Dysfunctional ryanodine receptors in the heart: New insights into complex cardiovascular diseases

Journal of Molecular and Cellular Cardiology

Volumn 58, Issue 1, 2013, Pages 225-231

  Marx, Steven O ^a   Marks, Andrew R ^a  

^a College of Physicians and Surgeons of Columbia University ^*  (United States)

Author keywords

Arrhythmia; Calcium; Heart failure; Phosphorylation; Ryanodine receptor

Indexed keywords

2,3,4,5 TETRAHYDRO 7 METHOXY 4 METHYL 1,4 BENZOTHIAZEPINE; 4 [3 (4 BENZYL 1 PIPERIDINYL)PROPIONYL] 2,3,4,5 TETRAHYDRO 7 METHOXY 1,4 BENZOTHIAZEPINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CALSTABIN 1; CALSTABIN 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; RYANODINE RECEPTOR 1; RYANODINE RECEPTOR 2; UNCLASSIFIED DRUG;

CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; DISEASE COURSE; DUCHENNE MUSCULAR DYSTROPHY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME REGULATION; GENETIC MANIPULATION; HEART ARRHYTHMIA; HEART FAILURE; INCIDENCE; MORBIDITY; NITROSYLATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXCITATION CONTRACTION COUPLING; HEART FAILURE; HUMANS; MICE; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

MUS;

EID: 84876304597     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.03.005     Document Type: Review

References (86)

