Cardiac ryanodine receptor phosphorylation by CaM kinase II: Keeping the balance right

Frontiers in Bioscience

Volumn 14, Issue 13, 2009, Pages 5134-5156

  Currie, Susan ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

Calcium; Cam kinase; Cardiac; Phosphorylation; Review; Ryanodine receptor; Sarcoplasmic reticulum

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CARRIER PROTEIN; MUSCLE PROTEIN; PHOSPHOPROTEIN PHOSPHATASE; RYANODINE RECEPTOR; SERINE; TRIADIN;

AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; CHEMISTRY; GENETICS; HEART ARRHYTHMIA; HEART FAILURE; HEART MUSCLE CELL; HUMAN; METABOLISM; PHOSPHORYLATION; REVIEW; SARCOPLASMIC RETICULUM;

AMINO ACID SEQUENCE; ANIMALS; ARRHYTHMIAS, CARDIAC; BINDING SITES; CALCIUM-BINDING PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CARRIER PROTEINS; HEART FAILURE; HUMANS; MODELS, CARDIOVASCULAR; MUSCLE PROTEINS; MYOCYTES, CARDIAC; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SERINE;

EID: 69149094813     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3591     Document Type: Article

References (136)

1. 2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states. Pharmacol Rev 49, 1-51(1997)
2. Bers D. M: Cardiac excitation-contraction coupling. Nature 415, 198-205(2002) (Pubitemid 34059525)
3. nd Ed. Kluwer Academic Press, Dordrecht, The Netherlands (2001)
4. 2+ release channel. Nat Cell Biol 2, 669-671(2000)
5. Marx S. O., Reiken S., Hisamatsu Y., Jayaraman T., Burkhoff D., Rosemblit N. and Marks A. R: PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101, 365-376(2000)
6. Bers D. M: Macromolecular complexes regulating ryanodine receptor function. J Mol Cell Cardiol 37, 417-429(2004) (Pubitemid 38953370)
7. Currie S., Loughrey C. M., Craig M. A. and Smith G. L: Calcium/calmodulin dependent protein kinase IIδ associates with the ryanodine receptor complex and regulates channel function in rabbit heart. Biochem J 377, 357-366(2004) (Pubitemid 38142191)
8. Lehnart S. E., Wehrens X. H., Reiken S., Warrier S., Belevych A. E., Harvey A. F., Richter W., Jin S. L., Conti M. and Marks A. R: Phosphodiesterase 4D deficiency in the ryanodine receptor complex promotes heart failure and arrhythmias. Cell 123, 25-35(2005) (Pubitemid 41414526)
9. Zalk R., Lehnart S. E. and Marks A. R: Modulation of the ryanodine receptor and intracellular calcium. Ann Rev Biochem 76, 367-385(2007)
10. 2+ release channel (ryanodine receptor). Biophys. J. 86, 797-804(2004) (Pubitemid 38209525)
11. Anthony D. F., Beattie J., Paul A. and Currie S: Interaction of calcium/calmodulin dependent protein kinase IIδC with sorcin indirectly modulates ryanodine receptor function in cardiac myocytes. J Mol Cell Cardiol 43, 492-503(2007) (Pubitemid 47451420)
12. Westhoff J. H., Hwang S. Y., Duncan R. S., Ozawa F., Volpe P. and Inokuchi K: Ves1/Homer proteins regulate ryanodine receptor type 2 function and intracellular calcium signaling. Cell Calcium 34, 261-269(2003) (Pubitemid 37009934)
13. Terentyev D., Viatchenko-Karpinski S., Vedamoorthyrao S., Oduru S., Györke I., Williams S. C. and Györke S: Protein-protein interactions between triadin and calsequestrin are involved in modulation of sarcoplasmic reticulum calcium release in cardiac myocytes. J Physiol 583, 71-80(2007) (Pubitemid 47244245)
14. 2+ release channel. J Clin Invest 117, 1344-1353(2007) (Pubitemid 46718422)
15. Chelu M. G. and Wehrens X. H. T: Sarcoplasmic reticulum calcium leak and cardiac arrhythmias. Biochem Soc Trans 35, 952-956(2007) (Pubitemid 350206403)
16. Bers D. M: Cardiac ryanodine receptor phosphorylation: target sites and functional consequences. Biochem J 396, e1-e3 (2006)
17. Reiken S., Gaburjakova M., Guatimosim S., Gomez A. M., D'Armiento J., Burkhoff D., Wang J., Vassort G., Lederer W. J. and Marks A. R: Protein kinase A phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. J Biol Chem 278, 444-453(2003) (Pubitemid 36043595)
