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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
From the Masonic Medical Research Laboratory, Utica, NY.
Correspondence to Dr Charles Antzelevitch, Masonic Medical Research Laboratory, 2150 Bleecker St, Utica, NY 13504.
Abstract Recent studies have described regional differences in the electrophysiology and pharmacology of ventricular myocardium in canine, feline, rat, guinea pig, and human hearts. In this study, we use standard microelectrode and whole-cell patch-clamp techniques to examine the characteristics of the action potential and the delayed rectifier K+ current (IK) in epicardial, M region (deep subepicardial to midmyocardial), and endocardial cells isolated from the canine left ventricle. Cells from the M region displayed much longer action potential durations (APDs) at slow rates. At a basic cycle length of 4 s, APD measured at 90% repolarization was 358±16 (mean±SEM), 262±12, and 287±11 ms in cells from the M region, epicardium, and endocardium, respectively. Steady state APD-rate relations were steeper in cells from the M region. In complete Tyrode's solution, IK was smaller in myocytes from the M region when compared with those isolated from the epicardium or endocardium. Further characterization of IK was conducted in a Na+-, K+-, and Ca2+-free bath solution to isolate the slowly activating component of the delayed rectifier (IKs) from the rapidly activating component (IKr). IKs was significantly smaller in M cells than in epicardial and endocardial cells. With repolarization to -20 mV, IKs tail current density was 1.99±0.30 pA/pF (mean±SEM) in epicardial cells, 1.83±0.18 pA/pF in endocardial cells, and 0.92±0.14 pA/pF in M cells. Voltage dependence and time course of activation and deactivation of IKs were similar in the three cell types. The relative contribution of IKr and IKs among the three cell types was examined by using 6 mmol/L [K+]o Tyrode's solution with and without E-4031, a highly selective blocker of IKr. An E-4031–sensitive current was observed in the presence but not in the absence of extracellular K+. This rapidly activating component showed characteristics similar to those of IKr as described in rabbit and cat ventricular cells. Deactivation of IKr was significantly slower than that of IKs. IKr (E-4031–sensitive component) tail current density was similar in the three cell types, whereas IKs (E-4031–insensitive component) tail current density was significantly smaller in the M cells. Our results suggest that the distinctive phase-3 repolarization features of M cells are due in part to a lesser contribution of IKs and that this distinction may also explain why M cells are the main targets for agents that prolong APD in ventricular myocardium. These findings may advance our understanding of the ionic basis for the electrocardiographic T wave, U wave, and long QT intervals as well as our understanding of factors contributing to the development of cardiac arrhythmias.
Key Words: ventricular myocardium • electrophysiology • heterogeneity • M cells • delayed rectifier K+ currents
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C. E Conrath, A. A.M Wilde, R. J.E Jongbloed, M. Alders, I. M van Langen, J Peter van Tintelen, P. A Doevendans, and T. Opthof Gender differences in the long QT syndrome: effects of {beta}-adrenoceptor blockade Cardiovasc Res, February 15, 2002; 53(3): 770 - 776. [Abstract] [Full Text] [PDF]
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M Lei, H Honjo, I Kodama, and M R Boyett Heterogeneous expression of the delayed-rectifier K+ currents iK,r and iK,s in rabbit sinoatrial node cells J. Physiol., September 15, 2001; 535(3): 703 - 714. [Abstract] [Full Text] [PDF]
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Z. Lu, K. Kamiya, T. Opthof, K. Yasui, and I. Kodama Density and Kinetics of IKr and IKs in Guinea Pig and Rabbit Ventricular Myocytes Explain Different Efficacy of IKs Blockade at High Heart Rate in Guinea Pig and Rabbit: Implications for Arrhythmogenesis in Humans Circulation, August 21, 2001; 104(8): 951 - 956. [Abstract] [Full Text] [PDF]
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A. C. Zygmunt, G. T. Eddlestone, G. P. Thomas, V. V. Nesterenko, and C. Antzelevitch Larger late sodium conductance in M cells contributes to electrical heterogeneity in canine ventricle Am J Physiol Heart Circ Physiol, August 1, 2001; 281(2): H689 - H697. [Abstract] [Full Text] [PDF]
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B. B. Lerman, E. D. Engelstein, and D. Burkhoff Mechanoelectrical Feedback: Role of {beta}-Adrenergic Receptor Activation in Mediating Load-Dependent Shortening of Ventricular Action Potential and Refractoriness Circulation, July 24, 2001; 104(4): 486 - 490. [Abstract] [Full Text] [PDF]
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C. Antzelevitch Transmural dispersion of repolarization and the T wave Cardiovasc Res, June 1, 2001; 50(3): 426 - 431. [Full Text] [PDF]
