Dynamic local changes in sarcoplasmic reticulum calcium: Physiological and pathophysiological roles

Journal of Molecular and Cellular Cardiology

Volumn 52, Issue 2, 2012, Pages 304-311

  Sobie, Eric A ^a   Lederer, W J ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Arrhythmia; Ca 2+ spark; Ca 2+ transient; Ca 2+ wave; Mathematical modeling; Triggered activity; Ventricular myocyte

Indexed keywords

CALCIUM ION;

ACTION POTENTIAL; CALCIUM DEPLETION; CALCIUM TRANSPORT; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; DIFFUSION; DISEASE MODEL; HEART ARRHYTHMIA; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; MATHEMATICAL MODEL; MOLECULAR MECHANICS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SARCOPLASMIC RETICULUM;

ANIMALS; CALCIUM; CALCIUM SIGNALING; HUMANS; MYOCYTES, CARDIAC; SARCOPLASMIC RETICULUM;

EID: 84855995319     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.06.024     Document Type: Review

References (99)

1. Cannell MB, Kong CHT. Local control in cardiac E-C coupling. J Mol Cell Cardiol 2012;52:298-303.
2. Chen-Izu Y., McCulle S.L., Ward C.W., Soeller C., Allen B.M., Rabang C., et al. Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys J 2006, 91:1-13.
3. Baddeley D., Jayasinghe I.D., Lam L., Rossberger S., Cannell M.B., Soeller C. Optical single-channel resolution imaging of the ryanodine receptor distribution in rat cardiac myocytes. Proc Natl Acad Sci USA 2009, 106:22275-22280.
4. 2+ release units and couplons in skeletal and cardiac muscles. Biophys J 1999, 77:1528-1539.
5. Cheng H., Lederer W.J., Cannell M.B. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 1993, 262:740-744.
6. Cannell M.B., Cheng H., Lederer W.J. The control of calcium release in heart muscle. Science 1995, 268:1045-1049.
7. Lopez-Lopez J.R., Shacklock P.S., Balke C.W., Wier W.G. Local calcium transients triggered by single L-type calcium channel currents in cardiac cells. Science 1995, 268:1042-1045.
8. 2+ release in ventricular myocytes. Biophys J 2008, 94:L54-L56.
9. + channels. J Physiol 2010, 588:4249-4260.
10. 2+]i waves in cardiac myocytes. Am J Physiol 1996, 270:C148-C159.
11. Rovetti R., Cui X., Garfinkel A., Weiss J.N., Qu Z. Spark-induced sparks as a mechanism of intracellular calcium alternans in cardiac myocytes. Circ Res 2010, 106:1582-1591.
12. 2+ release in myocytes from chronically ischemic myocardium. Circ Res 2008, 102:338-346.
13. 2+ release in human failing cardiomyocytes. Cardiovasc Res 2004, 62:63-73.
14. 2+ release in murine cardiomyocytes following myocardial infarction. J Physiol (Lond) 2006, 574:519-533.
15. Song L.S., Sobie E.A., McCulle S., Lederer W.J., Balke C.W., Cheng H. Orphaned ryanodine receptors in the failing heart. Proc Natl Acad Sci USA 2006, 103:4305-4310.
16. 2+ release from the sarcoplasmic reticulum as subcellular mechanism of cardiac contractile dysfunction. J Mol Cell Cardiol 2011, 50:390-400.
17. Blatter L.A., Kockskamper J., Sheehan K.A., Zima A.V., Huser J., Lipsius S.L. Local calcium gradients during excitation-contraction coupling and alternans in atrial myocytes. J Physiol 2003, 546:19-31.
18. Bootman M.D., Higazi D.R., Coombes S., Roderick H.L. Calcium signalling during excitation-contraction coupling in mammalian atrial myocytes. J Cell Sci 2006, 119:3915-3925.
19. Cordeiro J.M., Spitzer K.W., Giles W.R., Ershler P.E., Cannell M.B., Bridge J.H. Location of the initiation site of calcium transients and sparks in rabbit heart Purkinje cells. J Physiol 2001, 531:301-314.
20. 2+ transients of canine Purkinje cells. J Mol Cell Cardiol 2011, 50:662-669.