1. Takeshima H., Nishimura S., Matsumoto T., Ishida H., Kangawa K., Minamino N., et al. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 1989, 339:439-445.
2. 2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 1990, 265:2244-2256.
3. Schreiber S.L. Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science 1991, 251:283-287.
4. Jayaraman T., Brillantes A.-M.B., Timerman A.P., Erdjument-Bromage H., Fleischer S., Tempst P., et al. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 1992, 267:9474-9477.
5. Kaftan E., Marks A.R., Ehrlich B.E. Effects of rapamycin on ryanodine receptor/Ca(2+)-release channels from cardiac muscle. Circ Res 1996, 78:990-997.
6. Timerman A.P., Jayaraman T., Wiederrecht G., Onoue H., Marks A.R., Fleischer S. The ryanodine receptor from canine heart sarcoplasmic reticulum is associated with a novel FK-506 binding protein. Biochem Biophys Res Commun 1994, 198:701-706.
7. Marx S.O., Reiken S., Hisamatsu Y., Jayaraman T., Burkhoff D., Rosemblit N., et al. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 2000, 101:365-376.
8. Brillantes A.B., Ondrias K., Scott A., Kobrinsky E., Ondriasova E., Moschella M.C., et al. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 1994, 77:513-523.
9. Marx S.O., Reiken S., Hisamatsu Y., Gaburjakova M., Gaburjakova J., Yang Y.M., et al. Phosphorylation-dependent regulation of ryanodine receptors: a novel role for leucine/isoleucine zippers. J Cell Biol 2001, 153:699-708.
10. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
11. 2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 2004, 94:e61-e70.
12. Witcher D.R., Kovacs R.J., Schulman H., Cefali D.C., Jones L.R. Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J Biol Chem 1991, 266:11144-11152.
13. Rodriguez P., Bhogal M.S., Colyer J. Stoichiometric phosphorylation of cardiac ryanodine receptor on serine 2809 by calmodulin-dependent kinase II and protein kinase A. J Biol Chem 2003, 278:38593-38600.
14. Wehrens X.H., Lehnart S.E., Reiken S., Vest J.A., Wronska A., Marks A.R. Ryanodine receptor/calcium release channel PKA phosphorylation: a critical mediator of heart failure progression. Proc Natl Acad Sci U S A 2006, 103:511-518.
15. Kushnir A., Shan J., Betzenhauser M.J., Reiken S., Marks A.R. Role of CaMKIIdelta phosphorylation of the cardiac ryanodine receptor in the force frequency relationship and heart failure. Proc Natl Acad Sci U S A 2010, 107:10274-10279.
16. Respress J.L., van Oort R.J., Li N., Rolim N., Dixit S.S., Dealmeida A., et al. Role of RyR2 phosphorylation at S2814 during heart failure progression. Circ Res 2012, 110:1474-1483.
17. Shan J., Kushnir A., Betzenhauser M.J., Reiken S., Li J., Lehnart S.E., et al. Phosphorylation of the ryanodine receptor mediates the cardiac fight or flight response in mice. J Clin Invest 2010, 120:4388-4398.
18. Shan J., Betzenhauser M.J., Kushnir A., Reiken S., Meli A.C., Wronska A., et al. Role of chronic ryanodine receptor phosphorylation in heart failure and beta-adrenergic receptor blockade in mice. J Clin Invest 2010, 120:4375-4387.
19. Xiao B., Jiang M.T., Zhao M., Yang D., Sutherland C., Lai F.A., et al. Characterization of a novel PKA phosphorylation site, serine-2030, reveals no PKA hyperphosphorylation of the cardiac ryanodine receptor in canine heart failure. Circ Res 2005, 96:847-855.
20. Benkusky N.A., Weber C.S., Scherman J.A., Farrell E.F., Hacker T.A., John M.C., et al. Intact beta-adrenergic response and unmodified progression toward heart failure in mice with genetic ablation of a major protein kinase A phosphorylation site in the cardiac ryanodine receptor. Circ Res 2007, 101:819-829.
21. Zhang H., Makarewich C.A., Kubo H., Wang W., Duran J.M., Li Y., et al. Hyperphosphorylation of the cardiac ryanodine receptor at serine 2808 is not involved in cardiac dysfunction after myocardial infarction. Circ Res 2012, 110:831-840.