18. Wehrens X. H. T., Lehnart S. E., Reiken S., Vest J. A., Wronska A. and Marks A. R: Ryanodine receptor/calcium release channel PKA phosphorylation: a critical mediator of heart failure progression. Proc Natl Acad Sci USA 103, 511-518(2006) (Pubitemid 43153055)
19. 2+signaling in severe but compensated canine left ventricular hypertrophy. Circ Res 97(5), 457-464(2005) (Pubitemid 41298176)
20. Hall S. R., Wang L., Milne B., Hong M: Left ventricular dysfunction after acute intracranial hypertension is associated with increased hydroxyl free radical production, cardiac ryanodine hyperphosphorylation and troponin I degradation. J Heart Lung Tranplant. 24(10), 1639-1649(2005) (Pubitemid 41396465)
21. Dincer U. D., Araiza A., Knudson J. D., Shao C. H., Bidasee K. R., Tune J. D: Dysfunction of cardiac ryanodine receptors in the metabolic syndrome. J. Mol. Cell. Cardiol. 41, 108-114(2006) (Pubitemid 43946971)
22. Cheng Y., George I., Yi G. H., Reiken S., Gu A., Tao Y. K., Muraskin J., Qin S., He K. L., Hay I., Yu K., Oz M. C., Burkhoff D., Holmes J., Wang J: Bradycardic therapy improves left ventricular function and remodeling in dogs with coronary embolization-induced chronic heart failure. J. Pharmacol. Exp. Ther. 321, 469-476(2007) (Pubitemid 46624487)
23. 2 cluster spacing in spontaneously hypertensive rats with heart failure. Am. J. Physiol. Heart Circ. Physiol. 293(4), H2409-2417(2007) (Pubitemid 47605888)
24. O protein. Am. J. Physiol. Heart Circ. Physiol. 294(3), H1335-1347(2008) (Pubitemid 351468732)
25. Li Y., Kranias E. G., Mignery G. A. and Bers D. M: Protein kinase A phosphorylation of the ryanodine receptor does not affect calcium sparks in mouse ventricular myocytes. Circ Res 90, 309-316(2002) (Pubitemid 34633933)
26. 2+-release channel (ryanodine receptor) does not dissociate 12.6-kDa FK506-binding protein (FKBP12.6). Circ Res 94, 487-495(2004) (Pubitemid 38326284)
27. MacDonnell S., Garcia-Rivas G., Kubo H., Chen X., Scherman J. A., Valdivia H. and Houser S. R: Adrenergic regulation of cardiac contractility does not involve phosphorylation of the cardiac ryanodine receptor at serine 2808. Circ Res 102, e65-e72 (2008) (Pubitemid 351591558)
28. Xiao B., Jiang M. T., Zhao M., Yang D., Sutherland C., Lai F. A., Walsh M. P., Warltier D. C., Cheng H. and Chen S. R. W: Characterisation of a novel PKA phosphorylation site, serine 2030, reveals no PKA hyperphosphorylation of the cardiac ryanodine receptor in canine heart failure. Circ Res 96, 847-855(2005) (Pubitemid 40604968)
29. Benkusky N. A., Weber C. S., Scherman J. A., Farrell E. F., Hacker T. A., John M. C., Powers P. A. and Valdivia H. H: Intact β-adrenergic response and unmodified progression toward heart failure in mice with genetic ablation of a major protein kinase A phosphorylation site in the cardiac ryanodine receptor. Circ Res 101, 819-829(2007) (Pubitemid 350287197)
30. Xiao B., Zhong G., Obayashi M., Yang D., Chen K., Walsh M. P., Shimoni Y., Cheng H., ter Keurs H. and Chen S. R. W: Ser-2030, but not Ser-2808, is the major phosphorylation site in cardiac ryanodine receptors responding to protein kinase A activation upon β-adrenergic stimulation in normal and failing hearts. Biochem J 396, 7-16(2006) (Pubitemid 43764491)
31. 2+ leak in heart failure. Circ Res 97, 1314-1322(2005)
32. 2+/calmodulin- dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes. Circ Res 99, 398-406(2006) (Pubitemid 44253696)
33. Curran J., Hinton M. J., Rios E., Bers D. M. and Shannon T. R: β-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin dependent protein kinase. Circ Res 100, 391-398(2007)
34. Colbran R. J: Targeting of calcium/calmodulindependent protein kinase II. Biochem J 378, 1-16(2004)
