Shortened Ca 2+ signaling refractoriness underlies cellular arrhythmogenesis in a postinfarction model of sudden cardiac death

Circulation Research

Volumn 110, Issue 4, 2012, Pages 569-577

  Belevych, Andriy E ^a   Terentyev, Dmitry ^a   Terentyeva, Radmila ^a   Ho, Hsiang Ting ^a   Gyorke, Inna ^a   Bonilla, Ingrid M ^a,b   Carnes, Cynthia A ^a,b   Billman, George E ^a   Györke, Sandor ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

arrhythmia; Ca 2+ waves; excitation contraction coupling; refractoriness; ryanodine receptor

Indexed keywords

CAFFEINE; CALCIUM; ISOPRENALINE; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; TIOPRONIN; BENZYLAMINE DERIVATIVE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL STIMULATING AGENT; PROTEIN KINASE INHIBITOR; REDUCING AGENT; RYANODINE RECEPTOR; SULFONAMIDE;

ANIMAL CELL; ANIMAL TISSUE; ARRHYTHMOGENESIS; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELLULAR ARRHYTHMOGENESIS; CONTROLLED STUDY; DEPOLARIZATION; DIASTOLIC SPONTANEOUS CALCIUM WAVE; EXPERIMENTAL DOG; HEART INFARCTION; HEART VENTRICLE FIBRILLATION; MUSCLE CELL; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SUDDEN DEATH; ANIMAL; DISEASE MODEL; DOG; DRUG ANTAGONISM; DRUG EFFECT; EXCITATION CONTRACTION COUPLING; FEMALE; HEART MUSCLE CELL; HEART PACING; MALE; METABOLISM; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PHOSPHORYLATION; REACTION TIME; SARCOPLASMIC RETICULUM; TIME;

ADRENERGIC BETA-AGONISTS; ANIMALS; BENZYLAMINES; CAFFEINE; CALCIUM CHANNEL AGONISTS; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CARDIAC PACING, ARTIFICIAL; DEATH, SUDDEN, CARDIAC; DISEASE MODELS, ANIMAL; DOGS; EXCITATION CONTRACTION COUPLING; FEMALE; ISOPROTERENOL; MALE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; REACTION TIME; REDUCING AGENTS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SULFONAMIDES; TIME FACTORS; TIOPRONIN; VENTRICULAR FIBRILLATION;

EID: 84857645169     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.260455     Document Type: Article

References (41)

1. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Roger VL, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J. Heart disease and stroke statistics: 2010 update: a report from the American Heart Association. Circulation. 2010;121:e46-e215.
2. Bunch TJ, Hohnloser SH, Gersh BJ. Mechanisms of sudden cardiac death in myocardial infarction survivors: insights from the randomized trials of implantable cardioverter-defibrillators. Circulation. 2007;115:2451-2457.
3. Ter Keurs HE, Boyden PA. Calcium and arrhythmogenesis. Physiol Rev. 2007;87:457-506.
4. Laurita KR, Rosenbaum DS. Mechanisms and potential therapeutic targets for ventricular arrhythmias associated with impaired cardiac calcium cycling. J Mol Cell Cardiol. 2008;44:31-43.
5. Weiss JN, Nivala M, Garfinkel A, Qu Z. Alternans and arrhythmias: from cell to heart. Circ Res. 2011;108:98-112.
6. Gyorke S, Terentyev D. Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease. Cardiovasc Res. 2008;77:245-255.
7. 2+ release in cardiac myocytes. Circ Res. 2002;91:414-420.
8. 2+ release refractoriness in heart muscle. Circ Res. 2004;95:807-813.
9. 2+ release in rat ventricular myocytes. J Physiol. 2005;565:441-447.
10. Venetucci LA, Trafford AW, O'Neill SC, Eisner DA. The sarcoplasmic reticulum and arrhythmogenic calcium release. Cardiovasc Res. 2008;77:285-292.
11. 2+ activation in the cardiac ryanodine receptor is associated with ventricular fibrillation and sudden death. Proc Natl Acad Sci U S A. 2007;104:18309-18314.
12. Stern MD, Capogrossi MC, Lakatta EG. Spontaneous calcium release from the sarcoplasmic reticulum in myocardial cells: mechanisms and consequences. Cell Calcium. 1988;9:247-256.
13. Kashimura T, Briston SJ, Trafford AW, Napolitano C, Priori SG, Eisner DA, Venetucci LA. In the RyR2 (R4496C) mouse model of CPVT, betaadrenergic stimulation induces Ca waves by increasing SR Ca content and not by decreasing the threshold for Ca waves. Circ Res. 2010;107:1483-1489.
14. Billman GE. A comprehensive review and analysis of 25 years of data from an in vivo canine model of sudden cardiac death: implications for future anti-arrhythmic drug development. Pharmacol Ther. 2006;111:808-835.
15. Schwartz PJ, Billman GE, Stone HL. Autonomic mechanisms in ventricular fibrillation induced by myocardial ischemia during exercise in dogs with healed myocardial infarction: an experimental preparation for sudden cardiac death. Circulation. 1984;69:790-800.
16. Sridhar A, Nishijima Y, Terentyev D, Terentyeva R, Uelmen R, Kukielka M, Bonilla IM, Robertson GA, Gyorke S, Billman GE, Carnes CA. Repolarization abnormalities and afterdepolarizations in a canine model of sudden cardiac death. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1463-R1472.
17. 2+ store throughout cardiac myocyte. Circ Res. 2006;99:283-291.
18. Belevych AE, Terentyev D, Viatchenko-Karpinski S, Terentyeva R, Sridhar A, Nishijima Y, Wilson LD, Cardounel AJ, Laurita KR, Carnes CA, Billman GE, Gyorke S. Redox modification of ryanodine receptors underlies calcium alternans in a canine model of sudden cardiac death. Cardiovasc Res. 2009;84:387-395.
19. Diaz ME, Trafford AW, O'Neill SC, Eisner DA. A measurable reduction of sr Ca content follows spontaneous Ca release in rat ventricular myocytes. Pflugers Arch. 1997;434:852-854.
20. Venetucci LA, Trafford AW, Eisner DA. Increasing ryanodine receptor open probability alone does not produce arrhythmogenic calcium waves: threshold sarcoplasmic reticulum calcium content is required. Circ Res. 2007;100:105-111.
21. Xie LH, Chen F, Karagueuzian HS, Weiss JN. Oxidative stress-induced afterdepolarizations and calmodulin kinase II signaling. Circ Res. 2009;104:79-86.
22. Benkusky NA, Weber CS, Scherman JA, Farrell EF, Hacker TA, John MC, Powers PA, Valdivia HH. 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.
23. Xiao B, Zhong G, Obayashi M, Yang D, Chen K, Walsh MP, Shimoni Y, Cheng H, Ter Keurs H, Chen SR. Ser-2030, but not Ser-2808, is the major phosphorylation site in cardiac ryanodine receptors responding to protein kinase A activation upon beta-adrenergic stimulation in normal and failing hearts. Biochem J. 2006;396:7-16.
24. Pogwizd SM, Bers DM. Cellular basis of triggered arrhythmias in heart failure. Trends Cardiovasc Med. 2004;14:61-66.
25. 2+ clock in cardiac pacemaker cells. Biophys J. 2011;100:271-283.
26. 2+ in the heart. Circ Res. 2008;103:509-518.
27. Wasserstrom JA, Shiferaw Y, Chen W, Ramakrishna S, Patel H, Kelly JE, O'Toole MJ, Pappas A, Chirayil N, Bassi N, Akintilo L, Wu M, Arora R, Aistrup GL. Variability in timing of spontaneous calcium release in the intact rat heart is determined by the time course of sarcoplasmic reticulum calcium load. Circ Res. 2010;107:1117-1126.
28. Cheng H, Lederer WJ. Calcium sparks. Physiol Rev. 2008;88:1491-1545.
29. 2+ release during diastole and systole in isolated rat ventricular myocytes. J Physiol. 1990;430:519-536.
30. 2+ sparks. Biophys J. 2011;100:931-938.
31. 2+ in cardiomyocytes. J Physiol. 2009;587:4863-4872.
32. 2+ waves in isolated permeabilized rabbit ventricular cardiomyocytes. Biophys J. 2009;96:2744-2754.
33. 2+. Biophys J. 2010;99:377-387.
34. Zima AV, Blatter LA. Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res. 2006;71:310-321.
35. Currie S. Cardiac ryanodine receptor phosphorylation by CaM Kinase II: keeping the balance right. Front Biosci. 2009;14:5134-5156.
36. Xu L, Eu JP, Meissner G, Stamler JS. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science. 1998;279:234-237.
37. Ikemoto N, Yamamoto T. Regulation of calcium release by interdomain interaction within ryanodine receptors. Front Biosci. 2002;7:d671-d683.
38. 2+ leak via stabilization of ryanodine receptor in heart failure. J Am Coll Cardiol. 2007;49:1722-1732.
39. 2+-alternans in intact mouse hearts. J Mol Cell Cardiol. 2012;52:21-31.
40. Belevych AE, Terentyev D, Terentyeva R, Nishijima Y, Sridhar A, Hamlin RL, Carnes CA, Györke S. The relationship between arrhythmogenesis and impaired contractility in heart failure: role of altered ryanodine receptor function. Cardiovasc Res. 2011;90:493-502.
41. Wasserstrom JA, Sharma R, Kapur S, Kelly JE, Kadish AH, Balke CW, Aistrup GL. Multiple defects in intracellular calcium cycling in whole failing rat heart. Circ Heart Fail. 2009;2:223-232.