Type 2 ryanodine receptor: A novel therapeutic target in myocardial ischemia/reperfusion

Pharmacology and Therapeutics

Volumn 138, Issue 3, 2013, Pages 323-332

  Fauconnier, Jérémy ^a   Roberge, Stéphanie ^a   Saint, Nathalie ^a   Lacampagne, Alain ^a  

^a INSERM   (France)

Author keywords

Calcium; Heart; Mitochondria; Oxidative stress; Reperfusion injuries

Indexed keywords

CALCIUM; RYANODINE RECEPTOR 2;

CALCIUM TRANSPORT; CYTOSOL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; REVIEW; SARCOPLASMIC RETICULUM;

ANIMALS; CALCIUM; HUMANS; MITOCHONDRIA, HEART; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM;

EID: 84877575360     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2013.01.015     Document Type: Review

References (153)

1. Y. Abdallah, S.A. Kasseckert, W. Iraqi, M. Said, T. Shahzad, and A. Erdogan Interplay between Ca2+ cycling and mitochondrial permeability transition pores promotes reperfusion-induced injury of cardiac myocytes J Cell Mol Med 15 2011 2478 2485
2. T. Akita, T. Abe, S. Kato, I. Kodama, and J. Toyama Protective effects of diltiazem and ryanodine against ischemia-reperfusion injury in neonatal rabbit hearts J Thorac Cardiovasc Surg 106 1993 55 66
3. D.C. Andersson, M.J. Betzenhauser, S. Reiken, A.C. Meli, A. Umanskaya, and W. Xie Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging Cell Metab 14 2011 196 207
4. D.C. Andersson, and A.R. Marks Fixing ryanodine receptor Ca leak - a novel therapeutic strategy for contractile failure in heart and skeletal muscle Drug Discov Today Dis Mech 7 2010 e151 e157
5. B. Antoniu, D.H. Kim, M. Morii, and N. Ikemoto Inhibitors of Ca2+ release from the isolated sarcoplasmic reticulum. I. Ca2+ channel blockers Biochim Biophys Acta 816 1985 9 17
6. P. Aracena, W. Tang, S.L. Hamilton, and C. Hidalgo Effects of S-glutathionylation and S-nitrosylation on calmodulin binding to triads and FKBP12 binding to type 1 calcium release channels Antioxid Redox Signal 7 2005 870 881
7. L. Argaud, O. Gateau-Roesch, L. Augeul, E. Couture-Lepetit, J. Loufouat, and L. Gomez Increased mitochondrial calcium coexists with decreased reperfusion injury in postconditioned (but not preconditioned) hearts Am J Physiol Heart Circ Physiol 294 2008 H386 H391
8. L. Argaud, O. Gateau-Roesch, O. Raisky, J. Loufouat, D. Robert, and M. Ovize Postconditioning inhibits mitochondrial permeability transition Circulation 111 2005 194 197
9. D.E. Atsma, E.M. Bastiaanse, A. Jerzewski, L.J. Van der Valk, and A. Van der Laarse Role of calcium-activated neutral protease (calpain) in cell death in cultured neonatal rat cardiomyocytes during metabolic inhibition Circ Res 76 1995 1071 1078
10. D.M. Balshaw, N. Yamaguchi, and G. Meissner Modulation of intracellular calcium-release channels by calmodulin J Membr Biol 185 2002 1 8
11. A. Bandyopadhyay, D.W. Shin, J.O. Ahn, and D.H. Kim Calcineurin regulates ryanodine receptor/Ca(2+)-release channels in rat heart Biochem J 352 Pt. 1 2000 61 70
12. J.A. Beavo Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms Physiol Rev 75 1995 725 748
13. A.M. Bellinger, S. Reiken, M. Dura, P.W. Murphy, S.X. Deng, and D.W. Landry Remodeling of ryanodine receptor complex causes "leaky" channels: a molecular mechanism for decreased exercise capacity Proc Natl Acad Sci U S A 105 2008 2198 2202
14. K. Boengler, G. Heusch, and R. Schulz Mitochondria in postconditioning Antioxid Redox Signal 14 2011 863 880
15. R. Bolli, L. Becker, G. Gross, R. Mentzer Jr.; D. Balshaw, and D.A. Lathrop Myocardial protection at a crossroads: the need for translation into clinical therapy Circ Res 95 2004 125 134
16. S. Boncompagni, A.E. Rossi, M. Micaroni, G.V. Beznoussenko, R.S. Polishchuk, and R.T. Dirksen Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures Mol Biol Cell 20 2009 1058 1067
17. M. Boutjdir, N. el-Sherif, and W.B. Gough Effects of caffeine and ryanodine on delayed afterdepolarizations and sustained rhythmic activity in 1-day-old myocardial infarction in the dog Circulation 81 1990 1393 1400
