Coupled gating of skeletal muscle ryanodine receptors is modulated by Ca2+, Mg2+, and ATP

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 6, 2012, Pages

  Porta, Maura ^a   Diaz Sylvester, Paula L ^b   Neumann, Jake T ^b   Escobar, Ariel L ^c   Fleischer, Sidney ^d   Copello, Julio A ^b  

^a MIDWESTERN UNIVERSITY   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of California   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

Calcium release channels; Calcium signaling; Excitation contraction coupling

Indexed keywords

ADENOSINE TRIPHOSPHATE; CAFFEINE; CALCIUM; MAGNESIUM; RYANODINE RECEPTOR 1; STRONTIUM;

ARTICLE; CALCIUM TRANSPORT; CHANNEL GATING; CONTROLLED STUDY; CYTOSOL; NONHUMAN; PH; PRIORITY JOURNAL; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; ION CHANNEL GATING; MAGNESIUM; MUSCLE, SKELETAL; RABBITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84866370648     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00150.2012     Document Type: Article

References (78)

1. Allen DG, Lamb GD, Westerblad H. Impaired calcium release during fatigue. J Appl Physiol 104: 296-305, 2008.
2. 2+ release channels. Am J Physiol Cell Physiol 271: C144-C153, 1996.
3. Barg S, Copello JA, Fleischer S. Different interactions of cardiac and skeletal muscle ryanodine receptors with FK-506 binding protein isoforms. Am J Physiol Cell Physiol 272: C1726-C1733, 1997.
4. Capes EM, Loaiza R, Valdivia HH. Ryanodine receptors. Skelet Muscle 1: 18, 2011.
5. Cheng H, Lederer WJ. Calcium sparks. Physiol Rev 88: 1491-1545, 2008.
6. 2+ release is observed in native vesicles. J Membr Biol 135: 49-59, 1993.
7. Cooke R. Modulation of the actomyosin interaction during fatigue of skeletal muscle. Muscle Nerve 36: 756-777, 2007.
8. Copello J, Porta M, Diaz-Sylvester P, Nani A, Escobar A, Fleischer S, Fill M. Coordinated gating of multiple ryanodine receptors (RyRs). Biophys J 84: 17A-17A, 2003.
9. 2+ gating of skeletal muscle and cardiac ryanodine receptors. Biophys J 73: 141-156, 1997.
10. 2+. J Membr Biol 187: 51-64, 2002.
11. Coronado R, Morrissette J, Sukhareva M, Vaughan DM. Structure and function of ryanodine receptors. Am J Physiol Cell Physiol 266: C1485-C1504, 1994.
12. Diaz-Sylvester PL, Copello JA. Voltage-dependent modulation of cardiac ryanodine receptors (RyR2) by protamine. PLos One 4: e8315, 2009.
13. 2+, and ATP. Am J Physiol Cell Physiol 294: C1103-C1112, 2008.
14. Diaz-Sylvester PL, Porta M, Copello JA. Modulation of cardiac ryanodine receptor channels by alkaline Earth cations. PLos One 6: e26693, 2011.
15. Ding S, Sachs F. Evidence for non-independent gating of P2X2 receptors expressed in Xenopus oocytes. BMC Neurosci 3: 17, 2002.
16. Eltit JM, Li H, Ward CW, Molinski T, Pessah IN, Allen PD, Lopez JR. Orthograde dihydropyridine receptor signal regulates ryanodine receptor passive leak. Proc Natl Acad Sci USA 108: 7046-7051, 2011.
17. Figueroa L, Shkryl VM, Zhou J, Manno C, Momotake A, Brum G, Blatter LA, Ellis-Davies GC, Rios E. Synthetic localized calcium transients directly probe signalling mechanisms in skeletal muscle. J Physiol 590: 1389-1411, 2012.
18. Fill M, Copello JA. Ryanodine receptor calcium release channels. Physiol Rev 82: 893-922, 2002.
19. Fill M, Zahradnikova A, Villalba-Galea CA, Zahradnik I, Escobar AL, Gyorke S. Ryanodine receptor adaptation. J Gen Physiol 116: 873-882, 2000.
20. Fleischer S. Personal recollections on the discovery of the ryanodine receptors of muscle. Biochem Biophys Res Commun 369: 195-207, 2008.
21. Fleischer S, Inui M. Biochemistry and biophysics of excitation-contraction coupling. Annu Rev Biophys Biophys Chem 18: 333-364, 1989.
22. 2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc Natl Acad Sci USA 82: 7256-7259, 1985.
