Clinical potential of sodium-calcium exchanger inhibitors as antiarrhythmic agents

Drugs

Volumn 63, Issue 5, 2003, Pages 439-452

  Pogwizd, Steven M ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; 2 [4 (2,5 DIFLUOROBENZYLOXY)PHENOXY] 5 ETHOXYANILINE; ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMILORIDE; AMILORIDE DERIVATIVE; ANTIARRHYTHMIC AGENT; BEPRIDIL; CALCIUM CHANNEL L TYPE; CALCIUM ION; ION CHANNEL; MEPACRINE; OUABAIN; RYANODINE RECEPTOR; SODIUM CALCIUM EXCHANGE INHIBITOR; SODIUM ION; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANTIARRHYTHMIC ACTIVITY; ARRHYTHMOGENESIS; CONTROLLED STUDY; DRUG MECHANISM; EXCITATION CONTRACTION COUPLING; HEART ARRHYTHMIA; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE PERFUSION; HEART VENTRICLE ARRHYTHMIA; HUMAN; HUMAN CELL; NONHUMAN; RABBIT; RAT; REPERFUSION INJURY; REVIEW; SARCOPLASMIC RETICULUM; SODIUM CALCIUM EXCHANGE; STOICHIOMETRY;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; ARRHYTHMIA; CALCIUM; HEART FAILURE, CONGESTIVE; HUMANS; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; SODIUM; SODIUM-CALCIUM EXCHANGER;

ANIMALIA; ITI; ORYCTOLAGUS CUNICULUS; STROPHANTHUS GRATUS;

EID: 0037226250     PISSN: 00126667     EISSN: None     Source Type: Journal    
DOI: 10.2165/00003495-200363050-00001     Document Type: Review

References (110)

1. Bers DM. Excitation-contraction coupling and cardiac contractile force. 2nd ed. Dordrecht: Kluwer, 2001
2. Pogwizd SM, Schlotthauer K, Li L, et al. Arrhythmogenesis and contractile dysfunction in heart failure: roles of sodium-calcium exchange, inward rectifier potassium current, and residual β-adrenergic responsiveness. Circ Res 2001; 88: 1159-67
3. Koster OF, Szigeti GP, Beuckelmann DJ. Characterization of a [Ca2+]i-dependent current in human atrial and ventricular cardiomyocytes in the absence of Na+ and K+. Cardiovasc Res 1999; 41: 175-87
4. Wit AL, Rosen MR. After depolarizations and triggered activity: distinction from automaticity as an arrhythmogenic mechanism. In: Fozzard HA, Haber E, Jennings RB, et al., editors. Heart and cardiovascular system: scientific foundations. 2nd ed. New York (NY): Raven, 1992: 2113-63
5. Hryshko LV. The cardiac Na+-Ca2+ exchanger. In: Page E, Fozzard HA, Solaro RJ. editors. Handbook of physiology. Section 2: the cardiovascular system. Vol. 1: the heart. New York (NY): Oxford, 2002: 388-419
6. Blaustein MP, Lederer WJ. Sodium/calcium exchange: its physiological implications. Physiol Rev 1999; 79: 763-854
7. Egger M, Niggli E. Regulatory function of Na-Ca exchange in the heart: milestones and outlook. J Membr Biol 1999; 168: 107-30
8. Pogwizd SM, Bers DM. Na/Ca exchange in heart failure: contractile dysfunction and arrhythmogenesis. Ann N Y Acad Sci 2002; 976: 454-65
9. Sipido KR, Volders PGA, Vos MA, et al. Altered Na/Ca exchange activity in cardiac hypertrophy and heart failure: a new target for therapy? Cardiovasc Res 2002; 53: 782-805
10. Phillipson KD, Nicoll DA. Sodium-calcium exchange: a molecular perspective. Annu Rev Physiol 2000; 62: 111-33
11. Reeves JP. Sodium-calcium exchange: a possible target for drug development. Drug Dev Res 1989; 18: 295-304
12. Shigekawa M, Iwamoto M. Cardiac Na+-Ca++ exchange: molecular and pharmacological aspects. Circ Res 2001; 88: 864-76
13. Yashar PR, Fransua M, Frishman WH. The sodium-calcium ion membrane exchanger: physiologic significance and pharmacologic implications. J Clin Pharmacol 1998; 38: 393-401