21. Shannon T.R., Ginsburg K.S., Bers D.M. Potentiation of fractional sarcoplasmic reticulum calcium release by total and free intra-sarcoplasmic reticulum calcium concentration. Biophys J 2000, 78:334-343.
22. 2+ fluxes in rat ventricular myocytes. J Physiol 2000, 522(Pt 2):259-270.
23. 2+ release. J Physiol (Lond) 1997, 501(Pt 1):3-16.
24. 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.
25. 2+ leak-load relationship. Circ Res 2002, 91:594-600.
26. 2+ waves in isolated rabbit ventricular cardiomyocytes. Biophys J 2007, 93:2581-2595.
27. Diaz M.E., O'Neill S.C., Eisner D.A. Sarcoplasmic reticulum calcium content fluctuation is the key to cardiac alternans. Circ Res 2004, 94:650-656.
28. Xie L.H., Sato D., Garfinkel A., Qu Z., Weiss J.N. Intracellular Ca alternans: coordinated regulation by sarcoplasmic reticulum release, uptake, and leak. Biophys J 2008, 95:3100-3110.
29. Picht E., DeSantiago J., Blatter L.A., Bers D.M. Cardiac alternans do not rely on diastolic sarcoplasmic reticulum calcium content fluctuations. Circ Res 2006, 99:740-748.
30. Restrepo J.G., Weiss J.N., Karma A. Calsequestrin-mediated mechanism for cellular calcium transient alternans. Biophys J 2008, 95:3767-3789.
31. Weiss J.N., Nivala M., Garfinkel A., Qu Z. Alternans and arrhythmias: from cell to heart. Circ Res 2011, 108:98-112.
32. Laurita K.R., Rosenbaum D.S. Cellular mechanisms of arrhythmogenic cardiac alternans. Prog Biophys Mol Biol 2008, 97:332-347.
33. Stern M.D., Cheng H.P. Putting out the fire: what terminates calcium-induced calcium release in cardiac muscle?. Cell Calcium 2004, 35:591-601.
34. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
35. 2+ sparks, and local control of excitation-contraction coupling in normal heart muscle. Circ Res 1999, 85:770-776.
36. DelPrincipe F., Egger M., Niggli E. Calcium signalling in cardiac muscle: refractoriness revealed by coherent activation. Nat Cell Biol 1999, 1:323-329.
37. Bassani J.W.M., Yuan W., Bers D.M. Fractional SR Ca release is regulated by trigger Ca and SR Ca content in cardiac myocytes. Am J Physiol 1995, 268:C1313-C1319.
38. 2+ activation and inactivation sites on the luminal side of the cardiac ryanodine receptor complex. Circ Res 2000, 87:201-206.
39. 2+ sensing sites. Biophys J 1998, 75:2801-2810.
40. 2+ sparks: an investigative mathematical model of calcium-induced calcium release. Biophys J 2002, 83:59-78.
41. 2+ release in cardiac myocytes. Circ Res 2002, 91:414-420.
42. Kabbara A.A., Allen D.G. The use of the indicator fluo-5N to measure sarcoplasmic reticulum calcium in single muscle fibres of the cane toad. J Physiol 2001, 534:87-97.
43. 2+reserve. Circ Res 2003, 93:40-45.
44. 2+ blinks: rapid nanoscopic store calcium signaling. Proc Natl Acad Sci USA 2005, 102:3099-3104.
45. Terentyev D., Viatchenko-Karpinski S., Gyorke I., Volpe P., Williams S.C., Gyorke S. Calsequestrin determines the functional size and stability of cardiac intracellular calcium stores: Mechanism for hereditary arrhythmia. Proc Natl Acad Sci USA 2003, 100:11759-11764.
46. Terentyev D., Nori A., Santoro M., Viatchenko-Karpinski S., Kubalova Z., Gyorke I., et al. Abnormal interactions of calsequestrin with the ryanodine receptor calcium release channel complex linked to exercise-induced sudden cardiac death. Circ Res 2006, 98:1151-1158.
47. Terentyev D., Kubalova Z., Valle G., Nori A., Vedamoorthyrao S., Terentyeva R., et al. 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.
