Modulation of ryanodine receptor Ca2+ channels (review)

Molecular Medicine Reports

Volumn 3, Issue 2, 2010, Pages 199-204

  Ozawa, Terutaka ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Calmodulin; Calsequestrin; FK506 binding protein; Phosphorylation; Ryanodine receptor

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; AMINO ACID; CAFFEINE; CALCIUM CHANNEL L TYPE; CALCIUM ION; CALMODULIN; CALSEQUESTRIN; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; CYCLIC AMP DEPENDENT PROTEIN KINASE; FK 506 BINDING PROTEIN; IODINE 125; ISOPRENALINE; MAGNESIUM ION; RUTHENIUM RED; RYANODINE RECEPTOR;

ACINAR CELL; ARTERY MUSCLE; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CORONARY ARTERY; DEPOLARIZATION; ENZYME ACTIVITY; FERTILIZATION; HEART MUSCLE; HEART MUSCLE CELL; MICROSOME; MUSCLE CELL; MUSCLE CONTRACTION; NONHUMAN; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; REVIEW; SARCOPLASMIC RETICULUM; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; SKELETAL MUSCLE; TRANSVERSE TUBULAR SYSTEM; UTERUS;

EID: 77950823179     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr-00000240     Document Type: Review

References (122)

1. Berridge MJ and Irvine RF: Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312: 315-321, 1984.
2. 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. (Pubitemid 16193720)
3. Pessah IN, Waterhouse AL and Casida JE: The calcium-ryanodine receptor complex of skeletal and cardiac muscle. Biochem Biophys Res Commun 128: 449-456, 1985. (Pubitemid 16234094)
4. Inui M, Saito A and Fleischer S: Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem 262: 1740-1747, 1987.
5. Inui M, Saito A and Fleischer S: Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures. J Biol Chem 262: 15637-15642, 1987.
6. Takeshima H, Nishimura S, Matsumoto T, Ishida H, Kangawa K, Minamino N, Matsuo H, Ueda M, Hanaoka M, Hirose T and Numa S: Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339: 439-445, 1989. (Pubitemid 19145787)
7. 2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem 265: 13472-13483, 1990. (Pubitemid 120013385)
8. Ashley RH: Activation and conductance properties of ryanodine-sensitive calcium channels from brain microsomal membranes incorporated into planar lipid bilayers. J Membr Biol 111: 179-189, 1989.
9. McPherson PS and Campbell KP: Solubilization and biochemical characterization of the high affinity [3H]ryanodine receptor from rabbit brain membranes. J Biol Chem 265: 18454-18460, 1990. (Pubitemid 20382210)
10. Shoshan-Barmatz V: High affinity ryanodine binding sites in rat liver endoplasmic reticulum. FEBS Lett 263: 317-320, 1990. (Pubitemid 20143017)
11. DiJulio DH, Watson EL, Pessah IN, Jacobson KL, Ott SM, Buck ED and Singh JC: Ryanodine receptor type III (Ry3R) identification in mouse parotid acini: properties and modulation of [3H]ryanodine-binding sites. J Biol Chem 272: 15687-15696, 1997.
12. 2+ release channel complex of skeletal muscle sarcoplasmic reticulum: evidence for a cooperatively coupled, negatively charged homotetramer. J Biol Chem 264: 16776-16785, 1989. (Pubitemid 19243576)
13. 2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol 56: 485-508, 1994. (Pubitemid 24111871)
14. Coronado R, Morrissette J, Sukhareva M and Vaughan DM: Structure and function of ryanodine receptors. Am J Physiol 266: C1485-C1504, 1994. (Pubitemid 2110133)
15. Giannini G and Sorrentino V: Molecular structure and tissue distribution of ryanodine receptor calcium channels. Med Res Rev 15: 313-323, 1995.
16. 2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265: 2244-2256, 1990. (Pubitemid 20248337)
17. Menegazzi P, Larini F, Treves S, Guerrini R, Quadroni M and Zorzato F: Identification and characterization of three calmodulin binding sites of the skeletal muscle ryanodine receptor. Biochemistry 33: 9078-9084, 1994. (Pubitemid 24272856)
18. 2+ release channel (ryanodine receptor). Biophys J 69: 106-119, 1995.
19. 2+ release in the sarcoplasmic reticulum of rabbit skeletal muscle fibres. J Physiol 487: 573-582, 1995.
20. 2+ sensitivity of skeletal and cardiac muscle ryanodine receptors in the presence of calmodulin. Am J Physiol 279: C724-C733, 2000.