18. R.W. Butcher, and E.W. Sutherland Adenosine 3′,5′-phosphate in biological materials. I. Purification and properties of cyclic 3′,5′-nucleotide phosphodiesterase and use of this enzyme to characterize adenosine 3′,5′-phosphate in human urine J Biol Chem 237 1962 1244 1250
19. W.F. Cai, T. Pritchard, S. Florea, C.K. Lam, P. Han, and X. Zhou Ablation of junctin or triadin is associated with increased cardiac injury following ischaemia/reperfusion Cardiovasc Res 94 2012 333 341
20. M.G. Chelu, S. Sarma, S. Sood, S. Wang, R.J. van Oort, and D.G. Skapura Calmodulin kinase II-mediated sarcoplasmic reticulum Ca2+ leak promotes atrial fibrillation in mice J Clin Invest 119 2009 1940 1951
21. H. Cheng, and W.J. Lederer Calcium sparks Physiol Rev 88 2008 1491 1545
22. P.K. Chohan, R.B. Singh, N.S. Dhalla, and T. Netticadan L-arginine administration recovers sarcoplasmic reticulum function in ischemic reperfused hearts by preventing calpain activation Cardiovasc Res 69 2006 152 163
23. T.J. Connelly, and R. Coronado Activation of the Ca2+ release channel of cardiac sarcoplasmic reticulum by volatile anesthetics Anesthesiology 81 1994 459 469
24. J.A. Copello, S. Barg, A. Sonnleitner, M. Porta, P. Diaz-Sylvester, and M. Fill Differential activation by Ca2+, ATP and caffeine of cardiac and skeletal muscle ryanodine receptors after block by Mg2+ J Membr Biol 187 2002 51 64
25. P.R. Crisostomo, G.M. Wairiuko, M. Wang, B.M. Tsai, E.D. Morrell, and D.R. Meldrum Preconditioning versus postconditioning: mechanisms and therapeutic potentials J Am Coll Surg 202 2006 797 812
26. I. Dimitrijevic, M.L. Edvinsson, Q. Chen, M. Malmsjo, P.O. Kimblad, and L. Edvinsson Increased expression of vascular endothelin type B and angiotensin type 1 receptors in patients with ischemic heart disease BMC Cardiovasc Disord 9 2009 40
27. U.D. Dincer Cardiac ryanodine receptor in metabolic syndrome: is JTV519 (K201) future therapy? Diabetes Metab Syndr Obes 5 2012 89 99
28. R.J. Domenech, G. Sanchez, P. Donoso, V. Parra, and P. Macho Effect of tachycardia on myocardial sarcoplasmic reticulum and Ca2+ dynamics: a mechanism for preconditioning? J Mol Cell Cardiol 35 2003 1429 1437
29. Z. Dong, P. Saikumar, J.M. Weinberg, and M.A. Venkatachalam Calcium in cell injury and death Annu Rev Pathol 1 2006 405 434
30. P. Donoso, G. Sanchez, R. Bull, and C. Hidalgo Modulation of cardiac ryanodine receptor activity by ROS and RNS Front Biosci 16 2011 553 567
31. E.F. du Toit, and L.H. Opie Antiarrhythmic properties of specific inhibitors of sarcoplasmic reticulum calcium ATPase in the isolated perfused rat heart after coronary artery ligation J Am Coll Cardiol 23 1994 1505 1510
32. A. Dulhunty, C. Haarmann, D. Green, and J. Hart How many cysteine residues regulate ryanodine receptor channel activity? Antioxid Redox Signal 2 2000 27 34
33. T. Eschenhagen Is ryanodine receptor phosphorylation key to the fight or flight response and heart failure? J Clin Invest 120 2010 4197 4203
34. J. Fauconnier, A.C. Meli, J. Thireau, S. Roberge, J. Shan, and Y. Sassi Ryanodine receptor leak mediated by caspase-8 activation leads to left ventricular injury after myocardial ischemia-reperfusion Proc Natl Acad Sci U S A 108 2011 13258 13263
35. J. Fauconnier, J. Thireau, S. Reiken, C. Cassan, S. Richard, and S. Matecki Leaky RyR2 trigger ventricular arrhythmias in Duchenne muscular dystrophy Proc Natl Acad Sci U S A 107 2010 1559 1564
36. C.R. Frasier, R.L. Moore, and D.A. Brown Exercise-induced cardiac preconditioning: how exercise protects your achy-breaky heart J Appl Physiol 111 2011 905 915
37. B.B. Fredholm Astra Award Lecture. Adenosine, adenosine receptors and the actions of caffeine Pharmacol Toxicol 76 1995 93 101
38. L. Gomez, M. Paillard, H. Thibault, G. Derumeaux, and M. Ovize Inhibition of GSK3beta by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion Circulation 117 2008 2761 2768
