Novel therapeutic approaches for heart failure by normalizing calcium cycling

Nature Reviews Drug Discovery

Volumn 3, Issue 7, 2004, Pages 565-573

  Wehrens, Xander H T ^a   Marks, Andrew R ^a  

^a Columbia Univ Coll Physicians/Surg ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; 4 [3 (4 BENZYL 1 PIPERIDINYL)PROPIONYL] 2,3,4,5 TETRAHYDRO 7 METHOXY 1,4 BENZOTHIAZEPINE; ADENOSINE TRIPHOSPHATASE (CALCIUM); BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCINEURIN; CALCIUM CHANNEL L TYPE; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE RECEPTOR STIMULATING AGENT; NOLOMIROLE; PARVOVIRUS VECTOR; PHOSPHODIESTERASE INHIBITOR; PHOSPHOLAMBAN; PLACEBO; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; RYANODINE RECEPTOR; SODIUM CALCIUM EXCHANGE PROTEIN; VOLTAGE GATED CALCIUM CHANNEL;

CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CAUSE OF DEATH; CONGESTIVE HEART FAILURE; DIASTOLE; DRUG MECHANISM; EXCITATION CONTRACTION COUPLING; GENE MUTATION; GENE THERAPY; HEART ARRHYTHMIA; HEART VENTRICLE CONTRACTILITY; HUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SARCOPLASMIC RETICULUM; SIDE EFFECT; SUDDEN DEATH; SYMPATHETIC TONE; SYSTOLE;

EID: 3543134142     PISSN: 14741776     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrd1440     Document Type: Review

References (118)

1. Hunt, S.A. et al. ACC/AHA guidelines for the evaluation and management of chronic heart failure in the adult: executive summary. J. Am. Coll. Cardiol. 38, 2101-2113 (2001).
2. 2+ content in isolated failing and nonfailing human myocardium. Circ. Res. 85, 38-46 (1999).
3. Bers, D. M. Cardiac excitation-contraction coupling. Nature 415, 198-205 (2002).
4. Fill, M. & Copello, J. A. Ryanodine receptor calcium release channels. Physiol. Rev. 82, 893-922 (2002).
5. Wehrens, X. H. & Marks, A. R. Altered function and regulation of cardiac ryanodine receptors in cardiac disease. Trends Biochem. Sci. 28, 671-678 (2003).
6. 2+ release from the sarcoplasmic reticulum in guinea-pig ventiricular myocytes. J. Physiol. 508, 439-451 (1998).
7. 2+ exchange. Circ. Res. 81, 1034-1044 (1997).
8. Fabiato, A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol. 245, C1-C14 (1983).
9. Koss, K. L., Grupp, I. L. & Kranias, E. G. The relative phospholamban and SERCA2 ratio: a critical determinant of myocardial contractility. Basic Res. Cardiol. 92 (Suppl. 1), 17-24 (1997).
10. Jones, L. R., Simmerman, H. K., Wilson, W. W., Gurd, F. R. & Wegener, A. D. Purification and characterization of phospholamban from canine cardiac sarcoplasmic reticulum. J. Biol. Chem. 260, 7721-7730 (1985).
11. Bers, D. M. & Bridge, J. H. Relaxation of rabbit ventricular muscle by Na-Ca exchange and sarcoplasmic reticulum calcium pump. Ryanodine and voltage sensitivity. Circ. Res. 65, 334-342 (1989).
12. Marx, S. O. et al. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101, 365-376 (2000).
13. 2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ. Res. 94, e61-e70 (2004).
14. Braz, J. C. et al. PKC-α regulates cardiac contractility and propensity toward heart failure. Nature Med. 10, 248-254 (2004).
15. Rockman, H. A., Koch, W. J. & Lefkowitz, R. J. Seven-transmembrane-spanning receptors and heart function. Nature 415, 206-212 (2002).
16. Gomez, A. M. et al. Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science 276, 800-806 (1997).
17. Dzhura, I., Wu, Y., Colbran, R. J., Balser, J. R. & Anderson, M. E. Calmodulin kinase determines calcium-dependent facilitation of L-type calcium channels. Nature Cell Biol. 2, 173-177 (2000).
18. DeSantiago, J., Maier, L. S. & Bers, D. M. Frequency-dependent acceleration of relaxation in the heart depends on CaMKII, but not phospholamban. J. Mol. Cell. Cardiol. 34, 975-984 (2002).
