© 1996 American Heart Association, Inc.
Articles |
Ionic Mechanism of Action Potential Prolongation in Ventricular Myocytes From Dogs With Pacing-Induced Heart Failure
From the Division of Cardiology, Department of Medicine, The Johns Hopkins University School of Medicine, Baltimore, Md.
Correspondence to Gordon F. Tomaselli, MD, 844 Ross Bldg, The Johns Hopkins University School of Medicine, Baltimore, MD 21205. E-mail gtomasel@welchlink.welch.jhu.edu.
Abstract Membrane current abnormalities have been described in human heart failure. To determine whether similar current changes are observed in a large animal model of heart failure, we studied dogs with pacing-induced cardiomyopathy. Myocytes isolated from the midmyocardium of 13 dogs with heart failure induced by 3 to 4 weeks of rapid ventricular pacing and from 16 nonpaced control dogs did not differ in cell surface area or resting membrane potential. Nevertheless, action potential duration (APD) was significantly prolonged in myocytes isolated from failing ventricles (APD at 90% repolarization, 1097±73 milliseconds [failing hearts, n=30] versus 842±56 milliseconds [control hearts, n=25]; P<.05), and the prominent repolarizing notch in phase 1 was dramatically attenuated. Basal L-type Ca2+ current and whole-cell Na+ current did not differ in cells from failing and from control hearts, but significant differences in K+ currents were observed. The density of the inward rectifier K+ current (IK1) was reduced in cells from failing hearts at test potentials below -90 mV (at -150 mV, -19.1±2.2 pA/pF [failing hearts, n=18] versus -32.2±5.1 pA/pF [control hearts, n=15]; P<.05). The small outward current component of IK1 was also reduced in cells from failing hearts (at -60 mV, 1.7±0.2 pA/pF [failing hearts] versus 2.5±0.2 pA/pF [control hearts]; P<.05). The peak of the Ca2+-independent transient outward current (Ito) was dramatically reduced in myocytes isolated from failing hearts compared with nonfailing control hearts (at +80 mV, 7.0±0.9 pA/pF [failing hearts, n=20] versus 20.4±3.2 pA/pF [control hearts, n=15]; P<.001), while the steady state component was unchanged. There were no significant differences in Ito kinetics or single-channel conductance. A reduction in the number of functional Ito channels was demonstrated by nonstationary fluctuation analysis (0.4±0.03 channels per square micrometer [failing hearts, n=5] versus 1.2±0.1 channels per square micrometer [control hearts, n=3]; P<.001). Pharmacological reduction of Ito by 4-aminopyridine in control myocytes decreased the notch amplitude and prolonged the APD. Current clamp–release experiments in which current was injected for 8 milliseconds to reproduce the notch sufficed to shorten the APD significantly in cells from failing hearts. These data support the hypothesis that downregulation of Ito in pacing-induced heart failure is at least partially responsible for the action potential prolongation. Because the repolarization abnormalities mimic those in cells isolated from failing human ventricular myocardium, canine pacing-induced cardiomyopathy may provide insights into the development of repolarization abnormalities and the mechanisms of sudden death in patients with heart failure.
Key Words: action potential • heart failure • animal model • K+ current • transient outward current
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 J. J. C. Rosenthal and F. Bezanilla A comparison of propagated action potentials from tropical and temperate squid axons: different durations and conduction velocities correlate with ionic conductance levels J. Exp. Biol., June 15, 2002; 205(12): 1819 - 1830. [Abstract] [Full Text] [PDF]
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G. J. Rozanski and Z. Xu Glutathione and K+ channel remodeling in postinfarction rat heart Am J Physiol Heart Circ Physiol, June 1, 2002; 282(6): H2346 - H2355. [Abstract] [Full Text] [PDF]
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D. Lacroix, P. Gluais, C. Marquie, C. D'Hoinne, M. Adamantidis, and M. Bastide Repolarization abnormalities and their arrhythmogenic consequences in porcine tachycardia-induced cardiomyopathy Cardiovasc Res, April 1, 2002; 54(1): 42 - 50. [Abstract] [Full Text] [PDF]
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L.-M. Zhang, Z. Wang, and S. Nattel Effects of sustained beta -adrenergic stimulation on ionic currents of cultured adult guinea pig cardiomyocytes Am J Physiol Heart Circ Physiol, March 1, 2002; 282(3): H880 - H889. [Abstract] [Full Text] [PDF]
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K. R Sipido, P. G.A Volders, M. A Vos, and F. Verdonck Altered Na/Ca exchange activity in cardiac hypertrophy and heart failure: a new target for therapy? Cardiovasc Res, March 1, 2002; 53(4): 782 - 805. [Abstract] [Full Text] [PDF]
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R. Sah, R. J. Ramirez, and P. H. Backx Modulation of Ca2+ Release in Cardiac Myocytes by Changes in Repolarization Rate: Role of Phase-1 Action Potential Repolarization in Excitation-Contraction Coupling Circ. Res., February 8, 2002; 90(2): 165 - 173. [Abstract] [Full Text] [PDF]
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T. Watanabe, M. Yamaki, S. Yamauchi, O. Minamihaba, T. Miyashita, I. Kubota, and H. Tomoike Regional prolongation of ARI and altered restitution properties cause ventricular arrhythmia in heart failure Am J Physiol Heart Circ Physiol, January 1, 2002; 282(1): H212 - H218. [Abstract] [Full Text] [PDF]
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B Huang, D Qin, and N El-Sherif Spatial alterations of Kv channels expression and K+ currents in post-MI remodeled rat heart Cardiovasc Res, November 1, 2001; 52(2): 246 - 254. [Abstract] [Full Text] [PDF]