39. M. Griese, V. Perlitz, E. Jungling, and H. Kammermeier Myocardial performance and free energy of ATP-hydrolysis in isolated rat hearts during graded hypoxia, reoxygenation and high Ke+-perfusion J Mol Cell Cardiol 20 1988 1189 1201
40. W. Guo, and K.P. Campbell Association of triadin with the ryanodine receptor and calsequestrin in the lumen of the sarcoplasmic reticulum J Biol Chem 270 1995 9027 9030
41. Z.Y. Guo, Q. Jiao, S.T. Wang, M.H. Xu, and F.H. Gao Effect of ryanodine receptor 2 gene silencing on ischemia-reperfusion injury of rat myocardial cells Zhonghua Bing Li Xue Za Zhi 37 2008 760 764
42. S. Gyorke, and D. Terentyev Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease Cardiovasc Res 77 2008 245 255
43. G. Hajnoczky, G. Csordas, S. Das, C. Garcia-Perez, M. Saotome, and S. Sinha Roy Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis Cell Calcium 40 2006 553 560
44. D.J. Hausenloy, S. Lecour, and D.M. Yellon Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischemic postconditioning: two sides of the same coin Antioxid Redox Signal 14 2011 893 907
45. H. Hayashi, H. Terada, H. Katoh, and T.F. McDonald Prevention of reoxygenation-induced arrhythmias in guinea pig papillary muscles J Cardiovasc Pharmacol 27 1996 816 823
46. D.J. Hearse Reperfusion of the ischemic myocardium J Mol Cell Cardiol 9 1977 605 616
47. T.W. Hein, C. Zhang, W. Wang, C.I. Chang, N. Thengchaisri, and L. Kuo Ischemia-reperfusion selectively impairs nitric oxide-mediated dilation in coronary arterioles: counteracting role of arginase FASEB J 17 2003 2328 2330
48. J.S. Herland, F.J. Julian, and D.G. Stephenson Halothane increases Ca2+ efflux via Ca2+ channels of sarcoplasmic reticulum in chemically skinned rat myocardium J Physiol 426 1990 1 18
49. A.P. Hill, O. Kingston, and R. Sitsapesan Functional regulation of the cardiac ryanodine receptor by suramin and calmodulin involves multiple binding sites Mol Pharmacol 65 2004 1258 1268
50. S.R. Houser Does protein kinase a-mediated phosphorylation of the cardiac ryanodine receptor play any role in adrenergic regulation of calcium handling in health and disease? Circ Res 106 2010 1672 1674
51. P.A. Iaizzo, B.A. Johnson, K. Nagao, and W.J. Gallagher 4-chloro-m-cresol triggers malignant hyperthermia in susceptible swine at doses greatly exceeding those found in drug preparations Anesthesiology 90 1999 1723 1732
52. K. Inagaki, Y. Kihara, T. Izumi, and S. Sasayama The cardioprotective effects of a new 1,4-benzothiazepine derivative, JTV519, on ischemia/ reperfusion-induced Ca2+ overload in isolated rat hearts Cardiovasc Drugs Ther 14 2000 489 495
53. J. Jacobson, and M.R. Duchen Mitochondrial oxidative stress and cell death in astrocytes-requirement for stored Ca2+ and sustained opening of the permeability transition pore J Cell Sci 115 2002 1175 1188
54. S. Javadov, J.C. Hunter, G. Barreto-Torres, and R. Parodi-Rullan Targeting the mitochondrial permeability transition: cardiac ischemia-reperfusion versus carcinogenesis Cell Physiol Biochem 27 2011 179 190
55. R.B. Jennings, and K.A. Reimer Factors involved in salvaging ischemic myocardium: effect of reperfusion of arterial blood Circulation 68 1983 I25 I36
56. R.B. Jennings, H.M. Sommers, G.A. Smyth, H.A. Flack, and H. Linn Myocardial necrosis induced by temporary occlusion of a coronary artery in the dog Arch Pathol 70 1960 68 78
57. E. Kaftan, A.R. Marks, and B.E. Ehrlich Effects of rapamycin on ryanodine receptor/Ca(2+)-release channels from cardiac muscle Circ Res 78 1996 990 997
58. M.S. Kapiloff, N. Jackson, and N. Airhart mAKAP and the ryanodine receptor are part of a multi-component signaling complex on the cardiomyocyte nuclear envelope J Cell Sci 114 2001 3167 3176
59. T. Kawasaki, and M. Kasai Regulation of calcium channel in sarcoplasmic reticulum by calsequestrin Biochem Biophys Res Commun 199 1994 1120 1127
60. S. Kettlewell, P. Most, S. Currie, W.J. Koch, and G.L. Smith S100A1 increases the gain of excitation-contraction coupling in isolated rabbit ventricular cardiomyocytes J Mol Cell Cardiol 39 2005 900 910