21. Zhang L, Kelley J, Schmeisser G, Kobayashi YM and Jones LR: Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor: proteins of the cardiac junctional sarcoplasmic reticulum membrane. J Biol Chem 272: 23389-23397, 1997. (Pubitemid 27392481)
22. Wang S, Trumble WR, Liao H, Wesson CRCR, Dunker AK and KangCH: Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nat Struct Biol 5: 476-483, 1998. (Pubitemid 28265031)
23. Beard NA , Laver DR and Dulhunty AF: Calsequestrin and the calcium release channel of skeletal and cardiac muscle. Prog Biophys Mol Biol 85: 33-69, 2004. (Pubitemid 38431209)
24. Kawasaki T and Kasai M: Regulation of calcium channel in sarcoplasmic reticulum by calsequestrin. Biochem Biophys Res Commun 199: 1120-1127, 1994. (Pubitemid 24174775)
25. 2+ buffer inside the sarcoplasmic reticulum. Biochem J 337: 19-22, 1999. (Pubitemid 29039077)
26. Beard NA , Sakowska MM, Dulhunty AF and Laver DR : Calsequestrin is an inhibitor of skeletal muscle ryanodine receptor calcium release channels. Biophys J 82: 310-320, 2002. (Pubitemid 34289804)
27. Collins JH: Sequence anaslysis of the ryanodine receptor: possible association with a 12K, FK506-binding immunophilin/protein kinase C inhibitor. Biochem Biophys Res Commun 178: 1288-1290, 1991.
28. Jayaraman T, Brillantes A-M, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P and Marks AR : FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 267: 9474-9477, 1992.
29. Lam E, Martin MM, Timerman AP, Sabers C, Fleischer S, Lukas T, Abraham RT, O'Keefe SJ, O'Neill EA and Wiederrecht GJ: A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J Biol Chem 270: 26511-26522, 1995.
30. Timerman AP, Onoue H, Xin H-B, Barg S, Copello J, Wiederrecht G and Fleischer S: Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J Biol Chem 271: 20385-20391, 1996. (Pubitemid 26281806)
31. Timerman AP, Ogunbumni E, Freud E, Wiederrecht G, Marks AR and Fleischer S: The calcium release channel of sarcoplasmic reticulum is modulated by FK-506-binding protein: dissociation and reconstitution of FKBP-12 to the calcium release channel of skeletal muscle sarcoplasmic reticulum. J Biol Chem 268: 22992-22999, 1993. (Pubitemid 23328003)
32. 2+ from islet microsomes. J Biol Chem 272: 3133-3136, 1997. (Pubitemid 27066797)
33. Tang W-X, Chen Y-F, Zou A-P, Campbell WB and Li P-L: Role of FKBP12.6 in cAD PR-induced activation of reconstituted ryanodine receptors from arterial smooth muscle. Am J Physiol 282: H1304-H1310, 2002.
34. 2+-activated protease. J Biol Chem 259: 8550-8557, 1984. (Pubitemid 14090617)
35. Takasago T, Imagawa T, Furukawa K, Ogurusu T and Shigekawa M: Regulation of the cardiac ryanodine receptor by protein kinase-dependent phosphorylation. J Biochem 109: 163-170, 1991.
36. Suko J, Maurer-Fogy I, Plank B, Bertel O, Wyskovsky W, Hohenegger M and Hellmann G: Phosphorylation of serine 2843 in ryanodine receptor-calcium release channel of skeletal muscle by cAMP-, cGMP- and CaM-dependent protein kinase. Biochim Biophys Acta 1175: 193-206, 1993. (Pubitemid 23024891)
37. Strand MA, Louis CF and Mickelson JR: Phosphorylation of the porcine skeletal and cardiac muscle sarcoplasmic reticulum ryanodine receptor. Biochim Biophys Acta 1175: 319-326, 1993. (Pubitemid 23054320)
38. Witcher DR, Kovacs RJ, Schulman H, Cefali DC and Jones LR: Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J Biol Chem 266: 11144-11152, 1991. (Pubitemid 21906924)
39. Hain J, Nath S, Mayrleitner M, Fleischer S and Schindler H: Phosphorylation modulates the function of the calcium release channel of sarcoplasmic reticulum from skeletal muscle. Biophys J 67: 1823-1833, 1994. (Pubitemid 24342053)
40. Hain J, Onoue H, Mayrleitner M, Fleischer S and Schindler H: Phosphorylation modulates the function of the calcium release channel of sarcoplasmic reticulum from cardiac muscle. J Biol Chem 270: 2074-2081, 1995.