14. Bassani JWM, Bassani RA, Bers DM. Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 1994; 476: 279-93
15. Reeves JP, Hale CC. The stoichiometry of the cardiac sodium-calcium exchange system. J Biol Chem 1984; 259: 7733-9
16. Fujioka Y, Komeda M, Matsuoka S. Stoichiometry of Na+/Ca2+ exchange in inside-out patches excised from guinea-pig ventricular myocytes. J Physiol 2000; 523: 339-51
17. Sipido KR, Volders PGA, de Groot M, et al. Enhanced Ca2+ release and Na/Ca exchange activity in hypertrophied canine ventricular myocytes: potential link between contractile adaptation and arrhythmogenesis. Circulation 2000; 102: 2137-44
18. Grantham CJ, Cannell MB. Ca2+ influx during the cardiac action potential in guinea pig ventricular myocytes. Circ Res 1996; 79: 194-200
19. Sipido KR, Maes M, Van de Werf F. Low efficiency of Ca2+ entry through the Na+-Ca2+ exchanger as trigger for Ca2+ release from the sarcoplasmic reticulum: a comparison between L-type Ca2+ current and reverse-mode Na+-Ca2+ exchange. Circ Res 1997; 81: 1034-44
20. Evans AM, Cannell MB. The role of L-type Ca2+ current and Na+ current-stimulated Na/Ca exchange in triggering SR calcium release in guinea-pig cardiac ventricular myocytes. Cardiovasc Res 1997; 35: 294-302
21. Litwin SE, LI J, Bridge JHB. Na-Ca exchange and the trigger for sarcoplasmic reticulum Ca release: studies in adult rabbit ventricular myocytes. Biophys J 1998; 75: 359-71
22. Bers DM, Christensen DM, Nguyen TX. Can Ca entry via NaCa exchange directly activate cardiac muscle contraction? J Mol Cell Cardiol 1988; 20: 405-14
23. Mattiello JA, Margulies KB, Jeevanandam V, et al. Contribution of reverse-mode sodium-calcium exchange to contractions in failing human left ventricular myocytes. Cardiovasc Res 1998; 37: 424-31
24. Dipla K, Mattiello JA, Margulies KB, et al. The sarcoplasmic reticulum and the Na+/Ca+ exchanger both contribute to the Ca2+ transient of failing human ventricular myocytes. Circ Res 1999; 84: 435-44
25. Gaughan JP, Furukawa S, Jeevanandam V, et al. Sodium/calcium exchange contributes to contraction and relaxation in failed human ventricular myocytes. Am J Physiol 1999; 277: H714-24
26. Weber CR, Piacentino V, Ginsburg KS, et al. Na+-Ca2+ exchange current and submembrane [Ca2+] during the cardiac action potential. Circ Res 2002; 90: 182-9
27. Despa S, Islam MA, Pogwizd SM, et al. Intracellular Na+ concentration is elevated in heart failure, but Na/K-pump function is unchanged. Circulation 2002; 105: 2543-8
28. Undrovinas AI, Fleidervish IA, Makielski JC. Inward sodium current at resting potentials in single cardiac myocytes induced by the ischemic metabolite lysophosphatidylcholine. Circ Res 1992; 71: 1231-41
29. Ju YK, Saint DA, Gage PW. Hypoxia increases persistent sodium current in rat ventricular myocytes. J Physiol 1996; 497: 337-47
30. Karmazyn M, Gan XH, Humphreys RA, et al. The myocardial Na+-H+ exchange: structure, regulation, and its role in heart disease. Circ Res 1999; 85: 777-86
31. Eigel BN, Hadley RW. Contribution of the Na+ channel and Na+/H+ exchanger to the anoxic rise of [Na+] in ventricular myocytes. Am J Physiol 1999; 277: H1817-22
32. Schmidt TA, Kjeldsen K. Human myocardial Na,K-ATPase: quantification, regulation and relation to Ca. Cardiovasc Res 1998; 37: 335-45
33. Packer M. Sudden unexpected death in patients with congestive heart failure: a second frontier. Circulation 1985; 72: 681-5