22. Eisner D.A., Kashimura T., O'Neill S.C., Venetucci L.A., Trafford A.W. What role does modulation of the ryanodine receptor play in cardiac inotropy and arrhythmogenesis?. J Mol Cell Cardiol 2009, 46:474-481.
23. 2+ fluxes in rat ventricular myocytes. J Physiol 2000, 522(Pt 2):259-270.
24. Timerman A.P., Ogunbumni E., Freund E., Wiederrecht G., Marks A.R., Fleischer S. 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 1993, 268:22992-22999.
25. Gellen B., Fernandez-Velasco M., Briec F., Vinet L., LeQuang K., Rouet-Benzineb P., et al. Conditional FKBP12.6 overexpression in mouse cardiac myocytes prevents triggered ventricular tachycardia through specific alterations in excitation-contraction coupling. Circulation 2008, 117:1778-1786.
26. Chelu M.G., Danila C.I., Gilman C.P., Hamilton S.L. Regulation of ryanodine receptors by FK506 binding proteins. Trends Cardiovasc Med 2004, 14:227-234.
27. 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 2003, 93:531-540.
28. Doi M., Yano M., Kobayashi S., Kohno M., Tokuhisa T., Okuda S., et al. Propranolol prevents the development of heart failure by restoring FKBP12.6-mediated stabilization of ryanodine receptor. Circulation 2002, 105:1374-1379.
29. Prestle J., Janssen P.M., Janssen A.P., Zeitz O., Lehnart S.E., Bruce L., et al. Overexpression of FK506-binding protein FKBP12.6 in cardiomyocytes reduces ryanodine receptor-mediated Ca(2+) leak from the sarcoplasmic reticulum and increases contractility. Circ Res 2001, 88:188-194.
30. Yano M., Ono K., Ohkusa T., Suetsugu M., Kohno M., Hisaoka T., et al. Altered stoichiometry of FKBP12.6 versus ryanodine receptor as a cause of abnormal Ca(2+) leak through ryanodine receptor in heart failure. Circulation 2000, 102:2131-2136.
31. Ono K., Yano M., Ohkusa T., Kohno M., Hisaoka T., Tanigawa T., et al. Altered interaction of FKBP12.6 with ryanodine receptor as a cause of abnormal Ca(2+) release in heart failure. Cardiovasc Res 2000, 48:323-331.
32. Marx S.O., Gaburjakova J., Gaburjakova M., Henrikson C., Ondrias K., Marks A.R. Coupled gating between cardiac calcium release channels (ryanodine receptors). Circ Res 2001, 88:1151-1158.
33. Guo T., Cornea R.L., Huke S., Camors E., Yang Y., Picht E., et al. Kinetics of FKBP12.6 binding to ryanodine receptors in permeabilized cardiac myocytes and effects on Ca sparks. Circ Res 2010, 106:1743-1752.
34. 2+ transients in rat cardiac myocytes. Circ Res 1996, 79:1110-1121.
35. Jeyakumar L.H., Ballester L., Cheng D.S., McIntyre J.O., Chang P., Olivey H.E., et al. FKBP binding characteristics of cardiac microsomes from diverse vertebrates. Biochem Biophys Res Commun 2001, 281:979-986.
36. Timerman A.P., Onoue H., Xin H.B., Barg S., Copello J., Wiederrecht G., et al. Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J Biol Chem 1996, 271:20385-20391.
37. Stange M., Xu L., Balshaw D., Yamaguchi N., Meissner G. Characterization of recombinant skeletal muscle (Ser-2843) and cardiac muscle (Ser-2809) ryanodine receptor phosphorylation mutants. J Biol Chem 2003, 278:51693-51702.
38. Xu L., Eu J.P., Meissner G., Stamler J.S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 1998, 279:234-237.
39. Andersson D.C., Betzenhauser M.J., Reiken S., Meli A.C., Umanskaya A., Xie W., et al. Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab 2011, 14:196-207.
40. Dube P., Weber K.T. Congestive heart failure: pathophysiologic consequences of neurohormonal activation and the potential for recovery: part II. Am J Med Sci 2011, 342:503-506.
41. Lehnart S.E., Terrenoire C., Reiken S., Wehrens X.H., Song L.S., Tillman E.J., et al. Stabilization of cardiac ryanodine receptor prevents intracellular calcium leak and arrhythmias. Proc Natl Acad Sci U S A 2006, 103:7906-7910.
42. Wehrens X.H., Lehnart S.E., Reiken S.R., Deng S.X., Vest J.A., Cervantes D., et al. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science 2004, 304:292-296.