41. Lokuta AJ, Rogers TB, Lederer WJ and Valdivia HH: Modulation of cardiac ryanodine receptors of swine and rabbit by a phosphorylation-dephosphorylation mechanism. J Physiol 487: 609-622, 1995.
42. Rios E and Brum G: Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325: 717-720, 1987.
43. Tanabe T, Beam KG, Adams BA, Niidome T and Numa S: Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 346: 567-569, 1990.
44. Proenza C, O'Brien J, Nakai J, Mukherjee S, Allen PD and Beam KG: Identification of a region of RyR1 that participates in allosteric coupling with the α1S (CaV1.1) II-III loop. J Biol Chem 277: 6530-6535, 2002.
45. Protasi F: Structural interaction between RYRRYR s and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front Biosci 7: d650-d658, 2002.
46. N Näbauer M, Callewaert G, Cleemann L and Morad M: Regulation of calcium release is gated by calcium current, not gating charge, in cardiac myocytes. Science 244: 800-803, 1989.
47. 2+ channels and ryanodine receptors in cardiac myocytes. Proc Natl Acad Sci USA 92: 121-125, 1995.
48. Cannell MB and Soeller C: Numerical analysis of ryanodine receptor activation by L-type channel activity in the cardiac muscle diad. Biophys J 73: 112-122, 1997.
49. 2+ release in sarcoplasmic reticulum. J Biol Chem 259: 2365-2374, 1984.
50. 2+ and is modulated by Mg2+, adenine nucleotide and calmodulin. J Biol Chem 262: 3065-3073, 1987.
51. 2+ release in sea urchin egg homogenates: modulation by cyclic AD P-ribose. Science 253: 1143-1146, 1991.
52. Lee HC: Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J Biol Chem 268: 293-299, 1993.
53. 2+ channel. Nature 364: 76-79, 1993.
54. 2+ release from rat brain microsomes. FEBS Lett 318: 259-263, 1993.
55. Takasawa S, Nata K, Yonekura H and Okamoto H: Cyclic AD P-ribose in insulin secretion from pancreatic β cells. Science 259: 370-373, 1993.
56. 2+ release mechanism of rat pancreatic acinar cells is modulated by calmodulin. Biochim Biophys Acta 1452: 254-262, 1999.
57. 2+ release mechanism of rat pancreatic acinar cells: modulation by cyclic AD P-ribose and FK506. Biochim Biophys Acta 1693: 159-166, 2004.
58. Berridge MJ: A tale of two messengers. Nature 365: 388-389, 1993.
59. Lee HC, Aarhus R and Walseth TF: Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261: 352-355, 1993.
60. E Endo M: Calcium release from the sarcoplasmic reticulum. Physiol Rev 57: 71-108, 1977.
61. 2+ release channel of sarcoplasmic reticulum. J Biol Chem 261: 6300-6306, 1986.
62. Chu A, Díaz-Muñoz M, Hawkes MJ, Brush K and Hamilton SL: Ryanozine as a probe for the functional state of the skeletal muscle sarcoplasmic reticulum calcium release channel. Mol Pharmacol 37: 735-741, 1990.
63. 2+, Mg2+ and adenine nucleotides. Biochemistry 25: 236-244, 1986.
64. Laver DR , Baynes TM and Dulhunty AF: Magnesium inhibition of ryanodine-receptor calcium channels: evidence for two independent mechanisms. J Membr Biol 156: 213-229, 1997.
65. Miyamoto H and Racker E: Mechanism of calcium release from skeletal sarcoplasmic reticulum. J Membr Biol 66: 193-201, 1982.
66. Chiesi M, Schwaller R and Calviello G: Inhibition of rapid Ca-release from isolated skeletal and cardiac sarcoplasmic reticulum (SR) membranes. Biochem Biophys Res Commun 154: 1-8, 1988.
67. Ma J: Block by ruthenium red of the ryanodine-activated calcium release channel of skeletal muscle. J Gen Physiol 102: 1031-1056, 1993.
68. Yang HC, Reedy MM, Burke CL and Strasburg GM: Calmodulin interaction with the skeletal muscle sarcoplasmic reticulum calcium channel protein. Biochemistry 33: 518-525, 1994.
69. 2+ release channel. Biochemistry 38: 8532-8537, 1999.
70. Balshaw DM, Xu L, Yamaguchi N, Pasek DA and Meissner G: Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor). J Biol Chem 276: 20144-20153, 2001.
71. 2+ release channel (ryanodine receptor) by calmodulin. Biochem Biophys Res Commun 213: 1082-1090, 1995.
72. 2+-release channels from cardiac and skeletal muscle. Circ Res 64: 352-359, 1989.