19. 2+ release. Circ. Res. 92, 904-911 (2003).
20. 2+ current: a cellular mechanism for long Q-T arrhythmias. Am. J. Physiol. 276, H2168-H2178 (1999).
21. 2+-calmodulin-dependent protein kinase system. J. Mol. Cell. Cardiol. 24, 387-396 (1992).
22. Hagemann, D. et al. Frequency-encoding Thr17 phospholamban phosphorylation is independent of Ser16 phosphorylation in cardiac myocytes. J. Biol. Chem. 275, 22532-22536 (2000).
23. Hagemann, D. & Xiao, R. P. Dual site phospholamban phosphorylation and its physiological relevance in the heart. Trends Cardiovasc. Med. 12, 51-56 (2002).
24. Dempsey, E. C. et al. Protein kinase C isozymes and the regulation of diverse cell responses. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L429-L438 (2000).
25. Wang, J., Liu, X., Arneja, A. S. & Dhalla, N. S. Alterations in protein kinase A and protein kinase C levels in heart failure due to genetic cardiomyopathy. Can. J. Cardiol. 15, 683-690 (1999).
26. Sugden, P. H. & Bogoyevitch, M. A. Intracellular signalling through protein kinases in the heart. Cardiovasc. Res. 30, 478-492 (1995).
27. Pass, J. M. et al. Enhanced PKCβ II translocation and PKC-P II-RACK1 interactions in PKCE-induced heart failure: a role for RACK1. Am. J. Physiol. Heart Circ. Physiol. 281, H2500-H2510 (2001).
28. Tunwell, R. E. et al. The human cardiac muscle ryanodine receptor-calcium release channel: identification, primary structure and topological analysis. Biochem. J. 318, 477-487 (1996).
29. 2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic, reticulum, J. Biol. Chem. 265, 13472-13483 (1990).
30. Chu, A., Sumbilla, C., Inesi, G., Jay, S. D. & Campbell, K. P. Specific association of calmodulin-dependent protein kinase and related substrates with the junctional sarcoplasmic reticulum of skeletal muscle. Biochemistry 29, 5899-5905 (1990).
31. Brillantes, A.-M. B. et al. FKBP12 Optimizes function of the cloned expressed calcium release channel (ryanodine receptor). Biophys. J. 66, A19 (1994).
32. Marx, S. O. et al. Phosphorylation-dependent regulation of ryanodine receptors. A novel role for leucine/isoleucine zippers. J. Cell. Biol. 153, 699-708 (2001).
33. Currie, S., Loughrey, C. M., Craig, M. A. & Smith, G. L. Calcium/calmodulin-dependent protein kinase IIδ associates with the ryanodine receptor complex and regulates channel function in rabbit heart. Biochem. J. 377, 357-366 (2004).
34. Meyers, M. B. et al. Association of sorcin with the cardiac ryanodine receptor. J. Biol. Chem. 270, 26411-26418 (1995).
35. Zhang, L., Kelley, J., Schmeisser, G., Kobayashi, Y. M. & Jones, L. R. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J. Biol. Chem. 272, 23389-23397 (1997).
36. Flucher, B. E. et al. Triad formation: organization and function of the sarcoplasmic reticulum calcium release channel and triadin in normal and dysgenic muscle in vitro. J. Cell. Biol. 123, 1161-1174 (1993).
37. Collins, J., Tarcsafalvi, A. & Ikemoto, N. Identification of a region of calsequestrin that binds to the junctional face membrane of sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 167, 189-193 (1990).
38. Viatchenko-Karpinski, S. et al. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin. Circ. Res. 94, 471-477 (2004).
39. Wehrens, X. H. et al. FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 113, 829-840 (2003).
40. 2+ release channels (ryanodine receptors). Science 281, 818-821 (1998).
41. Gaburjakova, M. et al. FKBP12 binding modulates ryanodine receptor channel gating. J. Biol. Chem. 276, 16931-16935 (2001).
42. Hain, J., Onoue, H., Mayrleitner, M., Fleischer, S. & Schindler, H. Phosphorylation modulates the function of the calcium release channel of sarcoplasmic reticulum from cardiac muscle. J. Biol. Chem. 270, 2074-2081 (1995).
43. 2+ and phosphorylation. Science 267, 1997-2000 (1995).
44. Lokuta, A. J., Rogers, T. B., Lederer, W. J. & Valdivia, H. H. Modulation of cardiac ryanodine receptors of swine and rabbit by a phosphorylation-dephosphorylation mechanism. J. Phys. 487, 609-622 (1995).
