Control of sarcoplasmic reticulum Ca2+ release by stochastic RyR gating within a 3D model of the cardiac dyad and importance of induction decay for CICR termination

Biophysical Journal

Volumn 104, Issue 10, 2013, Pages 2149-2159

  Cannell, M B ^a   Kong, C H T ^a   Imtiaz, M S ^b   Laver, D R ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; RYANODINE RECEPTOR;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CALCIUM SIGNALING; CHANNEL GATING; HEART MUSCLE; METABOLISM; PHYSIOLOGY; RAT; SARCOLEMMA; SARCOPLASMIC RETICULUM; SPRAGUE DAWLEY RAT; STATISTICS; ULTRASTRUCTURE;

ANIMALS; CALCIUM; CALCIUM SIGNALING; ION CHANNEL GATING; MODELS, BIOLOGICAL; MYOCARDIUM; RATS; RATS, SPRAGUE-DAWLEY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOLEMMA; SARCOPLASMIC RETICULUM; STOCHASTIC PROCESSES;

EID: 84878140520     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.03.058     Document Type: Article

References (71)

1. D.M. Bers Cardiac excitation-contraction coupling Nature 415 2002 198 205
2. 2+ release channel of skeletal and cardiac sarcoplasmic reticulum Mol. Cell. Biochem. 82 1988 59 65
3. 2+ release channel (ryanodine receptor) from heart and skeletal muscle sarcoplasmic reticulum Methods Enzymol. 157 1988 490 505
4. A. Fabiato Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum Am. J. Physiol. 245 1983 C1 C14
5. M.B. Cannell, J.R. Berlin, and W.J. Lederer Effect of membrane potential changes on the calcium transient in single rat cardiac muscle cells Science 238 1987 1419 1423
6. 2+]i transients in guinea pig ventricular myocytes Circ. Res. 61 1987 148 154
7. E. Picht, and A.V. Zima D.M. Bers Dynamic calcium movement inside cardiac sarcoplasmic reticulum during release Circ. Res. 108 2011 847 856
8. H. Cheng, W.J. Lederer, and M.B. Cannell Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle Science 262 1993 740 744
9. M.D. Stern Theory of excitation-contraction coupling in cardiac muscle Biophys. J. 63 1992 497 517
10. M.B. Cannell, H. Cheng, and W.J. Lederer The control of calcium release in heart muscle Science 268 1995 1045 1049
11. J.R. López-López, and P.S. Shacklock W.G. Wier Local calcium transients triggered by single L-type calcium channel currents in cardiac cells Science 268 1995 1042 1045
12. M.B. Cannell, and C.H.T. Kong Local control in cardiac E-C coupling J. Mol. Cell. Cardiol. 52 2012 298 303
13. M.D. Stern, and H. Cheng Putting out the fire: what terminates calcium-induced calcium release in cardiac muscle? Cell Calcium 35 2004 591 601
14. 2+ sparks in rat ventricular myocytes J. Physiol. 507 1998 667 677
15. X. Koh, and B. Srinivasan A. Levchenko A 3D Monte Carlo analysis of the role of dyadic space geometry in spark generation Biophys. J. 90 2006 1999 2014
16. 2+ and phosphorylation Science 267 1995 1997 2000
17. 2+ oscillations Biophys. J. 71 1996 3477 3487
18. 2+ sparks: an investigative mathematical model of calcium-induced calcium release Biophys. J. 83 2002 59 78
19. S.O. Marx, and J. Gaburjakova A.R. Marks Coupled gating between cardiac calcium release channels (ryanodine receptors) Circ. Res. 88 2001 1151 1158
20. H.R. Ramay, O.Z. Liu, and E.A. Sobie Recovery of cardiac calcium release is controlled by sarcoplasmic reticulum refilling and ryanodine receptor sensitivity Cardiovasc. Res. 91 2011 598 605
21. T. Guo, D. Gillespie, and M. Fill Ryanodine receptor current amplitude controls Ca2+ sparks in cardiac muscle Circ. Res. 111 2012 28 36
22. 2+ diffusion Circ. Res. 103 2008 e105 e115
23. 2+ reserve Circ. Res. 93 2003 40 45
24. D.R. Laver, and C.H.T. Kong M.B. Cannell Termination of calcium-induced calcium release by induction decay: an emergent property of stochastic channel gating and molecular scale architecture J. Mol. Cell. Cardiol. 54 2013 98 100
25. 2+ release in rat ventricular myocytes J. Physiol. 565 2005 441 447
26. 2+ delivery system in muscle cells Appl. Physiol. Nutr. Metab. 34 2009 323 327
27. D.W. Fawcett, and N.S. McNutt The ultrastructure of the cat myocardium. I. Ventricular papillary muscle J. Cell Biol. 42 1969 1 45
28. M.S. Forbes, and E.E. van Neil Membrane systems of guinea pig myocardium: ultrastructure and morphometric studies Anat. Rec. 222 1988 362 379
29. W.G. Forssmann, and L. Girardier A study of the T system in rat heart J. Cell Biol. 44 1970 1 19
30. 2+ current through cardiac ryanodine receptor channels under quasi-physiological ionic conditions J. Gen. Physiol. 113 1999 177 186
31. 2+ current through mammalian cardiac and amphibian skeletal muscle ryanodine receptor channels under near-physiological ionic conditions J. Gen. Physiol. 122 2003 407 417
32. C. Soeller, and M.B. Cannell Numerical simulation of local calcium movements during L-type calcium channel gating in the cardiac diad Biophys. J. 73 1997 97 111