43. Lehnart S.E., Wehrens X.H., Laitinen P.J., Reiken S.R., Deng S.X., Cheng Z., et al. Sudden death in familial polymorphic ventricular tachycardia associated with calcium release channel (ryanodine receptor) leak. Circulation 2004, 109:3208-3214.
44. Wehrens X.H., Lehnart S.E., Huang F., Vest J.A., Reiken S.R., Mohler P.J., et al. FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 2003, 113:829-840.
45. 2+ leak in intact ventricular myocytes from rabbits in heart failure. Circ Res 2003, 93:592-594.
46. Belevych A., Kubalova Z., Terentyev D., Hamlin R.L., Carnes C.A., Gyorke S. Enhanced ryanodine receptor-mediated calcium leak determines reduced sarcoplasmic reticulum calcium content in chronic canine heart failure. Biophys J 2007, 93:4083-4092.
47. Andersson D.C., Marks A.R. Fixing ryanodine receptor Ca leak - a novel therapeutic strategy for contractile failure in heart and skeletal muscle. Drug Discov Today Dis Mech 2010, 7:e151-e157.
48. 2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice. J Clin Invest 2008, 118:2230-2245.
49. Lehnart S.E., Wehrens X.H., Reiken S., Warrier S., Belevych A.E., Harvey R.D., et al. Phosphodiesterase 4D deficiency in the ryanodine-receptor complex promotes heart failure and arrhythmias. Cell 2005, 123:25-35.
50. Arai M., Alpert N.R., MacLennan D.H., Barton P., Periasamy M. Alterations in sarcoplasmic reticulum gene expression in human heart failure. A possible mechanism for alterations in systolic and diastolic properties of the failing myocardium. Circ Res 1993, 72:463-469.
51. Hobai I.A., O'Rourke B. Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation 2001, 103:1577-1584.
52. 2+ cycling and new therapeutic approaches for heart failure. Circulation 2010, 121:822-830.
53. Ogrodnik J., Niggli E. Increased Ca(2+) leak and spatiotemporal coherence of Ca(2+) release in cardiomyocytes during beta-adrenergic stimulation. J Physiol 2010, 588:225-242.
54. 2+ leak in mouse heart. Biochem Biophys Res Commun 2009, 390:87-92.
55. Blayney L.M., Jones J.L., Griffiths J., Lai F.A. A mechanism of ryanodine receptor modulation by FKBP12/12.6, protein kinase A, and K201. Cardiovasc Res 2010, 85:68-78.
56. Yano M., Kobayashi S., Kohno M., Doi M., Tokuhisa T., Okuda S., et al. FKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation 2003, 107:477-484.
57. Reiken S., Gaburjakova M., Guatimosim S., Gomez A.M., D'Armiento J., Burkhoff D., 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 2003, 278:444-453.
58. Estrada-Quintero T., Uretsky B.F., Murali S., Griffith B.P., Kormos R.L. Neurohormonal activation and exercise function in patients with severe heart failure and patients with left ventricular assist system. A comparative study. Chest 1995, 107:1499-1503.
59. Reiken S., Wehrens X.H., Vest J.A., Barbone A., Klotz S., Mancini D., et al. Beta-blockers restore calcium release channel function and improve cardiac muscle performance in human heart failure. Circulation 2003, 107:2459-2466.
60. Reiken S., Gaburjakova M., Gaburjakova J., He Kl K.L., Prieto A., Becker E., et al. Beta-adrenergic receptor blockers restore cardiac calcium release channel (ryanodine receptor) structure and function in heart failure. Circulation 2001, 104:2843-2848.
61. Kushnir A., Betzenhauser M.J., Marks A.R. Ryanodine receptor studies using genetically engineered mice. FEBS Lett 2010, 584:1956-1965.
62. Huang F., Shan J., Reiken S., Wehrens X.H., Marks A.R. Analysis of calstabin2 (FKBP12.6)-ryanodine receptor interactions: rescue of heart failure by calstabin2 in mice. Proc Natl Acad Sci U S A 2006, 103:3456-3461.
63. 2+ release, but normal ryanodine receptors, in canine and human heart failure. Circ Res 2002, 91:1015-1022.
64. 2+ release (SOICR). Proc Natl Acad Sci U S A 2004, 101:13062-13067.
65. Sobie E.A., Lederer W.J. Dynamic local changes in sarcoplasmic reticulum calcium: physiological and pathophysiological roles. J Mol Cell Cardiol 2012, 52:304-311.
