Defective ryanodine receptor interdomain interactions may contribute to intracellular Ca2+ leak: A novel therapeutic target in heart failure

Circulation

Volumn 111, Issue 25, 2005, Pages 3342-3346

  Lehnart, Stephan E ^a   Wehrens, Xander H T ^a   Marks, Andrew R ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NONE   (United States)

Author keywords

Calcium; Death, sudden; Editorials; Heart failure; Sarcoplasmic reticulum

Indexed keywords

RYANODINE RECEPTOR;

CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; EDITORIAL; HEART FAILURE; HEART VENTRICLE ARRHYTHMIA; HUMAN; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS;

CALCIUM; HEART FAILURE, CONGESTIVE; HOMEOSTASIS; HUMANS; PROTEIN STRUCTURE, TERTIARY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 21544439823     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.105.551861     Document Type: Editorial

References (57)

1. Effect of enalapril on mortality and the development of heart failure in asymptomatic patients with reduced left ventricular ejection fractions. The SOLVD Investigators. N Engl J Med. 1992;327:685-691.
2. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, Palensky J, Wittes J. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med. 1999;341:709-717.
3. Pratt CM, Gardner M, Pepine C, Kohn R, Young JB, Greenberg B, Capone R, Kostis J, Henzlova M, Gosselin G, Weiss M, Francis M, Stewart D, Davis E, Yusuf S; SOLVD Investigators. Lack of long-term ventricular arrhythmia reduction by enalapril in heart failure. SOLVD Investigators. Am J Cardiol. 1995;75:1244-1249.
4. Stevenson WG, Stevenson LW, Middlekauff HR, Saxon LA. Sudden death prevention in patients with advanced ventricular dysfunction. Circulation. 1993;88:2953-2961.
5. Bristow MR, Ginsburg R, Minobe W, Cubicciotti RS, Sageman WS, Lurie K, Billingham ME, Harrison DC, Stinson EB. Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N Engl J Med. 1982;307:205-211.
6. Cohn JN, Levine TB, Olivari MT, Garberg V, Lura D, Francis GS, Simon AB, Rector T. Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure. N Engl J Med. 1984;311:819-823.
7. Packer M, Lee WH, Kessler PD, Gottlieb SS, Bernstein JL, Kukin ML. Role of neurohormonal mechanisms in determining survival in patients with severe chronic heart failure. Circulation. 1987;75:IV80-IV92.
8. The Cardiac Insufficiency Bisoprolol Study II (CIBIS-II): a randomised trial. Lancet. 1999;353:9-13.
9. Packer M, Coats AJ, Fowler MB, Katus HA, Krum H, Mohacsi P, Rouleau JL, Tendera M, Castaigne A, Roecker EB, Schultz MK, DeMets DL. Effect of carvedilol on survival in severe chronic heart failure. N Engl J Med. 2001;344:1651-1658.
10. Marks AR, Reiken S, Marx SO. Progression of heart failure: is protein kinase a hyperphosphorylation of the ryanodine receptor a contributing factor? Circulation. 2002;105:272-275.
11. Nienaber JJ, Tachibana H, Naga Prasad SV, Esposito G, Wu D, Mao L, Rockman HA. Inhibition of receptor-localized PI3K preserves cardiac beta-adrenergic receptor function and ameliorates pressure overload heart failure. J Clin Invest. 2003;112:1067-1079.
12. Morgan JP, Erny RE, Allen PD, Grossman W, Gwathmey JK. Abnormal intracellular calcium handling, a major cause of systolic and diastolic dysfunction in ventricular myocardium from patients with heart failure. Circulation. 1990;81:III21-III32.
13. Beuckelmann DJ, Nabauer M, Erdmann E. Intracellular calcium handling in isolated ventricular myocytes from patients with terminal heart failure. Circulation. 1992;85:1046-1055.
14. +-exchanger protein levels and diastolic function of failing human myocardium. Circulation. 1999;99:641-648.