73. Meissner G: Evidence of a role for calmodulin in the regulation of calcium release from skeletal muscle sarcoplasmic reticulum. Biochemistry 25: 244-251, 1986.
74. 2+ release channel (ryanodine receptor) expressed in HEK293 cells. J Biol Chem 272: 24234-24246, 1997.
75. Lee HC, Aarhus R, Graeff R, Gurnack ME and Walseth TF: Cyclic AD P ribose activation of the ryanodine receptor is mediated by calmodulin. Nature 370: 307-309, 1994.
76. Lee HC, Aarhus R and Graeff RM: Sensitization of calcium-induced calcium release by cyclic ADP-ribose and calmodulin. J Biol Chem 270: 9060-9066, 1995.
77. Yano K and Zarain-Herzberg A: Sarcoplasmic reticulum calsequestrins: structural and functional properties. Mol Cell Biochem 135: 61-70, 1994.
78. MacLennan DH and Wong PT: Isolation of a calcium-sequestering protein from sarcoplasmic reticulum. Proc Natl Acad Sci USA 68: 1231-1235, 1971.
79. 2+-binding proteins. Biochim Biophys Acta 298: 246-269, 1973.
80. Campbell KP, MacLennan DH, Jorgensen AO and Mintzer MC: Purification and characterization of calsequestrin from canine cardiac sarcoplasmic reticulum and identification of the 53,000 dalton glycoprotein. J Biol Chem 258: 1197-1204, 1983.
81. Fliegel L, Ohnishi M, Carpenter MR, Khanna VK, Reithmeier RA and MacLennan DH: Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequencing. Proc Natl Acad Sci USA 84: 1167-1171, 1987.
82. Scott BT, Simmerman HK, Collins JH, Nadal-Ginard B and Jones LR: Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J Biol Chem 263: 8958-8964, 1988.
83. Ikemoto N, Bhatnagar GM, Nagy B and Gergely J: Interaction of divalent cations with the 55,000-dalton protein component of the sarcoplasmic reticulum: studies of fluorescence and circular dichroism. J Biol Chem 247: 7835-7837, 1972.
84. Ostwald TJ and MacLennan DH: Isolation of a high affinity calcium-binding protein from sarcoplasmic reticulum. J Biol Chem 249: 974-979, 1974.
85. Cozens B and Reithmeier RA: Size and shape of rabbit skeletal muscle calsequestrin. J Biol Chem 259: 6248-6252, 1984.
86. Slupsky JR, Ohnishi M, Carpenter MR and Reithmeier RA: Characterization of cardiac calsequestrin. Biochemistry 26: 6539-6544, 1987.
87. 2+ binding effects on protein conformation and protein interactions of canine cardiac calsequestrin. J Biol Chem 263: 1376-1381, 1988.
88. Ikemoto N, Ronjat M, Mészáros LG and Koshita M: Postulated role of calsequestrin in the regulation of calcium release from sarcoplasmic reticulum. Biochemistry 28: 6764-6771, 1989.
89. Ikemoto N, Antoniu B, Kang JJ, Mészáros LG and Ronjat M: Intravesicular calcium transient during calcium release from sarcoplasmic reticulum. Biochemistry 30: 5230-5237, 1991.
90. 2+ release induced by myotoxin α in skeletal muscle sarcoplasmic reticulum. Can J Physiol Pharmacol 73: 1181-1185, 1995.
91. Györke S, Györke I, Terentyev D, Viatchenko-Karpinski S and Williams SC: Modulation of sarcoplasmic reticulum calcium release by calsequestrin in cardiac myocytes. Biol Res 37: 603-607, 2004.
92. Marks AR : Cellular functions of immunophilins. Physiol Rev 76: 631-649, 1996.
93. Brillantes A-MB, Ondriaš K, Scott A, Kobrinsky E, Ondriašová E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE and Marks AR AR : Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77: 513-523, 1994.
94. Mayrleitner N, Timerman AP, Wiederrecht G and Fleischer S: The calcium release channel of sarcoplasmic reticulum is modulated by FK-506 binding protein: effect of FKBP-12 on single channel activity of the skeletal muscle ryanodine receptor. Cell Calcium 15: 99-108, 1994.
95. Ahern GP, Junankar PR and Dulhunty AF: Single channel activity of the ryanodine receptor calcium release channel is modulated by FK-506. FEBS Lett 352: 369-374, 1994.
96. Barg S, Copello JA and Fleischer S: Different interactions of cardiac and skeletal muscle ryanodine receptors with FK-506 binding protein isoforms. Am J Physiol 272: C1726-C1733, 1997.