45. 2+. Cell Calcium 21, 283-290 (1997 ).
46. Terentyev, D., Viatchenko-Karpinski, S., Gyorke, I., Terentyeva, R. & Gyorke, S. Protein phosphatases decrease sarcoplasmic reticulum calcium content by stimulating calcium release in cardiac myocytes. J. Physiol. 552, 109-118 (2003).
47. Beuckelmann, D., Nabauer, M. & Erdmann, E. Intracellular calcium handling in isolated ventricular myocytes from patients with terminal heart failure. Circulation 85, 1046-1055 (1992).
48. Beuckelmann, D. J., Nabauer, M., Kruger, C. & Erdmann, E. Altered diastolic Ca handling in human ventricular myocytes from patients with terminal heart failure. Am. Heart J. 129, 684-689 (1995).
49. Kluger, J., Cody, R. J. & Laragh, J. H. The contributions of sympathetic tone and the renin-angiotensin system to severe chronic congestive heart failure: response to specific inhibitors (prazosin and captopril). Am. J. Cardiol. 49, 1667-1674 (1982).
50. Cohn, J. N. et al. Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure. N. Engl. J. Med. 311, 819-823 (1984).
51. 1 receptor messenger RNA abundance in the failing human heart. J. Clin. Invest. 92, 2737-2745 (1993).
52. 2-adrenergic receptor to different G proteins by protein kinase A. Nature 390, 88-91 (1997).
53. 1-adrenergic receptors in failing human heart. Circulation 87, 454-463 (1993).
54. 2+ channel density and regulation are altered in failing human ventricular myocytes and recover after support with mechanical assist devices. Circ. Res. 91, 517-524 (2002).
55. 2+ exchanger in failing pig myocytes. Circ. Res. 92, 897-903 (2003).
56. Brillantes, A., Allen, P. & Marks, A. Molecular cloning of the human cardiac calcium release channel cDNA: expression studies in end-stage human heart Failure. Circulation 84 (Suppl. II), 442 (1991).
57. 2+ transient of failing human ventricular myocytes. Circ. Res. 84, 435-444 (1999).
58. Lowes, B. D. et al. Myocardial gene expression in dilated cardiomyopathy treated with β-blocking agents. N. Engl. J. Med. 346, 1357-1365 (2002).
59. Reiken, S. et al. Protein kinase A phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. Role of phosphatases and response to isoproterenol. J. Biol. Chem. 278, 444-453 (2003).
60. 2+ leak through ryanodine receptor in heart failure. Circulation 102, 2131-2136 (2000).
61. MERIT-HF. Effect of metoprolol CR/XL in chronic heart failure: Metoprolol CR/XL Randomised Intervention Trial in Congestive Heart Failure (MERIT-HF). Lancet 353, 2001-2007 (1999).
62. Packer, M. et al. The effect of carvedilol on morbidity and mortality in patients with chronic heart failure. U. S. Carvedilol Heart Failure Study Group. N. Engl. J. Med. 334, 1349-1355 (1996).
63. CIBIS-II. The Cardiac Insufficiency Bisoprolol Study II (CIBIS-II): a randomised trial. Lancet 353, 9-13 (1999).
64. Reiken, S. et al. Beta-blockers restore calcium release channel function and improve cardiac muscle performance in human heart failure. Circulation 107, 2459-2466 (2003).
65. Reiken, S. et al. β-adrenergic receptor blockers restore cardiac calcium release channel (ryanodine receptor) structure and function in heart failure. Circulation 104, 2843-2848 (2001).
66. Doi, M. et al. Propranolol prevents the development of heart failure by restoring RKBP12.6-mediated stabilization of ryanodine receptor. Circulation 105, 1374-1379 (2002).
67. 2 agonist, blunts norepinephrine excretion and cardiac fibrosis in pressure overload. Cardiovasc. Drug Ther. 15, 131-138 (2001).
68. Bayes, M., Rabasseda, X. & Prous, J. R. Gateways to clinical trials. Methods Find. Exp. Clin. Pharmacol. 25, 565-597 (2003).
69. 1-adrenergic receptor. Involvement of G-protein-coupled receptor kinases and cAMP-dependent protein kinase. J. Biol. Chem. 270, 17953-17961 (1995).