35. Hoch B., Wobus A. M., Krause E. G. and Karczewski P: δ-CaMKII expression pattern in adult mouse heart and cardiogenic differentiation of embryonic stem cells. J Cell Biochem 79, 293-300(2000)
36. Meyer T., Hanson P. I., Stryer L. and Schulman H: calmodulin trapping by calcium-calmodulin dependent protein kinase. Science 256, 1199-1202(1992)
37. 2+/calmodulindependent protein kinase II in cardiac hypertrophy and heart failure. Cardiovasc Res 63, 476-486(2004) (Pubitemid 38970192)
38. Maier L. S. and Bers D. M: Calcium, calmodulin and calcium-calmodulin kinase II: heartbeat to heartbeat and beyond. J Mol Cell Cardiol 34, 919-939(2002) (Pubitemid 35316141)
39. 2+-activated protease. J Biol Chem 259, 8550-8557(1984) (Pubitemid 14090617)
40. 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)
41. 2+ release channel complex. J Biol Chem 264, 1329-1335(1989) (Pubitemid 19038129)
42. Rardon D. P., Cefali D. C., Mitchell R. D., Seiler S. M. and Jones L. R: High molecular weight proteins purified from cardiac junctional sarcoplasmic reticulum vesicles are ryanodine sensitive calcium channels. Circ Res 64, 779-789(1989) (Pubitemid 19105313)
43. Chu A., Sumbilla C., Inesi G., Jay S. D. and Campbell K. P: Specific association of calmodulin-dependent protein kinase and related substrates with the junctional sarcoplasmic reticulum. Biochem 29, 5899-5905(1990) (Pubitemid 20201390)
44. Hohenegger M. and Suko J: Phosphorylation of the purified cardiac ryanodine receptor by exogenous and endogenous kinases. Biochem J 296, 303-308(1993) (Pubitemid 23350827)
45. Bayer K. U., Harbers K. and Schulman H: αKAP is an anchoring protein for a novel CaM kianse II isoform in skeletal muscle. EMBO J. 17, 5598-5605(1998) (Pubitemid 28445971)
46. 2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem 265, 13472-13483(1990)
47. Witcher D. R., Kovacs R. J., Schulman H., Cefali D. C. and Jones L. R: Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J Biol Chem 266, 11144-11152(1991) (Pubitemid 21906924)
48. 2+/calmodulin-dependent protein kinase is conserved in the brain ryanodine receptor. J Biol Chem 267, 4963-4967(1992)
49. 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)
50. Lokuta A. J., Rogers T. B., Lederer W. J. and Valdivia H. H: Modulation of cardiac ryanodine receptors of swine and rabbit by a phosphorylation- dephosphorylation mechanism. J Physiol 487, 609-622(1995)
51. Rodriguez P., Bhogal M. S. and Colyer J: Stoichiometric phosphorylation of cardiac ryanodine receptor on serine 2809 by calmodulin dependent kinase II and proteína kinase A. J Biol Chem 278, 38593-38600(2003) (Pubitemid 37221756)
52. C isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ Res 92, 912-919(2003) (Pubitemid 36542533)
53. 2+ handling. Circ Res 92, 904-911(2003)
54. 2+/calmodulin dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor: Circ Res 94, e61-e70 (2004)
55. Heerdt P. M., Holmes J. W., Cai B., Barbone A., Madigan J. D., Reiken S., Lee D. L., Oz M. C., Marks A. R. and Burkhoff D: Chronic unloading by left ventricular assist device reverses contractile dysfunction and alters gene expression in end stage heart failure. Circ 102, 2713-2719(2000)
56. Kohlhaas M., Zhang T., Seidler T., Zibrova D., Dybkova N., Steen A., Wagner S., Chen L., Heller Brown J., Bers D. M. and Maier L. S: Increased sarcoplasmic reticulum calcium leak but unaltered contractility by acute CaMKII overexpression in isolated rabbit cardiac myocytes. Circ Res 98, 235-244(2006)
57. 2+ release kinetics during β-adrenergic stimulation. J Mol Cell Cardiol 43, 281-291(2007) (Pubitemid 47301934)
58. 2+ current trigger. J Physiol 556, 463-470(2004)
59. 2+. J Physiol 565, 801-813(2005) (Pubitemid 40903294)
60. 2+-calmodulin dependent protein kinase II on cardiac excitation-contraction coupling in ferret ventricular myocytes. J Physiol 501, 17-31(1997) (Pubitemid 27230398)
