Spark-induced sparks as a mechanism of intracellular calcium alternans in cardiac myocytes

Circulation Research

Volumn 106, Issue 10, 2010, Pages 1582-1591

  Rovetti, Robert ^a   Cui, Xiaohua ^b,c   Garfinkel, Alan ^c   Weiss, James N ^c   Qu, Zhilin ^c  

^a LOYOLA MARYMOUNT UNIVERSITY   (United States)

^b BEIJING NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Calcium alternans; Calcium sparks; Randomness; Recruitment; Refractoriness

Indexed keywords

CALCIUM ION;

ARTICLE; CALCIUM ALTERNANS; CALCIUM CELL LEVEL; CALCIUM METABOLISM; CALCIUM TRANSPORT; CELL INTERACTION; CELLULAR DISTRIBUTION; COMPUTER SIMULATION; CONTROLLED STUDY; HEART MUSCLE CELL; HEART PACING; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MUSCLE FIBRIL; PRIORITY JOURNAL; SARCOPLASMIC RETICULUM; THEORETICAL MODEL; WHOLE CELL;

ANIMALS; CALCIUM; CALCIUM SIGNALING; COMPUTER SIMULATION; DIFFUSION; KINETICS; MARKOV CHAINS; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; NONLINEAR DYNAMICS; PROBABILITY; SARCOPLASMIC RETICULUM; SODIUM-CALCIUM EXCHANGER;

EID: 77953022226     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.213975     Document Type: Article

References (54)