61. E. Lam, M.M. Martin, A.P. Timerman, C. Sabers, S. Fleischer, and T. Lukas A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor J Biol Chem 270 1995 26511 26522
62. H.C. Lee Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP Physiol Rev 77 1997 1133 1164
63. S.E. Lehnart, M. Mongillo, A. Bellinger, N. Lindegger, B.X. Chen, and W. Hsueh Leaky Ca2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice J Clin Invest 118 2008 2230 2245
64. S.E. Lehnart, X.H. Wehrens, S. Reiken, S. Warrier, A.E. Belevych, and R.D. Harvey Phosphodiesterase 4D deficiency in the ryanodine-receptor complex promotes heart failure and arrhythmias Cell 123 2005 25 35
65. A.J. Lokuta, M.B. Meyers, P.R. Sander, G.I. Fishman, and H.H. Valdivia Modulation of cardiac ryanodine receptors by sorcin J Biol Chem 272 1997 25333 25338
66. C. Long, L.G. Cook, G.Y. Wu, and B.M. Mitchell Removal of FKBP12/12.6 from endothelial ryanodine receptors leads to an intracellular calcium leak and endothelial dysfunction Arterioscler Thromb Vasc Biol 27 2007 1580 1586
67. C.M. Loughrey, N. Otani, T. Seidler, M.A. Craig, R. Matsuda, and N. Kaneko K201 modulates excitation-contraction coupling and spontaneous Ca2+ release in normal adult rabbit ventricular cardiomyocytes Cardiovasc Res 76 2007 236 246
68. L. Lucats, L. Vinet, A. Bize, X. Monnet, D. Morin, and J.B. Su The inotropic adaptation during late preconditioning against myocardial stunning is associated with an increase in FKBP12.6 Cardiovasc Res 73 2007 560 567
69. D.H. MacLennan, and M.S. Phillips Malignant hyperthermia Science 256 1992 789 794
70. J.J. Marengo, C. Hidalgo, and R. Bull Sulfhydryl oxidation modifies the calcium dependence of ryanodine-sensitive calcium channels of excitable cells Biophys J 74 1998 1263 1277
71. S.O. Marx, S. Reiken, Y. Hisamatsu, M. Gaburjakova, J. Gaburjakova, and Y.M. Yang Phosphorylation-dependent regulation of ryanodine receptors: a novel role for leucine/isoleucine zippers J Cell Biol 153 2001 699 708
72. S.O. Marx, S. Reiken, Y. Hisamatsu, T. Jayaraman, D. Burkhoff, and N. Rosemblit PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts Cell 101 2000 365 376
73. A. Mattiazzi, C. Mundina-Weilenmann, L. Vittone, and M. Said Phosphorylation of phospholamban in ischemia-reperfusion injury: functional role of Thr17 residue Mol Cell Biochem 263 2004 131 136
74. A. Mattiazzi, L. Vittone, and C. Mundina-Weilenmann Ca2+ -calmodulin-dependent protein kinase phosphorylation of ryanodine receptor may contribute to the beta-adrenergic regulation of myocardial contractility independently of increases in heart rate Circ Res 103 2008 e10 e11 (author reply e12)
75. S.J. McGarry, and A.J. Williams Digoxin activates sarcoplasmic reticulum Ca(2+)-release channels: a possible role in cardiac inotropy Br J Pharmacol 108 1993 1043 1050
76. D.R. Meldrum Tumor necrosis factor in the heart Am J Physiol 274 1998 R577 R595
77. D.R. Meldrum, J.C. Cleveland Jr.; M.B. Mitchell, R.T. Rowland, A. Banerjee, and A.H. Harken Constructive priming of myocardium against ischemia-reperfusion injury Shock 6 1996 238 242
78. M.E. Mendelsohn, and R.H. Karas The protective effects of estrogen on the cardiovascular system N Engl J Med 340 1999 1801 1811
79. M.B. Meyers, V.M. Pickel, S.S. Sheu, V.K. Sharma, K.W. Scotto, and G.I. Fishman Association of sorcin with the cardiac ryanodine receptor J Biol Chem 270 1995 26411 26418
80. M. Miyamae, S.A. Camacho, M.W. Weiner, and V.M. Figueredo Attenuation of postischemic reperfusion injury is related to prevention of [Ca2+]m overload in rat hearts Am J Physiol 271 1996 H2145 H2153
81. K. Miyoshi, M. Taniguchi, S. Seki, and S. Mochizuki Effects of magnesium and its mechanism on the incidence of reperfusion arrhythmias following severe ischemia in isolated rat hearts Cardiovasc Drugs Ther 14 2000 625 633
82. Müller, A. L.; Hryshko, L. V.; Dhalla, N. S. (in press). Extracellular and intracellular proteases in cardiac dysfunction due to ischemia-reperfusion injury. Int J Cardiol (2012 Feb 20, Epub ahead of print) (PMID: 22357424).