61. Zhang T., Kohlhaas M., Backs J., Mishra S., Philips W., Dybkova N., Chang S., Ling H., Bers D. M., Maier L. S., Olson E. N. and Heller Brown J: CaMKIIδ isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses. J Biol Chem 282, 35078-35087(2007) (Pubitemid 350232479)
62. 2+ from a thapsigarginsensitive store in the nuclear envelope by activating ryanodine receptors. J Cell Biol 163, 271-282(2003) (Pubitemid 37363128)
63. Chen-Izu Y., McCulle S. L., Ward C. W., Soeller C., Allen B. M., Rabang C., Cannell M. B., Balke C. W. and Izu L. T: Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys J 91, 1-13(2006)
64. Bare D. J., Kettlun C. S., Liang M., Bers D. M. and Mignery G.: Cardiac type 2 inositol 1, 4, 5-trisphosphate receptor. J Biol Chem 280, 15912-15920(2005)
65. 2+/calmodulin kinase signalling pathway in rat cardiac myocytes. J Physiol 583, 685-694(2007) (Pubitemid 47343498)
66. Bers D. M: Going to cAMP just got more complicated. J Physiol 583, 415-416(2007) (Pubitemid 47343475)
67. 2+ waves in cardiac myocytes. Circ Res 100, 399-407(2007).
68. 2+ release units and couplons in skeletal and cardiac muscles. Biophys J 77, 1528-1539(1999)
69. Lehnart S. E., Wehrens X. H. T., Reiken S., Warrier S., Belevych A. E., Harvey R. D., Richter W., Jin S. L., Conti M. and Marks A. R: Phosphodiesterase 4D deficiency in the ryanodine receptor complex promotes heart failure and arrhythmias. Cell 123, 25-35(2005) (Pubitemid 41414526)
70. Wehrens X. H. T. and Marks A. R: Novel therapeutic approaches for heart failure by normalising calcium cycling. Nature Rev 3, 1-9(2004)
71. Van der Blieck A. M., Meyers M. B., Biedler J. L., Hes E. and Borst P: A 22kDa protein (sorcin/V19) encoded by an amplified gene in multidrug-resistant cells, is homologous to the calcium-binding light chain of calpain. EMBO J 5, 3201-3208(1986)
72. 2+-dependent processes in the full length protein. J Mol Biol 317, 447-458(2002) (Pubitemid 34722182)
73. Lokuta A. J., Meyers M. B., Sander P. R., Fishman G. I. and Valdivia H. H: Modulation of cardiac ryanodine receptors by sorcin. J Biol Chem 272, 25333-25338(1997) (Pubitemid 27415725)
74. Meyers M. B., Pickel V. M., Sheu S. S., Sharma V. K., Scotto K. W. and Fishman G. I: Association of sorcin with the ryanodine receptor. J Biol Chem 270, 26411-26418(1995)
75. 2+ channels. J Biol Chem 273, 18930-18935(1998) (Pubitemid 28366281)
76. 2+ATPase and modulates excitation-contraction coupling in the heart. Basic Res Cardiol 100, 250-262(2003)
77. Smith G. L., Elliott E. B., Kettlewell S., Currie S. and Quinn F. R: NCX expression and function in a rabbit model of myocardial infarction. J Cardiovasc Electrophysiol 17, S57-S63 (2006)
78. Farrell E. F., Antaramian A., Rueda A., Gomez A. M. and Valdivia H. H: Sorcin inhibits calcium release and modulates excitation-contraction coupling in the heart. J Biol Chem 278, 34660-34666(2003) (Pubitemid 37553315)
79. Seidler T., Miller S. L. W., Loughrey CM., Kania A., Burow A., Kettlewell S., Teucher N., Wagner S., Kogler H., Meyers M. B., Hasenfuss G. and Smith G. L: Effects of adenovirus-mediated sorcin overexpression on excitationcontraction coupling in isolated rabbit cardiomyocytes. Circ Res 93, 132-139(2003) (Pubitemid 36919700)
80. 2+ levels in the heart by sorcin and FKBP12, two accessory proteins of ryanodine receptors. Trends Pharm Sci 19, 479-482(1998)
81. 2+ release channel in skeletal muscle. Biophys. J. 83, 2539-2549(2002) (Pubitemid 35265748)
82. Bandyopadhyay A., Shin D. W., Ahn J. O. and Kim D. K: Calcineurin regulates ryanodine receptor Ca2+ release channels in rat heart. Biochem. J. 352, 61-70