15. + handling. J Clin Invest. 1996;98:764-776.
16. Gomez AM, Valdivia HH, Cheng H, Lederer MR, Santana LF, Cannell MB, McCune SA, Altschuld RA, Lederer WJ. Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science. 1997;276:800-806.
17. Hobai IA, O'Rourke B. Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation. 2001;103:1577-1584.
18. +)-ATPase in failing and nonfailing human myocardium. Circ Res. 1994;75:434-442.
19. + leak in intact ventricular myocytes from rabbits in heart failure. Circ Res. 2003;93:592-594.
20. + release from cardiac sarcoplasmic reticulum in tachycardia-induced heart failure. Cardiovasc Res. 1999;44:146-155.
21. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell. 2000;101:365-376.
22. Reiken S, Gaburjakova M, Guatimosim S, Gomez AM, D'Armiento J, Burkhoff D, Wang J, Vassort G, Lederer WJ, Marks AR. 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.
23. Reiken S, Gaburjakova M, Gaburjakova J, He KI KL, Prieto A, Becker E, Yi Gh GH, Wang J. Burkhoff D, Marks AR. beta-adrenergic receptor blockers restore cardiac calcium release channel (ryanodine receptor) structure and function in heart failure. Circulation. 2001;104:2843-2848.
24. Doi M, Yano M, Kobayashi S, Kohno M, Tokuhisa T, Okuda S, Suetsugu M, Hisamatsu Y, Ohkusa T, Matsuzaki M. Propranolol prevents the development of heart failure by restoring FKBP12.6-mediated stabilization of ryanodine receptor. Circulation. 2002;105:1374-1379.
25. +) release, in heart failure. Cardiovasc Res. 2000;48:323-331.
26. +) leak through ryanodine receptor in heart failure. Circulation. 2000;102:2131-2136.
27. Lehnart SE, Wehrens XH, Laitinen PJ, Reiken SR, Deng SX, Cheng Z, Landry DW, Kontula K, Swan H. Marks AR. Sudden death in familial polymorphic ventricular tachycardia associated with calcium release channel (ryanodine receptor) leak. Circulation. 2004;109:3208-3214.
28. Wehrens XH, Lehnart SE, Huang F, Vest JA, Reiken SR, Mohler PJ, Sun J, Guatimosim S, Song LS, Rosemblit N, D'Armiento JM, Napolitano C, Memmi M, Priori SG, Lederer WJ, Marks AR. FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell. 2003;113:829-840.
29. Laitinen PJ, Brown KM, Piippo K, Swan H, Devaney JM, Brahmbhatt B, Donarum EA, Marino M, Tiso N. Viitasalo M. Toivonen L. Stephan DA, Kontula K. Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation. 2001;103:485-490.
30. Priori SG, Napolitano C, Tiso N, Memmi M, Vignati G, Bloise R, Sorrentino V, Danieli GA. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation. 2001;103:196-200.
31. Oda T, Yano M, Yamamoto T, Tokuhisa T, Okuda S, Doi M, Ohkusa T, Ikeda Y, Kobayashi S, Ikemoto N, Matsuzaki M. Defective regulation of interdomain interactions within the ryanodine receptor plays a key role in the pathogenesis of heart failure. Circulation. 2005;111:3400-3410.
32. Marks AR, Priori S, Memmi M, Kontula K, Laitinen PJ. Involvement of the cardiac ryanodine receptor/calcium release channel in catecholaminergic polymorphic ventricular tachycardia. J Cell Physiol. 2002;190:1-6.
33. +) channel regulation. J Biol Chem. 2000;275:11618-11625.
34. +) channel regulation. Trends Cardiovasc Med. 2000;10:310-316.
35. Ikemoto N, Yamamoto T. Regulation of calcium release by interdomain interaction within ryanodine receptors. Front Biosci. 2002;7:d671-d683.
36. + release in skinned skeletal muscle fibers. Am J Physiol Cell Physiol. 2001;281:C207-C214.
37. + spark frequency in skeletal muscle. J Gen Physiol. 2002;119:15-32.
38. + channel regulation by interdomain interaction within the ryanodine receptor. Biochem J. 2004;380:561-569.