33. 2+ sites Clin. Exp. Pharmacol. Physiol. 34 2007 889 896
34. 2+ release: cytoplasmic and luminal regulation modeled in a tetrameric channel J. Gen. Physiol. 132 2008 429 446
35. 2+]i during excitation-contraction coupling in cardiac myocytes Biophys. J. 67 1994 1942 1956
36. 2+]i waves in cardiac myocytes Am. J. Physiol. 270 1996 C148 C159
37. 2+ channels and ryanodine receptors in heart cells Nature 410 2001 592 596
38. 2+ diffusion Circ. Res. 103 2008 e105 e115
39. 2+ blinks: rapid nanoscopic store calcium signaling Proc. Natl. Acad. Sci. USA 102 2005 3099 3104
40. C.H.T. Kong, D.R. Laver, and M.B. Cannell Extraction of sub-microscopic Ca fluxes from blurred and noisy fluorescent indicator images with a detailed model fitting approach PLOS Comput. Biol. 9 2013 e1002931 e1002937
41. 2+]i during excitation-contraction coupling in cardiac myocytes Circ. Res. 76 1995 236 241
42. L.F. Santana, E.G. Kranias, and W.J. Lederer Calcium sparks and excitation-contraction coupling in phospholamban-deficient mouse ventricular myocytes J. Physiol. 503 1997 21 29
43. 2+ sparks Biophys. J. 82 2002 2396 2414
44. M.B. Cannell, and C. Soeller Numerical analysis of ryanodine receptor activation by L-type channel activity in the cardiac muscle diad Biophys. J. 73 1997 112 122
45. E.A. Sobie, and W.J. Lederer Dynamic local changes in sarcoplasmic reticulum calcium: physiological and pathophysiological roles J. Mol. Cell. Cardiol. 52 2012 304 311
46. E.R. Higgins, and P. Goel J. Sneyd Modelling calcium microdomains using homogenisation J. Theor. Biol. 247 2007 623 644
47. H. Cheng, and L.S. Song M.D. Stern Amplitude distribution of calcium sparks in confocal images: theory and studies with an automatic detection method Biophys. J. 76 1999 606 617
48. 2+ sparks evoked by action potentials in mouse ventricular myocytes J. Physiol. 518 1999 469 478
49. 2+ sparks and in situ operation of the ryanodine receptor array in cardiac cells Proc. Natl. Acad. Sci. USA 101 2004 3979 3984
50. 2+ release units in cardiac myocytes Biophys. J. 86 2004 182 190
51. D. Baddeley, and I.D. Jayasinghe C. Soeller Optical single-channel resolution imaging of the ryanodine receptor distribution in rat cardiac myocytes Proc. Natl. Acad. Sci. USA 106 2009 22275 22280
52. 2+ signaling in the heart J. Cell Sci. 122 2009 1005 1013
53. 2+/calmodulin-dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes Circ. Res. 99 2006 398 406
54. 2+/calmodulin- dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor Circ. Res. 94 2004 e61 e70
55. K.M. Dibb, and H.K. Graham A.W. Trafford Analysis of cellular calcium fluxes in cardiac muscle to understand calcium homeostasis in the heart Cell Calcium 42 2007 503 512
56. S.R. Shorofsky, and R. Aggarwal C.W. Balke Cellular mechanisms of altered contractility in the hypertrophied heart: big hearts, big sparks Circ. Res. 84 1999 424 434
57. 2+ sparks in myocytes from infarcted hearts Circ. Res. 87 2000 1040 1047
58. D. Gillespie, and M. Fill Pernicious attrition and inter-RyR2 CICR current control in cardiac muscle J. Mol. Cell. Cardiol. 58 2013 53 58
59. 2+ inhibition of skeletal RyRs reconstituted as isolated channels or coupled clusters J. Gen. Physiol. 124 2004 741 758
60. 2+ release, and catecholaminergic polymorphic ventricular tachycardia J. Clin. Invest. 116 2006 2510 2520
61. S. McLaughlin, and N. Mulrine A. McLaughlin Adsorption of divalent cations to bilayer membranes containing phosphatidylserine J. Gen. Physiol. 77 1981 445 473
62. F. Protasi, C. Franzini-Armstrong, and B.E. Flucher Coordinated incorporation of skeletal muscle dihydropyridine receptors and ryanodine receptors in peripheral couplings of BC3H1 cells J. Cell Biol. 137 1997 859 870
63. A. Saito, and M. Inui S. Fleischer Ultrastructure of the calcium release channel of sarcoplasmic reticulum J. Cell Biol. 107 1988 211 219
64. C. Soeller, and M.B. Cannell Examination of the transverse tubular system in living cardiac rat myocytes by 2-photon microscopy and digital image-processing techniques Circ. Res. 84 1999 266 275
65. N. Rizzi, and N. Liu S.G. Priori 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. 103 2008 298 306
66. 2+ release units and couplons in skeletal and cardiac muscles Biophys. J. 77 1999 1528 1539
67. M.S. Forbes, and N. Sperelakis Bridging junctional processes in couplings of skeletal, cardiac, and smooth muscle Muscle Nerve 5 1982 674 681
68. D.M. Bers Excitation-Contraction Coupling and Cardiac Contractile Force 2001 Kluwer Academic Dordrecht, The Netherlands
69. 2+-binding protein changes in CSQ2 knockout mice Am. J. Physiol. Heart Circ. Physiol. 300 2011 H595 H604
70. N. Ikemoto, and B. Nagy J. Gergely Studies on a metal-binding protein of the sarcoplasmic reticulum J. Biol. Chem. 249 1974 2357 2365
71. 2+ store throughout cardiac myocyte Circ. Res. 99 2006 283 291