Circulation, 119(9), 1220-1230.
29. Nabauer, M., Beuckelmann, D. J., & Erdmann, E. (1993). Characteristics of transient outward current in human ventricular myocytes from patients with terminal heart failure. Circulation Research, 73(2), 386-394. (Pubitemid 23212119)
30. Zicha, S., Xiao, L., Stafford, S., et al. (2004). Transmural expression of transient outward potassium current subunits in normal and failing canine and human hearts. The Journal of Physiology, 561 (Pt 3), 735-748. (Pubitemid 40074931)
31. Akar, F. G., Wu, R. C., Juang, G. J., et al. (2005). Molecular mechanisms underlying K+ current downregulation in canine tachycardia-induced heart failure. American Journal of Physiology. Heart and Circulatory Physiology, 288(6), H2887-H2896. (Pubitemid 40720671)
32. Xiao, L., Coutu, P., Villeneuve, L. R., et al. (2008). Mechanisms underlying rate-dependent remodeling of transient outward potassium current in canine ventricular myocytes. Circulation Research, 103, 733-742.
33. Nuss, H. B., Kaab, S., Kass, D. A., et al. (1999). Cellular basis of ventricular arrhythmias and abnormal automaticity in heart failure. American Journal of Physiology, 277(1 Pt 2), H80-H91. (Pubitemid 29354681)
34. Pogwizd, S. M., Schlotthauer, K., Li, L., et al. (2001). Arrhythmogenesis and contractile dysfunction in heart failure: Roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circulation Research, 88(11), 1159-1167. (Pubitemid 34132516)
35. Rozanski, G. J., Xu, Z., Whitney, R. T., et al. (1997). Electrophysiology of rabbit ventricular myocytes following sustained rapid ventricular pacing. Journal of Molecular and Cellular Cardiology, 29(2), 721-732. (Pubitemid 27192878)
36. Zaritsky, J. J., Eckman, D. M., Wellman, G. C., et al. (2000). Targeted disruption of Kir2.1 and Kir2.2 genes reveals the essential role of the inwardly rectifying K(+) current in K(+)-mediated vasodilation. Circulation Research, 87(2), 160-166. (Pubitemid 30616913)
37. McLerie, M., & Lopatin, A. N. (2003). Dominant-negative suppression of I(K1) in the mouse heart leads to altered cardiac excitability. Journal of Molecular and Cellular Cardiology, 35 (4), 367-378. (Pubitemid 36411698)
38. Liu, D. W., & Antzelevitch, C. (1995). Characteristics of the delayed rectifier current (IKr and IKs) in canine ventricular epicardial, midmyocardial, and endocardial myocytes. A weaker IKs contributes to the longer action potential of the M cell. Circ Res. Mar, 76(3), 351-365.
39. Furukawa, T., Bassett, A. L., Furukawa, N., et al. (1993). The ionic mechanism of reperfusion-induced early afterdepolarizations in feline left ventricular hypertrophy. The Journal of Clinical Investigation, 91(4), 1521-1531. (Pubitemid 23127354)
40. Pitt, G. S., Dun, W., & Boyden, P. A. (2006). Remodeled cardiac calcium channels. Journal of Molecular and Cellular Cardiology, 41(3), 373-388. (Pubitemid 44344291)
41. Chen, X., Piacentino, V., 3rd, Furukawa, S., et al. (2002). L-type Ca2+ channel density and regulation are altered in failing human ventricular myocytes and recover after support with mechanical assist devices. Circulation Research, 91(6), 517-524.
42. Schroder, F., Handrock, R., Beuckelmann, D. J., et al. (1998). Increased availability and open probability of single L-type calcium channels from failing compared with nonfailing human ventricle. Circulation, 98(10), 969-976. (Pubitemid 28446649)
43. Takahashi, T., Allen, P. D., Lacro, R. V., et al. (1992). Expression of dihydropyridine receptor (Ca2+ channel) and calsequestrin genes in the myocardium of patients with end-stage heart failure. The Journal of Clinical Investigation, 90(3), 927-935.