83. C.E. Murry, R.B. Jennings, and K.A. Reimer Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium Circulation 74 1986 1124 1136
84. M. Osada, T. Netticadan, K. Kawabata, K. Tamura, and N.S. Dhalla Ischemic preconditioning prevents I/R-induced alterations in SR calcium-calmodulin protein kinase II Am J Physiol Heart Circ Physiol 278 2000 H1791 H1798
85. H. Otani Ischemic preconditioning: from molecular mechanisms to therapeutic opportunities Antioxid Redox Signal 10 2008 207 247
86. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol Rev 87 2007 315 424
87. S. Pan, S.Y. Ryu, and S.S. Sheu Distinctive characteristics and functions of multiple mitochondrial Ca2+ influx mechanisms Sci China Life Sci 54 2011 763 769
88. A. Panwalkar, S. Verstovsek, and F.J. Giles Mammalian target of rapamycin inhibition as therapy for hematologic malignancies Cancer 100 2004 657 666
89. K. Paul-Pletzer, T. Yamamoto, N. Ikemoto, L.S. Jimenez, H. Morimoto, and P.G. Williams Probing a putative dantrolene-binding site on the cardiac ryanodine receptor Biochem J 387 2005 905 909
90. Z. Pedrozo, G. Sanchez, N. Torrealba, R. Valenzuela, C. Fernandez, and C. Hidalgo Calpains and proteasomes mediate degradation of ryanodine receptors in a model of cardiac ischemic reperfusion Biochim Biophys Acta 1802 2010 356 362
91. I.N. Pessah, E.L. Durie, M.J. Schiedt, and I. Zimanyi Anthraquinone-sensitized Ca2+ release channel from rat cardiac sarcoplasmic reticulum: possible receptor-mediated mechanism of doxorubicin cardiomyopathy Mol Pharmacol 37 1990 503 514
92. I.N. Pessah, and W. Feng Functional role of hyperreactive sulfhydryl moieties within the ryanodine receptor complex Antioxid Redox Signal 2 2000 17 25
93. I.N. Pessah, M.J. Schiedt, M.A. Shalaby, M. Mack, and S.N. Giri Etiology of sarcoplasmic reticulum calcium release channel lesions in doxorubicin-induced cardiomyopathy Toxicology 72 1992 189 206
94. P. Pinton, D. Ferrari, E. Rapizzi, F. Di Virgilio, T. Pozzan, and R. Rizzuto The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action EMBO J 20 2001 2690 2701
95. C. Piot, P. Croisille, P. Staat, H. Thibault, G. Rioufol, and N. Mewton Effect of cyclosporine on reperfusion injury in acute myocardial infarction N Engl J Med 359 2008 473 481
96. P. Pouliquin, S.M. Pace, S.M. Curtis, P.J. Harvey, E.M. Gallant, and F. Zorzato Effects of an alpha-helical ryanodine receptor C-terminal tail peptide on ryanodine receptor activity: modulation by Homer Int J Biochem Cell Biol 38 2006 1700 1715
97. P. Pouliquin, S.M. Pace, and A.F. Dulhunty In vitro modulation of the cardiac ryanodine receptor activity by Homer1 Pflugers Arch 458 2009 723 732
98. S.G. Priori, and S.R. Chen Inherited dysfunction of sarcoplasmic reticulum Ca2+ handling and arrhythmogenesis Circ Res 108 2011 871 883
99. K. Raedschelders, D.M. Ansley, and D.D. Chen The cellular and molecular origin of reactive oxygen species generation during myocardial ischemia and reperfusion Pharmacol Ther 133 2012 230 255
100. D.P. Rardon, D.C. Cefali, R.D. Mitchell, S.M. Seiler, D.R. Hathaway, and L.R. Jones Digestion of cardiac and skeletal muscle junctional sarcoplasmic reticulum vesicles with calpain II. Effects on the Ca2+ release channel Circ Res 67 1990 84 96
101. S. Reiken, M. Gaburjakova, J. Gaburjakova, K.L. He Kl, A. Prieto, and E. Becker beta-adrenergic receptor blockers restore cardiac calcium release channel (ryanodine receptor) structure and function in heart failure Circulation 104 2001 2843 2848