66. Hoch B., Haase H., Schulze W., Hagemann D., Morano I., Krause E.G., et al. Differentiation-dependent expression of cardiac delta-CaMKII isoforms. J Cell Biochem 1998, 68:259-268.
67. 2+/calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. J Clin Invest 2009, 119:1230-1240.
68. Priori S.G., Napolitano C., Tiso N., Memmi M., Vignati G., Bloise R., et al. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 2001, 103:196-200.
69. Swan H., Piippo K., Viitasalo M., Heikkila P., Paavonen T., Kainulainen K., et al. Arrhythmic disorder mapped to chromosome 1q42-q43 causes malignant polymorphic ventricular tachycardia in structurally normal hearts. J Am Coll Cardiol 1999, 34:2035-2042.
70. Sun H., Gaspo R., Leblanc N., Nattel S. Cellular mechanisms of atrial contractile dysfunction caused by sustained atrial tachycardia. Circulation 1998, 98:719-727.
71. Vest J.A., Wehrens X.H., Reiken S.R., Lehnart S.E., Dobrev D., Chandra P., et al. Defective cardiac ryanodine receptor regulation during atrial fibrillation. Circulation 2005, 111:2025-2032.
72. Sood S., Chelu M.G., van Oort R.J., Skapura D., Santonastasi M., Dobrev D., et al. Intracellular calcium leak due to FKBP12.6 deficiency in mice facilitates the inducibility of atrial fibrillation. Heart Rhythm 2008, 5:1047-1054.
73. 2+ leak promotes atrial fibrillation in mice. J Clin Invest 2009, 119:1940-1951.
74. 2+ exchanger function underlie delayed after depolarizations in patients with chronic atrial fibrillation. Circulation 2012, 125:2059-2070.
75. Shan J., Xie W., Betzenhauser M., Reiken S., Chen B.X., Wronska A., et al. Calcium leak through ryanodine receptors leads to atrial fibrillation in 3 mouse models of catecholaminergic polymorphic ventricular tachycardia. Circ Res 2012, 111:708-717.
76. Li N., Wang T., Wang W., Cutler M.J., Wang Q., Voigt N., et al. Inhibition of CaMKII phosphorylation of RyR2 prevents induction of atrial fibrillation in FKBP12.6 knockout mice. Circ Res 2012, 110:465-470.
77. van Oort R.J., Respress J.L., Li N., Reynolds C., De Almeida A.C., Skapura D.G., et al. Accelerated development of pressure overload-induced cardiac hypertrophy and dysfunction in an RyR2-R176Q knockin mouse model. Hypertension 2010, 55:932-938.
78. 2+ movement in large unilamellar vesicles by K201, a new 1,4-benzothiazepine derivative. Biochim Biophys Acta 1997, 1330:1-7.
79. Ito K., Shigematsu S., Sato T., Abe T., Li Y., Arita M. JTV-519, a novel cardioprotective agent, improves the contractile recovery after ischaemia-reperfusion in coronary perfused guinea-pig ventricular muscles. Br J Pharmacol 2000, 130:767-776.
80. + current in guinea-pig ventricular myocytes. Naunyn Schmiedebergs Arch Pharmacol 2000, 361:646-653.
81. Kimura J., Kawahara M., Sakai E., Yatabe J., Nakanishi H. Effects of a novel cardioprotective drug, JTV-519, on membrane currents of guinea pig ventricular myocytes. Jpn J Pharmacol 1999, 79:275-281.
82. Wehrens X.H., Lehnart S.E., Reiken S., van der Nagel R., Morales R., Sun J., et al. Enhancing calstabin binding to ryanodine receptors improves cardiac and skeletal muscle function in heart failure. Proc Natl Acad Sci U S A 2005, 102:9607-9612.
83. Fauconnier J., Meli A.C., Thireau J., Roberge S., Shan J., Sassi Y., et al. Ryanodine receptor leak mediated by caspase-8 activation leads to left ventricular injury after myocardial ischemia-reperfusion. Proc Natl Acad Sci U S A 2011, 108:13258-13263.
84. Fauconnier J., Thireau J., Reiken S., Cassan C., Richard S., Matecki S., et al. Leaky RyR2 trigger ventricular arrhythmias in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 2010, 107:1559-1564.
85. Bellinger A.M., Reiken S., Carlson C., Mongillo M., Liu X., Rothman L., et al. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 2009, 15:325-330.
86. Liu X., Betzenhauser M.J., Reiken S., Meli A.C., Xie W., Chen B.X., et al. Role of leaky neuronal ryanodine receptors in stress-induced cognitive dysfunction. Cell 2012, 150:1055-1067.