34. Pogwizd SM. Nonreentrant mechanisms underlying spontaneous ventricular arrhythmias in a model of nonischemic heart failure in rabbits. Circulation 1995; 92: 1034-48
35. Pogwizd SM, Hoyt RH, Saffitz JE, et al. Reentrant and focal mechanisms underlying ventricular tachycardia in the human heart. Circulation 1992; 86: 1872-87
36. Pogwizd SM, McKenzie JP, Cain ME. Mechanisms underlying spontaneous and induced ventricular arrhythmias in patients with idiopathic dilated cardiomyopathy. Circulation 1998; 98: 2404-14
37. Pogwizd SM, Qi M, Yuan W, et al. Upregulation of Na+/Ca2+ exchanger expression and function in an arrhythmogenic rabbit model of heart failure. Circ Res 1999; 85: 1009-19
38. Vermeulen JT, McGuire MA, Opthof T, et al. Triggered activity and automaticity in ventricular trabeculae of failing human and rabbit hearts. Cardiovasc Res 1994; 28: 1547-54
39. Hobai IA, O'Rourke B. Enhanced Ca2-activated Na-Ca2 exchange activity in canine pacing-induced heart failure. Circ Res 2000; 87: 690-8
40. Studer R, Reinecke H, Bilder J, et al. Gene expression of the cardiac Na+-Ca2+-exchanger in end-stage human heart failure. Circ Res 1994; 90: 1441-58
41. Hasenfuss G, Schillinger W, Preuss M, et al. Relationship between Na+-Ca2+-exchanger protein levels and diastolic function of failing human myocardium. Circulation 1999; 99: 641-8
42. Janse MJ, Wit AL. Electrophysiological mechanisms of ventricular arrhythmias resulting from myocardial ischemia and infarction. Physiol Rev 1989; 69: 1049-169
43. Pogwizd SM, Corr PB. Reentrant and nonreentrant mechanisms contribute to arrhythmogenesis during early myocardial ischemia: results using three-dimensional mapping. Circ Res 1987; 61: 352-71
44. Pogwizd SM, Corr PB. Mechanisms underlying the development of ventricular fibrillation during early myocardial ischemia. Circ Res 1990; 66: 672-95
45. Furukawa T, Kimura S, Furukawa N, et al. Role of cardiac ATP-regulated potassium channels in differential responses of endocardial and epicardial cells to ischemia. Circ Res 1991; 68: 1693-702
46. McHowat J, Yamada KA, Wu J, et al. Recent insights pertaining to sarcolemmal phospholipid alterations underlying arrhythmogenesis in the ischemic heart. J Cardiovasc Electrophysiol 1993; 4: 288-310
47. Kléber A, Riegger CV, Janse MJ. Electrical uncoupling and increase in extracellular resistance after induction of ischemia in isolated, arterially perfused rabbit papillary muscle. Circ Res 1987; 61: 271-9
48. Beardslee MA, Lerner DL, Tadros PN, et al. Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia. Circ Res 2000; 87: 656-62
49. Coetze WA, Opie LH. Effects of components of ischemia and metabolic inhibition on delayed after depolarizations in guinea pig papillary muscle. Circ Res 1987; 61: 157-65
50. Ferrier GR, Moffat MP, Lukas A. Possible mechanisms of ventricular arrhythmias elicited by ischemia followed by reperfusion: studies on isolated canine ventricular tissues. Circ Res 1985; 56: 184-94
51. Xiao XH, Allen DG. Role of Na+/H+ exchanger during ischemia and preconditioning in the isolated rat heart. Circ Res 1999; 85: 723-30
52. Bountra C, Vaughan-Jones RD. Effect of intracellular and extracellular pH on contraction in isolated mammalian cardiac tissue. J Physiol 1989; 418: 163-87
53. Yan GX, Kléber AG. Changes in extracellular and intracellular pH in ischemic rabbit papillary muscle. Circ Res 1992; 71: 460-70