44. Yang, Y., Chen, X., Margulies, K., et al. (2000). L-type Ca2+ channel alpha 1c subunit isoform switching in failing human ventricular myocardium. Journal of Molecular and Cellular Cardiology, 32(6), 973-984. (Pubitemid 30663105)
45. Hullin, R., Khan, I. F., Wirtz, S., et al. (2003). Cardiac L-type calcium channel beta-subunits expressed in human heart have differential effects on single channel characteristics. Journal of Biological Chemistry, 278(24), 21623-21630. (Pubitemid 36792562)
46. O'Rourke, B., Kass,D. A., Tomaselli, G. F., et al. (1999).Mechanisms of altered excitation-contraction coupling in canine tachycardiainduced heart failure, I: Experimental studies. Circulation Research, 84(5), 562-570. (Pubitemid 29138593)
47. Hobai, I. A., & O'Rourke, B. (2000). Enhanced Ca(2+)-activated Na(+)-Ca(2+) exchange activity in canine pacing-induced heart failure. Circulation Research, 87(8), 690-698.
48. Hobai, I. A., & O'Rourke, B. (2001). Decreased sarcoplasmic reticulum calcium content is responsible for defective excitationcontraction coupling in canine heart failure. Circulation, 103(11), 1577-1584. (Pubitemid 32226268)
49. Armoundas, A. A., Hobai, I. A., Tomaselli, G. F., et al. (2003). Role of sodium-calcium exchanger in modulating the action potential of ventricular myocytes from normal and failing hearts. Circulation Research, 93(1), 46-53. (Pubitemid 36859040)
50. Reiken, S., Gaburjakova, M., Guatimosim, S., et al. (2003). Protein kinase A phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. Role of phosphatases and response to isoproterenol. Journal of Biological Chemistry, 278(1), 444-453. (Pubitemid 36043595)
51. Marx, S. O., Reiken, S., Hisamatsu, Y., et al. (2000). PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): Defective regulation in failing hearts. Cell, 101(4), 365-376.
52. Curran, J., Hinton, M. J., Rios, E., et al. (2007). Beta-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circulation Research, 100(3), 391-398.
53. Jiang, M. T., Lokuta, A. J., Farrell, E. F., et al. (2002). Abnormal Ca2+ release, but normal ryanodine receptors, in canine and human heart failure. Circulation Research, 91(11), 1015-1022. (Pubitemid 35416638)
54. Xiao, B., Jiang, M. T., Zhao, M., et al. (2005). Characterization of a novel PKA phosphorylation site, serine-2030, reveals no PKA hyperphosphorylation of the cardiac ryanodine receptor in canine heart failure. Circulation Research, 96(8), 847-855. (Pubitemid 40604968)
55. MacDonnell, S. M., Garcia-Rivas, G., Scherman, J. A., et al. (2008). Adrenergic regulation of cardiac contractility does not involve phosphorylation of the cardiac ryanodine receptor at serine 2808. Circulation Research, 102(8), e65-e72. (Pubitemid 351591558)
56. Harzheim, D., Movassagh, M., Foo, R. S., et al. (2009). Increased InsP3Rs in the junctional sarcoplasmic reticulum augment Ca2+ transients and arrhythmias associated with cardiac hypertrophy. Proceedings of the National Academy of Sciences of the United States of America, 106(27), 11406-11411.
57. Ling, H., Zhang, T., Pereira, L., et al. (2009). Requirement for Ca2+/ calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. The Journal of Clinical Investigation, 119(5), 1230-1240.
58. Terentyev, D., Gyorke, I., Belevych, A. E., et al. (2008). Redox modification of ryanodine receptors contributes to sarcoplasmic reticulum Ca2+ leak in chronic heart failure. Circulation Research, 103(12), 1466-1472.
59. Plotnikov, A. N., Yu, H., Geller, J. C., et al. (2003). Role of L-type calcium channels in pacing-induced short-term and long-term cardiac memory in canine heart. Circulation, 107(22), 2844-2849. (Pubitemid 36705996)
60. Ai, X., Curran, J. W., Shannon, T. R., et al. (2005). Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circulation Research, 97(12), 1314-1322.
61. Kohlhaas, M., Zhang, T., Seidler, T., et al. (2006). Increased sarcoplasmic reticulum calcium leak but unaltered contractility by acute CaMKII overexpression in isolated rabbit cardiac myocytes. Circulation Research, 98(2), 235-244.