102. A. Renilla, M. Barreiro, V. Barriales, F. Torres, P. Alvarez, and J.L. Lambert Management and risk factors for mortality in very elderly patients with acute myocardial infarction Geriatr Gerontol Int 13 1 2013, Jan 146 151
103. P. Rodriguez, M.S. Bhogal, and J. Colyer Stoichiometric phosphorylation of cardiac ryanodine receptor on serine 2809 by calmodulin-dependent kinase II and protein kinase A J Biol Chem 278 2003 38593 38600
104. E. Rousseau, and G. Meissner Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine Am J Physiol 256 1989 H328 H333
105. E. Rousseau, C. Michaud, D. Lefebvre, S. Proteau, and A. Decrouy Reconstitution of ionic channels from inner and outer membranes of mammalian cardiac nuclei Biophys J 70 1996 703 714
106. M. Ruiz-Meana, A. Abellan, E. Miro-Casas, E. Agullo, and D. Garcia-Dorado Role of sarcoplasmic reticulum in mitochondrial permeability transition and cardiomyocyte death during reperfusion Am J Physiol Heart Circ Physiol 297 2009 H1281 H1289
107. M. Ruiz-Meana, D. Garcia-Dorado, E. Miro-Casas, A. Abellan, and J. Soler-Soler Mitochondrial Ca2+ uptake during simulated ischemia does not affect permeability transition pore opening upon simulated reperfusion Cardiovasc Res 71 2006 715 724
108. M. Ruiz-Meana, J. Inserte, C. Fernandez-Sanz, V. Hernando, E. Miro-Casas, and I. Barba The role of mitochondrial permeability transition in reperfusion-induced cardiomyocyte death depends on the duration of ischemia Basic Res Cardiol 106 2011 1259 1268
109. M.N. Sack, and E. Murphy The role of comorbidities in cardioprotection J Cardiovasc Pharmacol Ther 16 2011 267 272
110. K. Saeki, I. Obi, N. Ogiku, M. Shigekawa, T. Imagawa, and T. Matsumoto Cardioprotective effects of 9-hydroxyellipticine on ischemia and reperfusion in isolated rat heart Jpn J Pharmacol 89 2002 21 28
111. M. Said, R. Becerra, C.A. Valverde, M.A. Kaetzel, J.R. Dedman, and C. Mundina-Weilenmann Calcium-calmodulin dependent protein kinase II (CaMKII): a main signal responsible for early reperfusion arrhythmias J Mol Cell Cardiol 51 2011 936 944
112. G. Salama, E.V. Menshikova, and J.J. Abramson Molecular interaction between nitric oxide and ryanodine receptors of skeletal and cardiac sarcoplasmic reticulum Antioxid Redox Signal 2 2000 5 16
113. G. Sanchez, M. Escobar, Z. Pedrozo, P. Macho, R. Domenech, and S. Hartel Exercise and tachycardia increase NADPH oxidase and ryanodine receptor-2 activity: possible role in cardioprotection Cardiovasc Res 77 2008 380 386
114. M. Santonastasi, and X.H. Wehrens Ryanodine receptors as pharmacological targets for heart disease Acta Pharmacol Sin 28 2007 937 944
115. T. Seidler, N. Teucher, K. Hellenkamp, B. Unsold, C. Grebe, and P. Kramps Limitations of FKBP12.6-directed treatment strategies for maladaptive cardiac remodeling and heart failure J Mol Cell Cardiol 50 2011 33 42
116. T.J. Sewell, E. Lam, M.M. Martin, J. Leszyk, J. Weidner, and J. Calaycay Inhibition of calcineurin by a novel FK-506-binding protein J Biol Chem 269 1994 21094 21102
117. J. Shan, M.J. Betzenhauser, A. Kushnir, S. Reiken, A.C. Meli, and A. Wronska Role of chronic ryanodine receptor phosphorylation in heart failure and beta-adrenergic receptor blockade in mice J Clin Invest 120 2010 4375 4387
118. C. Sigalas, S. Bent, A. Kitmitto, S. O'Neill, and R. Sitsapesan Ca(2+)-calmodulin can activate and inactivate cardiac ryanodine receptors Br J Pharmacol 156 2009 794 806