54. Marban E, Kitakaze M, Koretsune Y, et al. Quantification of [Ca2]i in perfused hearts: critical evaluation of the 5F-BAPTA and nuclear magnetic resonance method as applied to the study of ischemia and reperfusion. Circ Res 1990; 66: 1255-67
55. Ch'En FFT, Vaughan-Jones RD, Clarke K, et al. Modeling myocardial ischemia and reperfusion. Prog Biophys Mol Biol 1998; 69: 515-38
56. Philipson KD, Ward R. Effects of fatty acids on Na+-Ca2+ exchange and Ca2+ permeability of cardiac sarcolemmal vesicles. J Biol Chem 1985; 260: 9666-71
57. Pogwizd SM, Corr PB. Electrophysiologic mechanisms underlying arrhythmias due to reperfusion of ischemic myocardium. Circulation 1987; 76: 404-26
58. Woodcock EA, Arthur JF, Harrison SN, et al. Reperfusion-induced Ins (1,4,5)P3 generation and arrhythmogenesis require activation of the Na+/Ca2+ exchanger. J Mol Cell Cardiol 2001; 33: 1861-9
59. Goldhaber JI, Ji S, Lamp ST, et al. Effects of exogenous free radicals on electromechanical function and metabolism in isolated rabbit and guinea pig hearts. J Clin Invest 1989; 83: 1800-9
60. Goldhaber JI. Free radicals enhance Na+/Ca2+ exchange in ventricular myocytes. Am J Physiol 1996; 271: H823-33
61. Barrington PL, Meier CF, Weglicki WB. Abnormal electrical activity induced by free radical generating systems in isolated cardiocytes. J Mol Cell Cardiol 1988; 20: 1163-78
62. Matsuura H, Shattock MJ. Membrane potential fluctuations and transient inward currents induced by reactive oxygen intermediates in isolated rabbit ventricular cells. Circ Res 1991; 68: 319-29
63. Josephson RA, Silverman HS, Lakatta EG, et al. Study of the mechanisms of hydrogen peroxide and hydroxyl free radical-induced cellular injury and calcium overload in cardiac myocytes. J Biol Chem 1991; 266: 2354-61
64. Kaczorowski GJ, Slaughter RS, King VF, et al. Inhibitors of sodium-calcium exchange: identification and development of probes of transport activity. Biochim Biophys Acta 1989; 988: 287-302
65. Siegl PKS, Cragoe EJ, Trumble MJ, et al. Inhibition of Na+/Ca2+ exchange in membrane vesicle and papillary muscle preparations from guinea pig heart by analogs of amiloride. Proc Natl Acad Sci U S A 1984; 81: 3238-42
66. Murphy E, Perlman M, London RE, et al. Amiloride delays the ischemia-induced rise in cytosolic free calcium. Circ Res 1991; 68: 1250-8
67. Yoshizumi M, Kitagawa T, Masuda Y, et al. Effect of amiloride on ischaemia and reperfusion injury in isolated, perfused rat hearts. Scand Cardiovasc J 1998; 32: 167-72
68. Otani H, Kato Y, Ko T, et al. Effects of amiloride and an analogue on ventricular arrhythmias, contracture and cellular injury during reperfusion in isolated and perfused guinea pig heart. Jpn Circulation J 1991; 55: 845-56
69. Duff HJ, Lester WM, Rahmberg M. Antiarrhythmic and electrophysiological activity in the dog. Circulation 1988; 78: 1469-77
70. Lotan CS, Miller SK, Pohost GM, et al. Amiloride in ouabain-induced acidification, inotropy and arrhythmia: 23Na & 31PNMR in perfused hearts. J Mol Cell Cardiol 1992; 24: 243-57
71. Bieleford DR, Hadley RW, Vassilev PM, et al. Membrane electrical properties of vesicular sodium-calcium exchange inhibitors in single atrial myocytes. Circ Res 1986; 59: 381-9
72. Kleyman TR, Cragoe EJ. Amiloride and its analogs as tools in the study of ion transport. J Membr Biol 1988; 105: 1-21