70. Harding, V. B., Jones, L. R., Lefkowitz, R. J., Koch, W. J. & Rockman, H. A. Cardiac β-ARK1 inhibition prolongs survival and augments beta-blocker therapy in a mouse model of severe heart failure. Proc. Natl Acad. Sci. USA 98, 5809-5814 (2001).
71. Rockman, H. A. et al. Expression of a β-adrenergic receptor kinase 1 inhibitor prevents the development of myocardial failure in gene-targeted mice. Proc. Natl Acad. Sci. USA 95, 7000-7005 (1998).
72. Gullestad, L. et al. Effect of metoprolol CR/XL on exercise tolerance in chronic heart failure - a substudy to the MERIT-HF trial. Eur. J. Heart Fail. 3, 463-468 (2001).
73. White, M. et al. Role of β-adrenergic receptor downregulation in the peak exercise response in patients with heart failure due to idiopathic dilated cardiomyopathy. Am. J. Cardiol. 76, 1271-1276 (1995).
74. Most, P. & Koch, W. J. Sealing the leak, healing the heart. Nature Med. 9, 993-934 (2003).
75. Wehrens, X. H. et al. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science 304, 292-296 (2004).
76. Kohno, M. et al. A new cardioprotective agent, JTV519, improves defective channel gating of ryanodine receptor in heart failure. Am. J. Physiol. Heart Circ. Physiol. 284, H1035-H1042 (2003).
77. Yano, M. et al. RKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation 107, 477-484 (2003).
78. Hajjar, R. J. et al. Modulation of ventricular function through gene transfer in vivo. Proc. Natl Acad. Sci. USA 95, 5251-5256 (1998).
79. Minamisawa, S. et al. Chronic phospholamban-sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated cardiomyopathy. Cell 99, 313-322 (1999).
80. 2+-ATPase overexpression by adenovirus mediated gene transfer and in transgenic mice. Cardiovasc. Res. 37, 360-366 (1998).
81. 2+-ATPase by gingerol analogous. Biol. Pharm. Bull. 19, 1377-1379 (1996).
82. 2+-ATPase and phospholamban interaction. Eur. J. Biochem. 247, 801-809 (1997).
83. Volders, P. G. et al. Similarities between early and delayed after depolarizations induced by isoproterenol in canine ventricular myocytes. Cardiovasc. Res. 34, 348-359 (1997).
84. Hoshijima, M. et al. Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nature Med. 8, 864-871 (2002).
85. Iwanaga, Y. et al. Chronic phospholamban inhibition prevents progressive cardiac dysfunction and pathological remodeling after infarction in rats. J. Clin. Invest. 113, 727-736 (2004).
86. del Monte, F., Harding, S. E., Dec, G. W., Gwathmey, J. K. & Hajjar, R. J. Targeting phospholamban by gene transfer in human heart failure. Circulation 105, 904-907 (2002).
87. Haghighi, K. et al. Human phospholamban null results in lethal dilated cardiomyopathy revealing a critical difference between mouse and human. J. Clin. Invest 111, 869-876 (2003).
88. 2+-sensitive isoforms in the failing human heart. Circulation 99, 384-391 (1999).
89. Wang, J., Liu, X., Sentex, E., Takeda, N. & Dhalla, N. S. Increased expression of protein kinase C isoforms in heart failure due to myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 284, H2277-H2287 (2003).
90. Hahn, H. S. et al. Protein kinase Cα negatively regulates systolic and diastolic function in pathological hypertrophy. Circ. Res. 93, 1111-1119 (2003).
91. Vlahos, C. J., McDowell, S. A. & Clerk, A. Kinases as therapeutic targets for heart failure. Nature Rev. Drug Discov. 2, 99-113 (2003).
92. Mattiello, J. A., Margulies, K. B., Jeevanandam, V. & Houser, S. R. Contribution of reverse-mode sodium-calcium exchange to contractions in failing human left ventricular myocytes. Cardiovasc. Res. 37, 424-431 (1998).
93. 2+ exchange in cells expressing NCX1. J. Biol. Chem. 271, 22391-22397 (1996).
94. 2+ exchange activity in canine pacing-induced heart failure. Circ. Res. 87, 690-698 (2000).
95. 2+ exchange: molecular and pharmacological aspects. Circ. Res. 88, 864-876 (2001).
96. 2+ leak from the sarcoplasmic reticulum and increases contractility Circ. Res. 88, 188-194 (2001).
97. Miyamoto, M. I. et al. Adenoviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc. Natl Acad. Sci. USA 97, 793-798 (2000).