39. + release channel (ryanodine receptor). J Biol Chem. 2003;278:3786-3792.
40. Liu Z, Zhang J, Sharma MR. Li P, Chen SR, Wagenknecht T. Three-dimensional reconstruction of the recombinant type 3 ryanodine receptor and localization of its amino terminus. Proc Natl Acad Sci USA. 2001;98:6104-6109.
41. + release channel has an oxidoreductase-like domain. Proc Natl Acad Sci USA. 2002;99:12155-12160.
42. Orlova EV, Serysheva II, van Heel M, Hamilton SL, Chiu W. Two structural configurations of the skeletal muscle calcium release channel. Nat Struct Biol. 1996;3:547-552.
43. + and AMP-PCP. Biophys J. 1999;77:1936-1944.
44. Wagenknecht T, Radermacher M, Grassucci R, Berkowitz J, Xin HB, Fleischer S. Locations of calmodulin and FK506-binding protein on the three-dimensional architecture of the skeletal muscle ryanodine receptor. J Biol Chem. 1997;272:32463-32471.
45. Gaburjakova M, Gaburjakova J, Reiken S, Huang F, Marx SO, Rosemblit N, Marks AR. FKBP12 binding modulates ryanodine receptor channel gating. J Biol Chem. 2001;276:16931-16935.
46. Bultynck G, Rossi D, Callewaert G, Missiaen L, Sorrentino V. Parys JB, De Smedt H. The conserved sites for the FK506-binding proteins in ryanodine receptors and inositol 1,4.5-trisphosphate receptors are structurally and functionally different. J Biol Chem. 2001;276:47715-47724.
47. Liu Z, Zhang J, Wang R, Wayne Chen SR, Wagenknecht T. Location of divergent region 2 on the three-dimensional structure of cardiac muscle ryanodine receptor/calcium release channel. J Mol Biol. 2004;338:533-545.
48. Zhang J, Liu Z, Masumiya H, Wang R, Jiang D, Li F, Wagenknecht T, Chen SR. Three-dimensional localization of divergent region 3 of the ryanodine receptor to the clamp-shaped structures adjacent to the FKBP binding sites. J Biol. Chem. 2003;278:14211-14218.
49. +/calmodulin- dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res. 2004;94:e61-e70.
50. Wehrens XH, Lehnart SE, Reiken SR, Deng SX, Vest JA, Cervantes D, Coromilas J, Landry DW, Marks AR. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science. 2004;304:292-296.
51. + content in isolated failing and nonfailing human myocardium. Circ Res. 1999;85:38-46.
52. Marx SO, Reiken S, Hisamatsu Y, Gaburjakova M, Gaburjakova J. Yang YM, Rosemblit N, Marks AR. Phosphorylation-dependent regulation of ryanodine receptors: a novel role for leucine/isoleucine zippers. J Cell Biol. 2001;153:699-708.
53. Reiken S, Wehrens XH, Vest JA, Barbone A, Klotz S, Mancini D, Burkhoff D, Marks AR. Beta-blockers restore calcium release channel function and improve cardiac muscle performance in human heart failure. Circulation. 2003;107:2459-2466.
54. Reiken S, Lacampagne A, Zhou H, Kherani A, Lehnart SE, Ward C, Huang F, Gaburjakova M, Gaburjakova J. Rosemblit N, Warren MS, He KL, Yi GH, Wang J, Burkhoff D, Vassort G, Marks AR. PKA phosphorylation activates the calcium release channel (ryanodine receptor) in skeletal muscle: defective regulation in heart failure. J Cell Biol. 2003;160:919-928.
55. Yano M, Kobayashi S, Kohno M, Doi M, Tokuhisa T, Okuda S. Suetsugu M, Hisaoka T, Obayashi M, Ohkusa T, Matsuzaki M. FKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation. 2003;107:477-484.
56. White M, Yanowitz F, Gilbert EM, Larrabee P, O'Connell JB, Anderson JL, Renlund D, Mealey P, Abraham WT, Bristow MR. Role of beta-adrenergic receptor downregulation in the peak exercise response in patients with heart failure due to idiopathic dilated cardiomyopathy. Am J Cardiol. 1995;76:1271-1276.
57. + release channel at 14 Å resolution. J Mol Biol. 2005;345:427-431.