119. R.B. Singh, L. Hryshko, D. Freed, and N.S. Dhalla Activation of proteolytic enzymes and depression of the sarcolemmal Na+/K+-ATPase in ischemia-reperfused heart may be mediated through oxidative stress Can J Physiol Pharmacol 90 2012 249 260
120. G.B. Smith, T. Stefenelli, S.T. Wu, J. Wikman-Coffelt, W.W. Parmley, and C.E. Zaugg Rapid adaptation of myocardial calcium homeostasis to short episodes of ischemia in isolated rat hearts Am Heart J 131 1996 1106 1112
121. H.Y. Sun, N.P. Wang, F. Kerendi, M. Halkos, H. Kin, and R.A. Guyton Hypoxic postconditioning reduces cardiomyocyte loss by inhibiting ROS generation and intracellular Ca2+ overload Am J Physiol Heart Circ Physiol 288 2005 H1900 H1908
122. M.A. Talukder, A. Kalyanasundaram, X. Zhao, L. Zuo, P. Bhupathy, and G.J. Babu Expression of SERCA isoform with faster Ca2+ transport properties improves postischemic cardiac function and Ca2+ handling and decreases myocardial infarction Am J Physiol Heart Circ Physiol 293 2007 H2418 H2428
123. M.A. Talukder, J.L. Zweier, and M. Periasamy Targeting calcium transport in ischaemic heart disease Cardiovasc Res 84 2009 345 352
124. M. Tani, and J.R. Neely Role of intracellular Na+ in Ca2+ overload and depressed recovery of ventricular function of reperfused ischemic rat hearts. Possible involvement of H+ -Na+ and Na+ -Ca2+ exchange Circ Res 65 1989 1045 1056
125. F.T. Thandroyen, J. McCarthy, K.P. Burton, and L.H. Opie Ryanodine and caffeine prevent ventricular arrhythmias during acute myocardial ischemia and reperfusion in rat heart Circ Res 62 1988 306 314
126. A.P. Timerman, E. Ogunbumni, E. Freund, G. Wiederrecht, A.R. Marks, and S. Fleischer The calcium release channel of sarcoplasmic reticulum is modulated by FK-506-binding protein. Dissociation and reconstitution of FKBP-12 to the calcium release channel of skeletal muscle sarcoplasmic reticulum J Biol Chem 268 1993 22992 22999
127. B. Turan, and G. Vassort Ryanodine receptor: a new therapeutic target to control diabetic cardiomyopathy Antioxid Redox Signal 15 2011 1847 1861
128. R.J. van Oort, J.L. Respress, N. Li, C. Reynolds, A.C. De Almeida, and D.G. Skapura Accelerated development of pressure overload-induced cardiac hypertrophy and dysfunction in an RyR2-R176Q knockin mouse model Hypertension 55 2010 932 938
129. M. Vandonselaar, R.A. Hickie, J.W. Quail, and L.T. Delbaere Trifluoperazine-induced conformational change in Ca(2+)-calmodulin Nat Struct Biol 1 1994 795 801
130. L. Vittone, C. Mundina-Weilenmann, and A. Mattiazzi Phospholamban phosphorylation by CaMKII under pathophysiological conditions Front Biosci 13 2008 5988 6005
131. P. Volpe, P. Palade, B. Costello, R.D. Mitchell, and S. Fleischer Spontaneous calcium release from sarcoplasmic reticulum. Effect of local anesthetics J Biol Chem 258 1983 12434 12442
132. R. Wang, X. Zhong, X. Meng, A. Koop, X. Tian, and P.P. Jones Localization of the dantrolene-binding sequence near the FK506-binding protein-binding site in the three-dimensional structure of the ryanodine receptor J Biol Chem 286 2011 12202 12212
133. H. Watanabe, N. Chopra, D. Laver, H.S. Hwang, S.S. Davies, and D.E. Roach Flecainide prevents catecholaminergic polymorphic ventricular tachycardia in mice and humans Nat Med 15 2009 380 383
134. X. Wu, and D.M. Bers Free and bound intracellular calmodulin measurements in cardiac myocytes Cell Calcium 41 2007 353 364
135. H.B. Xin, T. Senbonmatsu, D.S. Cheng, Y.X. Wang, J.A. Copello, and G.J. Ji Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy Nature 416 2002 334 338