98. Ennis, I. L., Li, R. A., Murphy, A. M., Marban, E. & Nuss, H. B. Dual gene therapy with SERCA1 and Kir2.1 abbreviates excitation without suppressing contractility. J. Clin. Invest. 109, 393-400 (2002).
99. Ji, Y., Loukianov, E., Loukianova, T., Jones, L. R. & Periasamy M. SERCA1a can functionally substitute for SERCA2a in the heart. Am. J. Physiol. 276, H89-H97 (1999).
100. 2+ exchanger inhibitors SEA0400 and KB-R7943. Am. J. Physiol. Heart Circ. Physiol. 284, H903-H910 (2003).
101. Wehrens, X. H., Vos, M. A., Doevendans, P. A. & Wellens, H. J. Novel insights in the congenital long QT syndrome. Ann. Intern. Med. 137, 981-992 (2002).
102. Marks, A. R., Priori, S., Memmi, M., Kontula, K. & Laitinen, P. J. Involvement of the cardiac ryanodine receptor/calcium release channel in catecholaminergic polymorphic ventricular tachycardia. J. Cell. Physiol. 190, 1-6 (2002).
103. Leenhardt, A. et al. Catecholaminergic polymorphic ventricular tachycardia in children. A 7-year follow-up of 21 patients. Circulation 91, 1512-1519 (1995).
104. Laitinen, P. J. et al. Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation 103, 485-490 (2001).
105. Prior, S. G. et al. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 103, 196-200 (2001).
106. Fisher, J. D., Krikler D. & Hallidie-Smith, K. A. Familial polymorphic ventricular arrhythmias: a quarter century of successful medical treatment based on serial exercise-pharmacologic testing. J. Am. Coll. Cardiol. 34, 2015-2022 (1999).
107. Swan, H. et al. Arrhythmic disorder mapped to chromosome 1q42-q43 causes malignant polymorphic ventricular tachycardia in structurally normal hearts. J. Am. Coll. Cardiol. 34, 2035-2042 (1999).
108. George, C. H., Higgs, G. V. & Lai, F. A. Ryanodine receptor mutations associated with stress-induced ventricular tachycardia mediate increased calcium release in stimulated cardiomyocytes. Circ. Res. 93, 531-540 (2003).
109. 2+ release channel (ryanodine receptor) mutant associated with ventricular tachycardia and sudden death. Circ. Res. 91, 218-225 (2002).
110. Kaneko, N. New 1,4-benzothiazepine derivative, K201, demonstrates cardioprotective effects against sudden cardiac cell death and intracellular calcium blocking action. Drug Dev. Res. 33, 429-438 (1994).
111. Kaneko, N., Ago, H., Matsuda, R., Inagaki, E. & Miyano, M. Crystal structure of annexin V with its ligand K-201 as a calcium channel activity inhibitor. J. Mol. Biol. 274, 16-20 (1997).
112. Kawabata, H., Ryomoto, T. & Ishikawa, K. Effect of a novel cardioprotective agent, JTV-519, on metabolism, contraction and relaxation in the ischemia-reperfused rabbit heart. Jpn Circ. J. 64, 772-776 (2000).
113. 2+ overload in isolated rat hearts. Cardiovasc. Drugs Ther. 14, 489-495 (2000).
114. Inagaki, K. et al. Anti-ischemic effect of a novel cardioprotective agent, JTV519, is mediated through specific activation of delta-isoform of protein kinase C in rat ventricular myocardium. Circulation 101, 797-804 (2000).
115. Ito, K. et al. JTV-519, a novel cardioprotective agent, improves the contractile recovery after ischaemia-reperfusion in coronary perfused guinea-pig ventricular muscles. Br. J. Pharmacol. 130, 767-76 (2000).
116. Nakaya, H., Furusawa, Y., Ogura, T., Tamagawa, M. & Uemura, H. Inhibitory effects of JTV-519, a novel cardioprotective drug, on potassium currents and experimental atrial fibrillation in guinea-pig hearts. Br. J. Pharmacol. 131, 1363-1372 (2000).
117. Kumagai, K., Nakashima, H., Gondo, N. & Saku, K. Antiarrhythmic effects of JTV-519, a novel cardioprotective drug, on atrial fibrillation/flutter in a canine sterile pericarditis model. J. Cardiovasc. Electrophysiol. 14, 880-884 (2003).
118. 2+ release causes myocyte depolarization. Underlying mechanism and threshold for triggered action potentials. Circ. Res. 87, 774-780 (2000).