73. Slaughter RS, Garcia ML, Cragoe Jr EJ, et al. Inhibition of sodium-calcium exchange in cardiac sarcolemmal vesicles: 1. mechanism of inhibition by amiloride analogues. Biochemistry 1988; 27: 2403-9
74. Murata Y, Harada K, Nakajima F, et al. Non-selective effects of amiloride and its analogues on ion transport systems and their cytotoxicities in cardiac myocytes. Jpn J Pharmacol 1995; 68: 279-85
75. Watano T, Kimura J, Morita T, et al. A novel antagonist, No. 7943, of the Na+/Ca2+ exchange current in guinea-pig cardiac ventricular cells. Br J Pharmacol 1996; 119: 555-63
76. Lipp P, Port L. Voltage dependence of sodium-calcium exchange current in guinea-pig atrial myocytes determined by means of an inhibitor. J Physiol 1988; 403: 355-66
77. Bush LR, Kaczorowski GJ, Siegl KS. Antiarrhythmic properties of dichlorobenzamil, a sodium-calcium exchange inhibitor. Circulation 1985; 72: 111-313
78. Murphy JG, Smith TW, Marsh JD. Mechanisms of reoxygenation-induced calcium overload in cultured chick embryo heart cells. Am J Physiol 1988; 254: H1133-41
79. Floreani M, Tessari P, Debetto P, et al. Effects of N-chlorobenzyl analogues of amiloride on myocardial contractility, Na-Ca-exchange carrier and other cardiac enzymatic activities. Naunyn Schmiedebergs Arch Pharmacol 1987; 336: 661-9
80. Bollensdorf C, Zimmer T, Benndorf K. Amiloride derivatives are potent blockers of KATP channels. Naunyn Schmiedebergs Arch Pharmacol 2001; 364: 351-8
81. Wettwer E, Himmel H, Ravens U. Amiloride derivatives as blockers of Na+/Ca2+ exchange: effects on mechanical and electrical function of guinea-pig myocardium. Pharmacol Toxicol 1992; 71: 95-102
82. de la Pena P, Reeves P. Inhibition and activation of Na+/Ca2+ exchange activity by quinacrine. Am J Physiol 1987; 252: C24-9
83. Han X, Ferrier GR. Contribution of Na+-Ca2+ exchange to stimulation of transient inward current by isoproterenol in rabbit cardiac Purkinje fibers. Circ Res 1995; 76: 664-74
84. Garcia ML, Slaughter RS, King VF, et al. Inhibition of sodium-calcium exchange in cardiac sarcolemmal membrane vesicles. Biochemistry 1998; 27: 2410-5
85. Li Z, Nicoll DA, Collins A, et al. Identification of a peptide inhibitor of the cardiac sarcolemmal Na+-Ca2+ exchanger. J Biol Chem 1991; 266: 1014-20
86. Chin TK, Spitzer KW, Philipson KD, et al. The effect of exchanger inhibitory peptide (XIP) on sodium-calcium exchange current in guinea pig ventricular cells. Circ Res 1993; 72: 497-503
87. Iwamoto T, Watano T, Shigekawa M. A novel isothiourea derivative selectively inhibits the reverse mode of Na+/Ca2+ exchange in cells expressing NCX1. J Biol Chem 1996; 271: 22391-7
88. Satoh H, Ginsburg KS, Qing K, et al. KB-R7943 of Ca2 influx via Na/Ca2 exchange does not alter twitches or glycoside inotropy but prevents Ca2 overload in rat ventricular myocytes. Circulation 2000; 101: 1441-6
89. Fujita S, Endoh M. Influence of a Na+-H+ exchange inhibitor ethylisopropylamiloride, a Na+-Ca2+ exchange inhibitor KB-R7943 and their combination on the increases in contractility and Ca2+ transient induced by angiotensin II in isolated adult rabbit ventricular myocytes. Naunyn Schmiedebergs Arch Pharmacol 1999; 360: 575-84
90. Yang H-T, Sakurai K, Sugawara H, et al. Role of Na+/Ca2+ exchange in endothelin- 1-induced increases in Ca2+ transient and contractility in rabbit ventricular myocytes: pharmacological analysis with KB-R7943. Br J Pharmacol 1999; 126: 1785-95