136. L. Xu, and G. Meissner Mechanism of calmodulin inhibition of cardiac sarcoplasmic reticulum Ca2+ release channel (ryanodine receptor) Biophys J 86 2004 797 804
137. L. Xu, A. Tripathy, D.A. Pasek, and G. Meissner Potential for pharmacology of ryanodine receptor/calcium release channels Ann N Y Acad Sci 853 1998 130 148
138. M. Yano, S. Kobayashi, M. Kohno, M. Doi, T. Tokuhisa, and S. Okuda FKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure Circulation 107 2003 477 484
139. M. Yano, S. Okuda, T. Oda, T. Tokuhisa, H. Tateishi, and M. Mochizuki Correction of defective interdomain interaction within ryanodine receptor by antioxidant is a new therapeutic strategy against heart failure Circulation 112 2005 3633 3643
140. N. Yaras, E. Tuncay, N. Purali, B. Sahinoglu, G. Vassort, and B. Turan Sex-related effects on diabetes-induced alterations in calcium release in the rat heart Am J Physiol Heart Circ Physiol 293 2007 H3584 H3592
141. G. Yu, R. Zucchi, S. Ronca-Testoni, and G. Ronca Protection of ischemic rat heart by dantrolene, an antagonist of the sarcoplasmic reticulum calcium release channel Basic Res Cardiol 95 2000 137 143
142. A. Zahradnikova, and P. Palade Procaine effects on single sarcoplasmic reticulum Ca2+ release channels Biophys J 64 1993 991 1003
143. M. Zaugg, E. Lucchinetti, M. Uecker, T. Pasch, and M.C. Schaub Anaesthetics and cardiac preconditioning. Part I. Signalling and cytoprotective mechanisms Br J Anaesth 91 2003 551 565
144. M. Zaugg, L. Wang, L. Zhang, P.H. Lou, E. Lucchinetti, and A.S. Clanachan Choice of anesthetic combination determines Ca2+ leak after ischemia-reperfusion injury in the working rat heart: favorable versus adverse combinations Anesthesiology 116 2012 648 657
145. Z.Q. Zhao, J.S. Corvera, M.E. Halkos, F. Kerendi, N.P. Wang, and R.A. Guyton Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning Am J Physiol Heart Circ Physiol 285 2003 H579 H588
146. Q. Zhou, J. Xiao, D. Jiang, R. Wang, K. Vembaiyan, and A. Wang Carvedilol and its new analogs suppress arrhythmogenic store overload-induced Ca2+ release Nat Med 17 2011 1003 1009
147. A.V. Zima, and L.A. Blatter Redox regulation of cardiac calcium channels and transporters Cardiovasc Res 71 2006 310 321
148. A.V. Zima, J.A. Copello, and L.A. Blatter Effects of cytosolic NADH/NAD(+) levels on sarcoplasmic reticulum Ca(2+) release in permeabilized rat ventricular myocytes J Physiol 555 2004 727 741
149. A.V. Zima, J. Qin, M. Fill, and L.A. Blatter Tricyclic antidepressant amitriptyline alters sarcoplasmic reticulum calcium handling in ventricular myocytes Am J Physiol Heart Circ Physiol 295 2008 H2008 H2016
150. Y. Zou, Y. Liang, H. Gong, N. Zhou, H. Ma, and A. Guan Ryanodine receptor type 2 is required for the development of pressure overload-induced cardiac hypertrophy Hypertension 58 2011 1099 1110
151. R. Zucchi, F. Ronca, and S. Ronca-Testoni Modulation of sarcoplasmic reticulum function: a new strategy in cardioprotection? Pharmacol Ther 89 2001 47 65
152. R. Zucchi, G. Yu, P. Galbani, M. Mariani, G. Ronca, and S. Ronca-Testoni Sulfhydryl redox state affects susceptibility to ischemia and sarcoplasmic reticulum Ca2+ release in rat heart. Implications for ischemic preconditioning Circ Res 83 1998 908 915
153. J.L. Zweier, J.T. Flaherty, and M.L. Weisfeldt Direct measurement of free radical generation following reperfusion of ischemic myocardium Proc Natl Acad Sci U S A 84 1987 1404 1407