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N. Decher, O. Uyguner, C. R Scherer, B. Karaman, M. Yuksel-Apak, A. E Busch, K. Steinmeyer, and B. Wollnik hKChIP2 is a functional modifier of hKv4.3 potassium channels: Cloning and expression of a short hKChIP2 splice variant Cardiovasc Res, November 1, 2001; 52(2): 255 - 264. [Abstract] [Full Text] [PDF]
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W. Han, D. Chartier, D. Li, and S. Nattel Ionic Remodeling of Cardiac Purkinje Cells by Congestive Heart Failure Circulation, October 23, 2001; 104(17): 2095 - 2100. [Abstract] [Full Text] [PDF]
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Z. Wang, W. Kutschke, K. E. Richardson, M. Karimi, and J. A. Hill Electrical Remodeling in Pressure-Overload Cardiac Hypertrophy: Role of Calcineurin Circulation, October 2, 2001; 104(14): 1657 - 1663. [Abstract] [Full Text] [PDF]
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S. Kaab and M. Nabauer Diversity of ion channel expression in health and disease Eur. Heart J. Suppl., September 1, 2001; 3(suppl_K): K31 - K40. [Abstract] [PDF]
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R. F Gilmour Jr. Life out of balance: The sympathetic nervous system and cardiac arrhythmias Cardiovasc Res, September 1, 2001; 51(4): 625 - 626. [Full Text] [PDF]
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R. Sah, R. J Ramirez, R. Kaprielian, and P. H Backx Alterations in action potential profile enhance excitation-contraction coupling in rat cardiac myocytes J. Physiol., May 15, 2001; 533(1): 201 - 214. [Abstract] [Full Text] [PDF]
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 P. B. Adamson and E. Vanoli Early autonomic and repolarization abnormalities contribute to lethal arrhythmias in chronic ischemic heart failure: Characteristics of a novel heart failure model in dogs with postmyocardial infarction left ventricular dysfunction J. Am. Coll. Cardiol., May 1, 2001; 37(6): 1741 - 1748. [Abstract] [Full Text] [PDF]
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D. Babuty and M. J Lab Mechanoelectric contributions to sudden cardiac death Cardiovasc Res, May 1, 2001; 50(2): 270 - 279. [Full Text] [PDF]
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S. Demolombe, G. Lande, F. Charpentier, M. A van Roon, M. J.B van den Hoff, G. Toumaniantz, I. Baro, G. Guihard, N. Le Berre, A. Corbier, et al. Transgenic mice overexpressing human KvLQT1 dominant-negative isoform Part I: Phenotypic characterisation Cardiovasc Res, May 1, 2001; 50(2): 314 - 327. [Abstract] [Full Text] [PDF]
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I. A. Hobai and B. O'Rourke Decreased Sarcoplasmic Reticulum Calcium Content Is Responsible for Defective Excitation-Contraction Coupling in Canine Heart Failure Circulation, March 20, 2001; 103(11): 1577 - 1584. [Abstract] [Full Text] [PDF]
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J. Huang, J. M. Rogers, C. R. Killingsworth, G. P. Walcott, B. H. KenKnight, W. M. Smith, and R. E. Ideker Improvement of Defibrillation Efficacy and Quantification of Activation Patterns During Ventricular Fibrillation in a Canine Heart Failure Model Circulation, March 13, 2001; 103(10): 1473 - 1478. [Abstract] [Full Text] [PDF]
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 C.-E. Laurent, R. Cardinal, G. Rousseau, M. Vermeulen, C. Bouchard, M. Wilkinson, J. A. Armour, and M. Bouvier Functional desensitization to isoproterenol without reducing cAMP production in canine failing cardiocytes Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2001; 280(2): R355 - R364. [Abstract] [Full Text] [PDF]
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J.-Q. He, M. W Conklin, J. D Foell, M. R Wolff, R. A Haworth, R. Coronado, and T. J Kamp Reduction in density of transverse tubules and L-type Ca2+ channels in canine tachycardia-induced heart failure Cardiovasc Res, February 1, 2001; 49(2): 298 - 307. [Abstract] [Full Text] [PDF]
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S. S. Chugh, S. B. Johnson, and D. L. Packer Altered response to ibutilide in a heart failure model Cardiovasc Res, January 1, 2001; 49(1): 94 - 102. [Abstract] [Full Text] [PDF]
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C. Pandozi, L. Bianconi, L. Calo, A. Castro, F. Lamberti, M. C. Scianaro, G. Gentilucci, and M. Santini Postcardioversion atrial electrophysiologic changes induced by oral verapamil in patients with persistent atrial fibrillation J. Am. Coll. Cardiol., December 1, 2000; 36(7): 2234 - 2241. [Abstract] [Full Text] [PDF]
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J. L. Greenstein, R. Wu, S. Po, G. F. Tomaselli, and R. L. Winslow Role of the Calcium-Independent Transient Outward Current Ito1 in Shaping Action Potential Morphology and Duration Circ. Res., November 24, 2000; 87(11): 1026 - 1033. [Abstract] [Full Text] [PDF]
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S. Nattel Acquired delayed rectifier channelopathies: how heart disease and antiarrhythmic drugs mimic potentially-lethal congenital cardiac disorders Cardiovasc Res, November 1, 2000; 48(2): 188 - 190. [Full Text] [PDF]
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Y. Tsuji, T. Opthof, K. Kamiya, K. Yasui, W. Liu, Z. Lu, and I. Kodama 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, November 1, 2000; 48(2): 300 - 309. [Abstract] [Full Text] [PDF]
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K. Schlotthauer and D. M. Bers Sarcoplasmic Reticulum Ca2+ Release Causes Myocyte Depolarization : Underlying Mechanism and Threshold for Triggered Action Potentials Circ. Res., October 27, 2000; 87(9): 774 - 780. [Abstract] [Full Text] [PDF]
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