91. Mukai M, Terada H, Sugiyama S, et al. Effects of selective inhibitor of Na+/Ca2+ exchange, KB-R7943, on reoxygenation-induced injuries in guinea pig papillary muscles. J Cardiovasc Pharmacol 2000; 35: 121-8
92. Ladilov Y, Haffner C, Balser-Schäfer H, et al. Cardioprotective effects of KB-R7943: a novel inhibitor of the reverse mode of Na+/Ca2+ exchanger. Am J Physiol 1999; 276: H1868-76
93. Nakamura A, Harada K, Sugimoto H, et al. Effects of KB-7943, a novel Na+/Ca2+ exchange inhibitor, on myocardial ischemia/reperfusion injury. Nippon Yakurigaku Zasshi 1998; 111: 105-15
94. Imahashi K, Kusuoka H, Hashimoto K, et al. Intracellular sodium accumulation during ischemia as the substrate for reperfusion injury. Circ Res 1999; 84: 1401-6
95. Elias CL, Lukas A, Shurraw S, et al. Inhibition of Na+/Ca2+ exchange by KB-R7943: transport mode selectivity and anti-arrhythmic consequences. Am J Physiol 2001; 281: H1334-45
96. Lu HR, Yang P, Remeysen P, et al. Ischemia/reperfusion-induced arrhythmias in anaesthetized rats: a role of Na+ and Ca2+ influx. Eur J Pharmacol 1999; 365: 233-9
97. Yamamura K, Tani M, Hasegawa H, et al. Very low dose of the Na+/Ca2+ exchange inhibitor, KB-7943, protects ischemic reperfused aged Fischer 344 rat hearts: considerable strain difference in the sensitivity to KB-R7943. Cardiovasc Res 2001; 52: 397-406
98. Kurogouchi F, Furukawa Y, Zhao D, et al. A Na+/Ca+ exchanger inhibitor, KB-R7943, caused negative inotropic responses and negative followed by positive chronotropic responses in isolated, blood-perfused dog heart preparations. Jpn J Pharmacol 2000; 82: 155-63
99. Despa S, Islam MA, Pogwizd SM, et al. Intracellular [Na+] and Na+ pump rate in rat and rabbit ventricular myocytes. J Physiol 2002; 539: 133-43
100. Bers DM. Cardiac Na/Ca exchange function in rabbit, mouse and man: what's the difference?. J Mol Cell Cardiol 2002; 34: 364-73
101. Kimura J, Watano T, Kawahara M, et al. Direction-independent block of bi-directional Na+/Ca2+ exchange current by KB-R7943 in guinea-pig cardiac myocytes. Br J Pharmacol 1999; 128: 969-74
102. Tanaka H, Nishimaru K, Aikawa T, et al. Effect of SEA0400, a novel inhibitor of sodium-calcium exchanger, on myocardial ionic currents. Br J Pharmacol 2002; 135: 1096-100
103. Matsuda T, Arakawa N, Takuma K, et al. SEA0400, a novel and selective inhibitor of the Na+-Ca2+ exchanger, attenuates reperfusion injury in the in vitro and in vivo cerebral ischemic models. J Pharmacol Exp Ther 2001; 298: 249-56
104. Reuter H, Henderson SA, Han T, et al. Knockout mice for pharmacological screening: testing the specificity of Na+-Ca2+ exchange inhibitors. Circ Res 2002; 91: 90-2
105. Packer M, Carver JR, Rodeheffer RJ, et al. Effects of oral milrinone on mortality in severe chronic heart failure. N Engl J Med 1991; 325: 1468-75
106. Hasenfuss G. Alterations of calcium-regulatory proteins in heart failure. Cardiovasc Res 1998; 37: 279-89
107. Puglisi JL, Bers DM. LabHEART: an interactive computer model of rabbit ventricular myocytes ion channels and Ca transport. Am J Physiol 2001; 281: C2049-60
108. Luo C-H, Rudy Y. A dynamic model of the cardiac ventricular action potential: I. simulations of ionic currents and concentration changes. Circ Res 1994; 74: 1071-96
109. Priebe L, Beuckelmann DJ. Simulation study of cellular electric properties in heart failure. Circ Res 1998; 82: 1206-23
110. Winslow RL, Rice JJ, Jaffri S, et al. Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure: II. model studies. Circ Res 1999; 84: 571-86