48. Viatchenko-Karpinski S., Terentyev D., Gyorke I., Terentyeva R., Volpe P., Priori S.G., et al. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin. Circ Res 2004, 94:471-477.
49. Zima A.V., Picht E., Bers D.M., Blatter L.A. Partial inhibition of sarcoplasmic reticulum Ca release evokes long-lasting Ca release events in ventricular myocytes: Role of luminal Ca in termination of Ca release. Biophys J 2008, 94:1867-1879.
50. 2+ diffusion. Circ Res 2008, 103:e105-e115.
51. 2+ waves in isolated permeabilized rabbit ventricular cardiomyocytes. Biophys J 2009, 96:2744-2754.
52. 2+ in cardiomyocytes. J Physiol 2009, 587:4863-4872.
53. 2+ release refractoriness in heart muscle. Circ Res 2004, 95:807-813.
54. 2+ release in rat ventricular myocytes. J Physiol 2005, 565:441-447.
55. Ramay H.R., Liu O.Z., Sobie E.A. Recovery of cardiac calcium release is controlled by sarcoplasmic reticulum refilling and ryanodine receptor sensitivity. Cardiovasc Res 2011, 91:598-605.
56. 2+ sites. Biophys J 2007, 92:3541-3555.
57. 2+ regulation of single cardiac ryanodine receptors: insights provided by calsequestrin and its mutants. J Gen Physiol 2008, 131:325-334.
58. Gyorke I., Hester N., Jones L.R., Gyorke S. The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys J 2004, 86:2121-2128.
59. 2+ release units, impaired excitation-contraction coupling, and cardiac arrhythmias. Proc Natl Acad Sci USA 2009, 106:7636-7641.
60. Terentyev D., Viatchenko-Karpinski S., Vedamoorthyrao S., Oduru S., Gyorke I., Williams S.C., et al. Protein protein interactions between triadin and calsequestrin are involved in modulation of sarcoplasmic reticulum calcium release in cardiac myocytes. J Physiol 2007, 583:71-80.
61. 2+ wave propagation in ventricular myocytes. Biophys J 2010, 98:2515-2523.
62. Yin C.C., D'Cruz L.G., Lai F.A. Ryanodine receptor arrays: not just a pretty pattern?. Trends Cell Biol 2008, 18:149-156.
63. 2+ current. Circ Res 2001, 88:195-201.
64. Bers D.M. Excitation-contraction coupling and cardiac contractile force 2001, Kluwer Academic Publishers, Dordrecht. Second ed.
65. 2+ current through mammalian cardiac and amphibian skeletal muscle ryanodine receptor Channels under near-physiological ionic conditions. J Gen Physiol 2003, 122:407-417.
66. 2+ release (SOICR). Proc Natl Acad Sci USA 2004, 101:13062-13067.
67. 2+ activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death. Circ Res 2005, 97:1173-1181.
68. 2+ signaling in the heart: the role of ryanodine receptor sensitivity. J Gen Physiol 2010, 136:135-142.
69. Wasserstrom J.A., Shiferaw Y., Chen W., Ramakrishna S., Patel H., Kelly J.E., et al. 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.
70. Santana L.F., Kranias E.G., Lederer W.J. Calcium sparks and excitation-contraction coupling in phospholamban- deficient mouse ventricular myocytes. J Physiol (Lond) 1997, 503:21-29.
71. 2+ sparks in rat ventricular myocytes. J Physiol (Lond) 1996, 496:575-581.
72. 2+ release, and catecholaminergic polymorphic ventricular tachycardia. J Clin Invest 2006, 116:2510-2520.
73. Song L., Alcalai R., Arad M., Wolf C.M., Toka O., Conner D.A., et al. Calsequestrin 2 (CASQ2) mutations increase expression of calreticulin and ryanodine receptors, causing catecholaminergic polymorphic ventricular tachycardia. J Clin Invest 2007, 117:1814-1823.
74. Escobar A.L., Kornyeyev D., Hilliard F.A., Chopra N., Knollmann B.C. Calsequestrin Determines Refractoriness Of Calcium Release From Sarcoplasmic Reticulum Of Cardiac Muscle. Biophys J 2008, 94:898A.