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P. Taggart, P. M.I Sutton, T. Opthof, R. Coronel, R. Trimlett, W. Pugsley, and P. Kallis Transmural repolarisation in the left ventricle in humans during normoxia and ischaemia Cardiovasc Res, June 1, 2001; 50(3): 454 - 462. [Abstract] [Full Text] [PDF]
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T. V. Pham, E. A. Sosunov, R. Z. Gainullin, P. Danilo Jr, and M. R. Rosen Impact of Sex and Gonadal Steroids on Prolongation of Ventricular Repolarization and Arrhythmias Induced by IK-Blocking Drugs Circulation, May 1, 2001; 103(17): 2207 - 2212. [Abstract] [Full Text] [PDF]
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 U. C. Hoppe, E. Marban, and D. C. Johns Distinct gene-specific mechanisms of arrhythmia revealed by cardiac gene transfer of two long QT disease genes, HERG and KCNE1 PNAS, April 24, 2001; 98(9): 5335 - 5340. [Abstract] [Full Text] [PDF]
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F. L Burton and S. M Cobbe Dispersion of ventricular repolarization and refractory period Cardiovasc Res, April 1, 2001; 50(1): 10 - 23. [Full Text] [PDF]
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W. Han, Z. Wang, and S. Nattel Slow delayed rectifier current and repolarization in canine cardiac Purkinje cells Am J Physiol Heart Circ Physiol, March 1, 2001; 280(3): H1075 - H1080. [Abstract] [Full Text] [PDF]
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L. Virag, N. Iost, M. Opincariu, J. Szolnoky, J. Szecsi, G. Bogats, P. Szenohradszky, A. Varro, and J. Gy. Papp The slow component of the delayed rectifier potassium current in undiseased human ventricular myocytes Cardiovasc Res, March 1, 2001; 49(4): 790 - 797. [Abstract] [Full Text] [PDF]
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T. Volk, T. H.-D. Nguyen, J.-H. Schultz, J. Faulhaber, and H. Ehmke Regional alterations of repolarizing K+ currents among the left ventricular free wall of rats with ascending aortic stenosis J. Physiol., February 1, 2001; 530(3): 443 - 455. [Abstract] [Full Text] [PDF]
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C. Antzelevitch Electrical Heterogeneity, Cardiac Arrhythmias, and the Sodium Channel Circ. Res., November 24, 2000; 87(11): 964 - 965. [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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M. Jiang, C. Cabo, J.-A. Yao, P. A Boyden, and G.-N. Tseng Delayed rectifier K currents have reduced amplitudes and altered kinetics in myocytes from infarcted canine ventricle Cardiovasc Res, October 1, 2000; 48(1): 34 - 43. [Abstract] [Full Text] [PDF]
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J. Merot, V. Probst, M. Debailleul, U. Gerlach, N. S. Moise, H. Le Marec, and F. Charpentier Electropharmacological characterization of cardiac repolarization in German shepherd dogs with an inherited syndrome of sudden death: abnormal response to potassium channel blockers J. Am. Coll. Cardiol., September 1, 2000; 36(3): 939 - 947. [Abstract] [Full Text] [PDF]
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 W Haverkamp, G Breithardt, A.J Camm, M.J Janse, M.R Rosen, C Antzelevitch, D Escande, M Franz, M Malik, A Moss, et al. The potential for QT prolongation and proarrhythmia by non-antiarrhythmic drugs: clinical and regulatory implications. Report on a Policy Conference of the European Society of Cardiology Eur. Heart J., August 1, 2000; 21(15): 1216 - 1231. [PDF]
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A.J. Camm, M.J. Janse, D.M. Roden, M.R. Rosen, J. Cinca, and S.M. Cobbe Congenital and acquired long QT syndrome Eur. Heart J., August 1, 2000; 21(15): 1232 - 1237. [PDF]
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W. Haverkamp, G. Breithardt, A.J. Camm, M. J Janse, M. R Rosen, C. Antzelevitch, D. Escande, M. Franz, M. Malik, A. Moss, et al. The potential for QT prolongation and pro-arrhythmia by non-anti-arrhythmic drugs: Clinical and regulatory implications: Report on a Policy Conference of the European Society of Cardiology Cardiovasc Res, August 1, 2000; 47(2): 219 - 233. [Full Text] [PDF]
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W. Guo, H. Li, B. London, and J. M. Nerbonne Functional Consequences of Elimination of Ito, f and Ito, s : Early Afterdepolarizations, Atrioventricular Block, and Ventricular Arrhythmias in Mice Lacking Kv1.4 and Expressing a Dominant-Negative Kv4 {alpha} Subunit Circ. Res., July 7, 2000; 87(1): 73 - 79. [Abstract] [Full Text] [PDF]
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J. F. Spear and E. N. Moore Modulation of arrhythmias by isoproterenol in a rabbit heart model of d-sotalol-induced long Q-T intervals Am J Physiol Heart Circ Physiol, July 1, 2000; 279(1): H15 - H25. [Abstract] [Full Text] [PDF]
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J. M Nerbonne Molecular basis of functional voltage-gated K+ channel diversity in the mammalian myocardium J. Physiol., June 1, 2000; 525(2): 285 - 298. [Abstract] [Full Text] [PDF]
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