1. Bers DM. Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol. 2008;70:23-49.
2. ter Keurs HEDJ, Boyden PA. Calcium and arrhythmogenesis. Physiol Rev. 2007;87:457-506.
3. Weiss JN, Karma A, Shiferaw Y, Chen PS, Garfinkel A, Qu Z. From pulsus to pulseless: the saga of cardiac alternans. Circ Res. 2006;98: 1244-1253.
4. Eisner DA, Choi HS, Diaz ME, O'Neill SC, Trafford AW. Integrative analysis of calcium cycling in cardiac muscle. Circ Res. 2000;87: 1087-1094.
5. Blatter LA, Kockskamper J, Sheehan KA, Zima AV, Huser J, Lipsius SL. Local calcium gradients during excitation-contraction coupling and alternans in atrial myocytes. J Physiol. 2003;546:19-31.
6. 2+ transient in rat ventricular myocytes. Circ Res. 2002;91:585-593.
7. Diaz ME, O'Neill SC, Eisner DA. Sarcoplasmic reticulum calcium content fluctuation is the key to cardiac alternans. Circ Res. 2004;94: 650-656.
8. 2+ signaling, cardiac alternans, and ventricular arrhythmias in intact rat heart. Circ Res. 2006;99:e65-e73.
9. Xie LH, Sato D, Garfinkel A, Qu Z, Weiss JN. Intracellular Ca alternans: coordinated regulation by sarcoplasmic reticulum release, uptake, and leak. Biophys J. 2008;95:3100-3110.
10. Gaeta SA, Bub G, Abbott GW, Christini DJ. Dynamical mechanism for subcellular alternans in cardiac myocytes. Circ Res. 2009;105:335-342.
11. 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.
12. Picht E, DeSantiago J, Blatter LA, Bers DM. Cardiac alternans do not rely on diastolic sarcoplasmic reticulum calcium content fluctuations. Circ Res. 2006;99:740-748.
13. Huser J, Wang YG, Sheehan KA, Cifuentes F, Lipsius SL, Blatter LA. Functional coupling between glycolysis and excitation-contraction coupling underlies alternans in cat heart cells. J Physiol. 2000;524(Pt 3):795-806.
14. Shiferaw Y, Watanabe MA, Garfinkel A, Weiss JN, Karma A. Model of intracellular calcium cycling in ventricular myocytes. Biophys J. 2003; 85:3666-3686.
15. Tao T, O'Neill SC, Diaz ME, Li YT, Eisner DA, Zhang H. Alternans of cardiac calcium cycling in a cluster of ryanodine receptors: a simulation study. Am J Physiol Heart Circ Physiol. 2008;295:H598-H609.
16. Cheng H, Lederer WJ, Cannell MB. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science. 1993;262:740-744.
17. Cheng H, Lederer WJ. Calcium Sparks. Physiol Rev. 2008;88:1491-1545.
18. Stern MD. Theory of excitation-contraction coupling in cardiac muscle. Biophys J. 1992;63:497-517.
19. 2+]i waves in cardiac myocytes. Am J Physiol. 1996;270:C148-C159.
20. 2+ release sites along Z-lines in rat heart cells. J Physiol. 1996;497(Pt 1):31-38.
21. 2+ sparks in frog skeletal muscle. J Physiol. 2000;528:419-433.
22. 2+ sparks evoked by action potentials in mouse ventricular myocytes. J Physiol. 1999;518(Pt 2):469-478.
23. 2+ channels and ryanodine receptors in heart cells. Nature. 2001;410:592-596.
24. 2+ channels. Circ Res. 2003;92:532-538.
25. 2+ release in rat ventricular myocytes. J Physiol. 2005;565:441-447.
26. 2+ release and vulnerability to arrhythmias. J Cardiovasc Electrophysiol. 2006; 17(Suppl 1):S64-S70.
27. Stern MD, Song LS, Cheng H, Sham JS, Yang HT, Boheler KR, Rios E. Local control models of cardiac excitation-contraction coupling. A possible role for allosteric interactions between ryanodine receptors. J Gen Physiol. 1999;113:469-489.
28. 2+ blinks: rapid nanoscopic store calcium signaling. Proc Natl Acad Sci USA. 2005;102:3099-3104.
29. 2+ diffusion. Circ Res. 2008;103:e105-e115.
30. Cui X, Rovetti RJ, Yang L, Garfinkel A, Weiss JN, Qu Z. Period-doubling bifurcation in an array of coupled stochastically excitable elements subjected to global periodic forcing. Phys Rev Lett. 2009;103: 044102-044104.
31. Luzza F, Oreto G. Verapamil-induced electrical and cycle length alternans during supraventricular tachycardia: what is the mechanism? J Cardiovasc Electrophysiol. 2003;14:323-324.
32. 2+ alternans in rat ventricular myocytes. J Physiol. 2009;587:1283-1292.
33. Saitoh H, Bailey JC, Surawicz B. Action potential duration alternans in dog Purkinje and ventricular muscle fibers: further evidence in support of two different mechanisms. Circulation. 1989;80:1421-1431.
34. Dumitrescu C, Narayan P, Efimov IR, Cheng Y, Radin MJ, McCune SA, Altschuld RA. Mechanical alternans and restitution in failing SHHF rat left ventricles. Am J Physiol Heart Circ Physiol. 2002;282:H1320-H1326. (Pubitemid 34654884)
35. Schmidt AG, Kadambi VJ, Ball N, Sato Y, Walsh RA, Kranias EG, Hoit BD. Cardiac-specific overexpression of calsequestrin results in left ventricular hypertrophy, depressed force-frequency relation and pulsus alternans in vivo. J Mol Cell Cardiol. 2000;32:1735-1744.
36. 2+ release in cardiac myocytes. Circ Res. 2002;91:414-420.
37. Restrepo JG, Weiss JN, Karma A. Calsequestrin-mediated mechanism for cellular calcium transient alternans. Biophys J. 2008;95:3767-3789.
38. Soeller C, Crossman D, Gilbert R, Cannell MB. Analysis of ryanodine receptor clusters in rat and human cardiac myocytes. Proc Natl Acad Sci USA. 2007;104:14958-14963.
39. Chen-Izu Y, McCulle SL, Ward CW, Soeller C, Allen BM, Rabang C, Cannell MB, Balke CW, Izu LT. Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys J. 2006; 91:1-13.
40. 2+ release units and couplons in skeletal and cardiac muscles. Biophys J. 1999;77:1528-1539.
41. 2+ sparks in myocytes from infarcted hearts. Circ Res. 2000;87:1040-1047.
42. Gomez AM, Guatimosim S, Dilly KW, Vassort G, Lederer WJ. Heart failure after myocardial infarction: altered excitation-contraction coupling. Circulation. 2001;104:688-693.
43. 2+ release in murine cardiomyocytes following myocardial infarction. J Physiol. 2006;574:519-533.
44. Brette F, Orchard C. T-tubule function in mammalian cardiac myocytes. Circ Res. 2003;92:1182-1192.
45. Qian YW, Clusin WT, Lin SF, Han J, Sung RJ. Spatial heterogeneity of calcium transient alternans during the early phase of myocardial ischemia in the blood-perfused rabbit heart. Circulation. 2001;104:2082-2087.
46. Wilson LD, Jeyaraj D, Wan X, Hoeker GS, Said TH, Gittinger M, Laurita KR, Rosenbaum DS. Heart failure enhances susceptibility to arrhyth-mogenic cardiac alternans. Heart Rhythm. 2009;6:251-259.
47. Lehnart SE, Terrenoire C, Reiken S, Wehrens XHT, Song L-S, Tillman EJ, Mancarella S, Coromilas J, Lederer WJ, Kass RS, Marks AR. Stabilization of cardiac ryanodine receptor prevents intracellular calcium leak and arrhythmias. Proc Natl Acad Sci USA. 2006;103:7906-7910.
48. 2+ release (SOICR). Proc Natl Acad Sci USA. 2004;101:13062-13067.
49. Gyorke I, Hester N, Jones LR, Gyorke S. The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys J. 2004;86:2121-2128.
50. 2+ sparks. Biophys J. 1998;75:595-600.
51. Chen-Izu Y, Ward CW, Stark W Jr, Banyasz T, Sumandea MP, Balke CW, Izu LT, Wehrens XH. Phosphorylation of RyR2 and shortening of RyR2 cluster spacing in spontaneously hypertensive rat with heart failure. Am J Physiol Heart Circ Physiol. 2007;293:H2409-H2417.
52. Shannon TR, Wang F, Bers DM. Regulation of cardiac sarcoplasmic reticulum Ca release by luminal [Ca] and altered gating assessed with a mathematical model. Biophys J. 2005;89:4096-4110.
53. Shannon TR, Ginsburg KS, Bers DM. Potentiation of fractional sarcoplasmic reticulum calcium release by total and free intra-sarcoplasmic reticulum calcium concentration. Biophys J. 2000;78:334-343.
54. Terentyev D, Kubalova Z, Valle G, Nori A, Vedamoorthyrao S, Ter-entyeva R, Viatchenko-Karpinski S, Bers DM, Williams SC, Volpe P, Gyorke S. Modulation of SR Ca release by luminal Ca and calsequestrin in cardiac myocytes: effects of CASQ2 mutations linked to sudden cardiac death. Biophys J. 2008;95:2037-2048.