75. Rizzi N., Liu N., Napolitano C., Nori A., Turcato F., Colombi B., et al. Unexpected structural and functional consequences of the R33Q homozygous mutation in cardiac calsequestrin: a complex arrhythmogenic cascade in a knock in mouse model. Circ Res 2008, 103:298-306.
76. Keller M., Kao J.P.Y., Egger M., Niggli E. Calcium waves driven by "sensitization" wave-fronts. Cardiovasc Res 2007, 74:39-45.
77. 2+ waves in rat ventricular myocytes. J Physiol (Lond) 1999, 518:173-186.
78. Swietach P., Spitzer K.W., Vaughan-Jones R.D. Modeling calcium waves in cardiac myocytes: importance of calcium diffusion. Front Biosci 2010, 15:661-680.
79. Thul R., Smith G.D., Coombes S. A bidomain threshold model of propagating calcium waves. J Math Biol 2008, 56:435-463.
80. 2+-mobility in the sarcoplasmic reticulum of ventricular myocytes is low. Biophys J 2008, 95:1412-1427.
81. 2+ store throughout cardiac myocyte. Circ Res 2006, 99:283-291.
82. Picht E., Zima A.V., Shannon T.R., Duncan A.M., Blatter L.A., Bers D.M. Dynamic calcium movement inside cardiac sarcoplasmic reticulum during release. Circ Res 2011, 108:847-856.
83. 2+ release units in cardiac myocytes. Biophys J 2004, 86:182-190.
84. 2+ sparks and in situ operation of the ryanodine receptor array in cardiac cells. Proc Natl Acad Sci USA 2004, 101:3979-3984.
85. 2+ sparks in frog skeletal muscle recorded at high time resolution. J Gen Physiol 1999, 113:187-198.
86. Rios E., Zhou J., Brum G., Launikonis B.S., Stern M.D. Calcium-dependent inactivation terminates calcium release in skeletal muscle of amphibians. J Gen Physiol 2008, 131:335-348.
87. Brochet D.X., Xie W., Yang D., Cheng H., Lederer W.J. Quarky calcium release in the heart. Circ Res 2011, 108:210-218.
88. 2+ efflux theory and practice. Prog Biophys Mol Biol 2006, 90:172-185.
89. 2+ signaling in rat ventricular myocytes with realistic transverse-axial tubular geometry and inhibited sarcoplasmic reticulum. PLoS Comput Biol 2010, 6:e1000972.
90. Izu L.T., Means S.A., Shadid J.N., Chen-Izu Y., Balke C.W. Interplay of ryanodine receptor distribution and calcium dynamics. Biophys J 2006, 91:95-112.
91. Shannon T.R., Wang F., Bers D.M. Regulation of cardiac sarcoplasmic reticulum Ca release by luminal [Ca] and altered gating assessed with a mathematical model. Biophys J 2005, 89:4096-4110.
92. Hashambhoy Y.L., Greenstein J.L., Winslow R.L. Role of CaMKII in RyR leak, EC coupling and action potential duration: a computational model. J Mol Cell Cardiol 2010, 49:617-624.
93. Greenstein J.L., Hinch R., Winslow R.L. Mechanisms of excitation-contraction coupling in an integrative model of the cardiac ventricular myocyte. Biophys J 2006, 90:77-91.
94. 2+ homeostasis in a minimal model of permeabilized ventricular myocytes. Am J Physiol Heart Circ Physiol 2010, 299:H1996-H2008.
95. Williams G.S., Huertas M.A., Sobie E.A., Jafri M.S., Smith G.D. Moment closure for local control models of calcium-induced calcium release in cardiac myocytes. Biophys J 2008, 95:1689-1703.
96. Sobie E.A. Parameter sensitivity analysis in electrophysiological models using multivariable regression. Biophys J 2009, 96:1264-1274.
97. Niederer S.A., Fink M., Noble D., Smith N.P. A meta-analysis of cardiac electrophysiology computational models. Exp Physiol 2009, 94:486-495.
98. Sarkar A.X., Sobie E.A. Regression analysis for constraining free parameters in electrophysiological models of cardiac cells. PLoS Comput Biol 2010, 6:e1000914.
99. Sobie E.A., Ramay H.R. Excitation-contraction coupling gain in ventricular myocytes: insights from a parsimonious model. J Physiol 2009, 587:1293-1299.