23. Fleischer S, Tonomura Y, United States-Japan Cooperative Science Program. Structure and Function of Sarcoplasmic Reticulum. Proceedings of a Symposium on Structure and Function of Sacroplasmic [sic] Reticulum, held at Kansai Seminar House, Ikuno, Dojo-Cho, Kita-Ku, Kobe, Japan, November 1982. New York: Academic, 1985.
24. Franzini-Armstrong C. Functional implications of RyR-dHPR relationships in skeletal and cardiac muscles. Biol Res 37: 507-512, 2004.
25. Franzini-Armstrong C. Ultrastructural studies on feet/ryanodine receptors. In: Ryanodine Receptors, edited by Sorrentino V. Boca Raton, FL: CRC, 1995, p. 1-16.
26. 2+ release units and couplons in skeletal and cardiac muscles. Biophys J 77: 1528-1539, 1999.
27. Gaburjakova J, Gaburjakova M. Identification of changes in the functional profile of the cardiac ryanodine receptor caused by the coupled gating phenomenon. J Membr Biol 234: 159-169, 2010.
28. 2+ release in heart. Science 260: 807-809, 1993.
29. 2+. Biophys J 66: 1879-1886, 1994.
30. Klein S, Timmer J, Honerkamp J. Analysis of multichannel patch clamp recordings by hidden Markov models. Biometrics 53: 870-884, 1997.
31. Krouse ME, Wine JJ. Evidence that CFTR channels can regulate the open duration of other CFTR channels: cooperativity. J Membr Biol 182: 223-232, 2001.
32. Laver DR, Baynes TM, Dulhunty AF. Magnesium inhibition of ryanodine-receptor calcium channels: evidence for two independent mechanisms. J Membr Biol 156: 213-229, 1997.
33. Laver DR, Eager KR, Taoube L, Lamb GD. Effects of cytoplasmic and luminal pH on Ca(2+) release channels from rabbit skeletal muscle. Biophys J 78: 1835-1851, 2000.
34. 2+ inhibition of skeletal RyRs reconstituted as isolated channels or coupled clusters. J Gen Physiol 124: 741-758, 2004.
35. 2+ inhibits the ryanodine receptor from cardiac muscle. J Membr Biol 147: 7-22, 1995.
36. Ma J. Desensitization of the skeletal muscle ryanodine receptor: evidence for heterogeneity of calcium release channels. Biophys J 68: 893-899, 1995.
37. Manivannan K, Ramanan SV, Mathias RT, Brink PR. Multichannel recordings from membranes which contain gap junctions. Biophys J 61: 216-227, 1992.
38. Marx SO, Gaburjakova J, Gaburjakova M, Henrikson C, Ondrias K, Marks AR. Coupled gating between cardiac calcium release channels (ryanodine receptors). Circ Res 88: 1151-1158, 2001.
39. 2+ release channels (ryanodine receptors). Science 281: 818-821, 1998.
40. 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 101: 365-376, 2000.
41. 2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol 56: 485-508, 1994.
42. 2+, and adenine nucleotides. Biochemistry 25: 236-244, 1986.
43. 2+ current through cardiac ryanodine receptor channels under quasi-physiological ionic conditions. J Gen Physiol 113: 177-186, 1999.
44. Miller C. Ion Channel Reconstitution. New York: Plenum Press, 1986.
45. O'Brien J, Valdivia HH, Block BA. Physiological differences between the alpha and beta ryanodine receptors of fish skeletal muscle. Biophys J 68: 471-482, 1995.
46. 2+ release in frog skeletal muscle. J Muscle Res Cell Motil 31: 81-92, 2010.
47. Ondrias K, Mojzisova A. Coupled gating between individual cardiac ryanodine calcium release channels. Gen Physiol Biophys 21: 73-84, 2002.
48. Porta M, Diaz-Sylvester PL, Nani A, Fill M, Fleischer S, Copello JA. Modulation of coordinated gating of ryanodine receptor (RyR) channels in planar lipid bilayers. Biophys J 86: 241A-241A, 2004.
49. Porta M, Diaz-Sylvester PL, Nani A, Ramos-Franco J, Copello JA. Ryanoids and imperatoxin affect the modulation of cardiac ryanodine receptors by dihydropyridine receptor peptide A. Biochim Biophys Acta 1778: 2469-2479, 2008.
50. 2+ sparks. Biophys J 100: 931-938, 2011.