62. Maier, L. S., Zhang, T., Chen, L., et al. (2003). Transgenic CaMKIIdeltaC overexpression uniquely alters cardiac myocyte Ca2+ handling: Reduced SR Ca2+ load and activated SR Ca2+ release. Circulation Research, 92(8), 904-911. (Pubitemid 36542532)
63. Chakir, K., Daya, S. K., Tunin, R. S., et al. (2008). Reversal of global apoptosis and regional stress kinase activation by cardiac resynchronization. Circulation, 117(11), 1369-1377. (Pubitemid 351501490)
64. Aiba, T., Barth, A. S., Liu, T., et al. (2008). Cardiac resynchronization therapy restores beta-adrenergic reserve of ca2+ homeostasis in a canine model of dyssynchronous heart failure. Circulation, 118(Suppl), 523-524.
65. Chakir, K., Daya, S. K., Aiba, T., et al. (2009). Mechanisms of enhanced beta-adrenergic reserve from cardiac resynchronization therapy. Circulation, 119(9), 1231-1240.
66. Shang, L. L., Pfahnl, A. E., Sanyal, S., et al. (2007). Human heart failure is associated with abnormal C-terminal splicing variants in the cardiac sodium channel. Circulation Research, 101(11), 1146-1154. (Pubitemid 350146441)
67. Pu, J., & Boyden, P. A. (1997). 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. Jul, 81(1), 110-119. (Pubitemid 27272989)
68. Undrovinas, A. I., Maltsev, V. A., & Sabbah, H. N. (1999). Repolarization abnormalities in cardiomyocytes of dogs with chronic heart failure: Role of sustained inward current. Cellular and Molecular Life Sciences, 55(3), 494-505. (Pubitemid 29178888)
69. Valdivia, C. R., Chu, W. W., Pu, J., et al. (2005). Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. Journal of Molecular and Cellular Cardiology, 38(3), 475-483. (Pubitemid 40331938)
70. Aiba, T., Hashambhoy, Y., Barth, A., et al. (2009). Cardiac resynchronization therapy improves altered na channel gating in canine model of dyssynchronous heart failure. Circulation, 120, S627.
71. Fernandez-Velasco, M., Ruiz-Hurtado, G., Hurtado, O., et al. (2007). TNF-alpha downregulates transient outward potassium current in rat ventricular myocytes through iNOS overexpression and oxidant species generation. American Journal of Physiology. Heart and Circulatory Physiology, 293(1), H238-H245. (Pubitemid 47105078)
72. Xie, L. H., Chen, F., Karagueuzian, H. S., et al. (2009). Oxidativestress-induced afterdepolarizations and calmodulin kinase II signaling. Circulation Research, 104(1), 79-86.
73. Maltsev, V. A., Reznikov, V., Undrovinas, N. A., et al. (2008). Modulation of late sodium current by Ca2+, calmodulin, and CaMKII in normal and failing dog cardiomyocytes: Similarities and differences. American Journal of Physiology. Heart and Circulatory Physiology, 294(4), H1597-H1608. (Pubitemid 351490589)
74. Wagner, S., Dybkova, N., Rasenack, E. C., et al. (2006). Ca2+/ calmodulin-dependent protein kinase II regulates cardiac Na+ channels. The Journal of Clinical Investigation, 116(12), 3127-3138. (Pubitemid 44878627)
75. Aiba, T., Hesketh, G. G., Liu, T., et al. (2010). Na+channel regulation by Ca2+/calmodulin and Ca2+/calmodulin-dependent protein kinase II in guinea-pig ventricular myocytes. Cardiovascular Research, 85(3), 454-463.
76. Wu, Y., Temple, J., Zhang, R., et al. (2002). Calmodulin kinase II and arrhythmias in a mouse model of cardiac hypertrophy. Circulation, 106(10), 1288-1293. (Pubitemid 34988650)
77. Wagner, S., Ruff, H. M., Weber, S. L., et al. (2011). Reactive oxygen species-activated Ca/calmodulin kinase IIdelta is required for late I(Na) augmentation leading to cellular Na and Ca overload. Circulation Research, 108(5), 555-565.