97. 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 and 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.
98. Kaftan E, Marks AR and Ehrlich BE: Effects of rapamycin on ryanodine receptor/Ca2+-release channels from cardiac muscle. Circ Res 78: 990-997, 1996.
99. 2+ release channel closure in rat heart. J Physiol 500: 343-354, 1997.
100. Leite MF, Dranoff JA, Gao L and Nathanson MH: Expression and subcellular localization of the ryanodine receptor in rat pancreatic acinar cells. Biochem J 337: 305-309, 1999.
101. Fitzsimmons TJ, Gukovsky I, McRoberts JA, Rodriguez E, Lai FA and Pandol SJ: Multiple isoforms of the ryanodine receptor are expressed in rat pancreatic acinar cells. Biochem J 351: 265-271, 2000.
102. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N and Marks ARAR: PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101: 365-376, 2000.
103. Takeshima H: Primary structure and expression from cDNA s of the ryanodine receptor. Ann NY Acad Sci 707: 165-177, 1993.
104. Chu A, Sumbilla C, Inesi G, Jay SD and Campbell KP: Specific association of calmodulin-dependent protein kinase and related substrates with the junctional sarcoplasmic reticulum of skeletal muscle. Biochemistry 29: 5899-5905, 1990.
105. 2+ release channel is phosphorylated at serine 2843 in intact rabbit skeletal muscle. Biol Chem Hoppe-Seyler 376: 45-49, 1995.
106. Sonnleitner A, Fleischer S and Schindler H: Gating of the skeletal calcium release channel by ATP is inhibited by protein phosphatase 1 but not by Mg2+. Cell Calcium 21: 283-290, 1997.
107. Dulhunty AF, Laver D, Curtis SM, Pace S, Haarmann C and Gallant EM: Characteristics of irreversible ATP activation suggest that native skeletal ryanodine receptors can be phosphorylated via an endogenous CaMKII. Biophys J 81: 3240-3252, 2001.
108. Igami K, Yamaguchi N and Kasai M: Regulation of depolarization-induced calcium release from skeletal muscle triads by cyclic AMP-dependent protein kinase. Jpn J Physiol 49: 81-87, 1999.
109. Takasago T, Imagawa T and Shigekawa M: Phosphorylation of the cardiac ryanodine receptor by cAMP-dependent protein kinase. J Biochem 106: 872-877, 1989.
110. Sutherland EW: Studies on the mechanism of hormone action. Science 177: 401-408, 1972.
111. Yoshida A, Takahashi M, Imagawa T, Shigekawa M, Takisawa H and Nakamura T: Phosphorylation of ryanodine receptors in rat myocytes during β-adrenergic stimulation. J Biochem 111: 186-190, 1992.
112. Valdivia HH, Kaplan JH, Ellis-Davies GC and Lederer WJ: Rapid adaptation of cardiac ryanodine receptors: modulation by Mg2+ and phosphorylation. Science 267: 1997-2000, 1995.
113. Wehrens XH, Lehnart SE, Huang F, Vest JA, Reiken SR, Mohler PJ, Sun J, Guatimosim S, Song LS, Rosemblit N, D'Armiento JM, Napolitano C, Memmi M, Priori SG, Lederer WJ and Marks AR: FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 113: 829-840, 2003.
114. Reiken S, Gaburjakova M, Gaburjakova J, He KL, Prieto A, Becker E, Yi GH, Wang J, Burkhoff D and Marks AR: β-adrenergic receptor blockers restore cardiac calcium release channel (ryanodine receptor) structure and function in heart failure. Circulation 104: 2843-2848, 2001.
115. 2+ release in heart failure. Cardiovasc Res 48: 323-331, 2000.
116. 2+ leak through ryanodine receptor in heart failure. Circulation 102: 2131-2136, 2000.
117. 2+/ calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94: e61-e70, 2004.
118. 2+-calmodulin-dependent protein kinase II on cardiac excitation-contraction coupling in ferret ventricular myocytes. J Physiol 501: 17-31, 1997.
119. Buckley NM, Penefsky ZJ and Litwak RS: Comparative force-frequency relationships in human and other mammalian ventricular myocardium. Pflugers Arch 332: 259-270, 1972.
120. 2+/calmodulin-dependent protein kinase is conserved in the brain ryanodine receptor. J Biol Chem 267: 4963-4967, 1992.
121. 2+ release from microsomal vesicles of rat parotid acinar cells. Biochem Biophys Res Commun 246: 422-425, 1998.
122. 2+ mobilization. J Biol Chem 270: 30257-30259, 1995.