51. Protasi F. Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front Biosci 7: d650-658, 2002.
52. 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 160: 919-928, 2003.
53. Rios E, Brum G. Involvement of dihydropyridine receptors in excitationcontraction coupling in skeletal muscle. Nature 325: 717-720, 1987.
54. Rios E, Stern MD. Calcium in close quarters: microdomain feedback in excitation-contraction coupling and other cell biological phenomena. Annu Rev Biophys Biomol Struct 26: 47-82, 1997.
55. Rios E, Zhou J, Brum G, Launikonis BS, Stern MD. Calcium-dependent inactivation terminates calcium release in skeletal muscle of amphibians. J Gen Physiol 131: 335-348, 2008.
56. Rosales RA, Fill M, Escobar AL. Calcium regulation of single ryanodine receptor channel gating analyzed using HMM/MCMC statistical methods. J Gen Physiol 123: 533-553, 2004.
57. 2+ release channel of skeletal muscle sarcoplasmic reticulum by caffeine and related compounds. Arch Biochem Biophys 267: 75-86, 1988.
58. Saito A, Inui M, Radermacher M, Frank J, Fleischer S. Ultrastructure of the calcium release channel of sarcoplasmic reticulum. J Cell Biol 107: 211-219, 1988.
59. Saito A, Seiler S, Chu A, Fleischer S. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J Cell Biol 99: 875-885, 1984.
60. Schindler H. Planar lipid-protein membranes: strategies of formation and of detecting dependencies of ion transport functions on membrane conditions. Methods Enzymol 171: 225-253, 1989.
61. Sitsapesan R, McGarry SJ, Williams AJ. Cyclic ADP-ribose competes with ATP for the adenine nucleotide binding site on the cardiac ryanodine receptor Ca(2+)-release channel. Circ Res 75: 596-600, 1994.
62. Sitsapesan R, Williams A. The Structure and Function of Ryanodine Receptors. London, UK: Imperial College Press, 1999.
63. 2+. J Membr Biol 146: 133-144, 1995.
64. Smith JS, Coronado R, Meissner G. Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels. Nature 316: 446-449, 1985.
65. 2+. J Gen Physiol 88: 573-588, 1986.
66. Smith JS, Imagawa T, Ma J, Fill M, Campbell KP, Coronado R. Purified ryanodine receptor from rabbit skeletal muscle is the calciumrelease channel of sarcoplasmic reticulum. J Gen Physiol 92: 1-26, 1988.
67. Sobie EA, Dilly KW, dos Santos Cruz J, Lederer WJ, Jafri MS. Termination of cardiac Ca(2+) sparks: an investigative mathematical model of calcium-induced calcium release. Biophys J 83: 59-78, 2002.
68. 2+. Cell Calcium 21: 283-290, 1997.
69. Sorrentino V. Ryanodine Receptors. Boca Raton, FL: CRC, 1996.
70. Stern MD, Cheng H. Putting out the fire: what terminates calciuminduced calcium release in cardiac muscle? Cell Calcium 35: 591-601, 2004.
71. Sutko JL, Airey JA, Welch W, Ruest L. The pharmacology of ryanodine and related compounds. Pharmacol Rev 49: 53-98, 1997.
72. Trapani V, Farruggia G, Marraccini C, Iotti S, Cittadini A, Wolf FI. Intracellular magnesium detection: imaging a brighter future. Analyst 135: 1855-1866, 2010.
73. Tripathy A, Xu L, Mann G, Meissner G. Calmodulin activation and inhibition of skeletal muscle Ca2+ release channel (ryanodine receptor). Biophys J 69: 106-119, 1995.
74. Tsugorka A, Rios E, Blatter LA. Imaging elementary events of calcium release in skeletal muscle cells. Science 269: 1723-1726, 1995.
75. Velez P, Gyorke S, Escobar AL, Vergara J, Fill M. Adaptation of single cardiac ryanodine receptor channels. Biophys J 72: 691-697, 1997.
76. Zahradnikova A, Zahradnik I. Description of modal gating of the cardiac calcium release channel in planar lipid membranes. Biophys J 69: 1780-1788, 1995.
77. 2+ sparks and embers of mammalian muscle. Properties of the sources. J Gen Physiol 122: 95-114, 2003.
78. 2+ sparks demonstrated in cultured mammalian muscle. Am J Physiol Cell Physiol 290: C539-C553, 2006.