83. Bultynck G., Vermassen E., Szlufcik K., De Smet P., Fissore R. A., Callewaert G., Missiaen L., DeSmedt H. and Parys J. B: Calcineurin and intracellular Ca2+ release channels: regulation or association? Biochem. Biophys. Res. Comm. 311, 1181-1193(2003) (Pubitemid 37393441)
84. Terentyev D., Viatchenko-Karpinski S., Gyorke I., Terentyeva R. and Gyorke S: Protein phosphatases decrease sarcoplasmic reticulum calcium content by stimulating calcium release in cardiac myocytes. J. Physiol. 552, 109-118(2003) (Pubitemid 37265471)
85. Zhang T., Johnson E. N., Gu Y., Morisette M. R., Sah V. P., Gigena M. S., Belke D. D., Dillmann W. H., Rogers T. B., Schulman H., Ross Jr J. and Heller Brown J: The cardiac-specific nuclear DB isoform of calcium/calmodulin dependent protein kinase II induces hypertrophy and dilated cardiomyopathy associated with increased protein phosphatase 2A activity. J Biol Chem 277, 1261-1267(2002) (Pubitemid 34968878)
86. Colpo P., Nori A., Sacchetto R., Damiani E. and Margreth A: Phosphorylation of the triadin cytoplasmic domain by CaM proteín kinase in Rabbit Fast switch muscle sarcoplasmic reticulum. Mol Cell Biochem 223, 139-145(2001) (Pubitemid 32952101)
87. Rose A. J., Alsted T. J., Kobbero J. B. and Richter EA: Regulation and function of CaMKII of fast twitch rat skeletal muscle. J Physiol 580, 993-1005(2007)
88. Jones L. R., Zhang L., Sanborn K., Jorgensen A. O. and Kelley J: Purification, primary structure and immunological characterisation of the 26kDa calsequestrin binding protein from cardiac junctional sarcoplasmic reticulum. J Biol Chem 270, 30787-30796(1995) (Pubitemid 26005148)
89. Fill M. and Copello J. A: Ryanodine receptor calcium release channels. Physiol Rev 82, 893-922(2002)
90. Huke S. and Bers D. M: Ryanodine receptor phosphorylation at Serine 2030, 2808 and 2814 in intact rat cardiomyocytes. Biophys J Suppl. S132a (2007)
91. 2+ leak in heart failure: mere observation or functional relevance? Cardiovasc Res 77, 302-314(2008) (Pubitemid 351197633)
92. Violin J. D., Zhang J., Tsien R. Y. and Newton A. C: A genetically encoded fluorescent reported reveals oscillatory phosphorylation by protein kinase C. J Cell Biol 161, 899-909(2003) (Pubitemid 36718423)
93. 2+ indicator GCaMP2. Proc Natl Acad Sci USA 103, 4753-4758(2006)
94. 2 dysfunction in arrhythmogenesis. Biophys J Suppl S 264a (2006)
95. 2+/calmodulindependent protein kinase δC activate or inhibit the cardiac ryanodine receptor ion channel? Circ Res 100, 293-295(2007)
96. Wu Y., Colbran R. J. and Anderson M. E: Calmodulin kinase is a molecular switch for cardiac excitationcontraction coupling. Proc Natl Acad Sci USA 98, 2877-2881(2001) (Pubitemid 32209577)
97. Takasago T., Imagawa T., Furukawa K., Ogurusu T. and Shikegawa M: Regulation of the cardiac ryanodine receptor by protein kinase dependent phosphorylation. J Biochem 109, 163-170(1991)
98. 2+ leak-load relationship. Circ Res 91, 594-600(2002)
99. Venetucci L. A., Trafford A. W. and Eisner D. A: Increasing ryanodine receptor open probability alone does not produce arrhythmogenic calcium waves: threshold sarcoplasmic reticulum calcium content is required. Circ Res 100, 105-111(2007) (Pubitemid 46066778)
100. Hagemann D., and Xiao R. P: Dual site phospholamban phosphorylation and its physiological relevance in the heart. Trends Cardiovasc Med 12, 51-56(2002) (Pubitemid 34145263)
101. 2+/calmodulin kinase signalling pathway. Circ Res 95, 798-806(2004) (Pubitemid 39390582)
102. Wehrens X. H. T. and Marks A. R: Altered function and regulation of cardiac ryanodine receptors in cardiac disease. Trends Biochem Sci 28, 671-678(2003) (Pubitemid 37500902)
103. Marban E: Cardiac channelopathies. Nature 415, 213-218(2002) (Pubitemid 34059527)
104. 2+ release channel dysfunction. Circ. Res. 98, 88-97(2006) (Pubitemid 43970207)
105. 2) underlie catecholaminergic polymorphic ventricular tachycardia. Circ 103, 196-200(2001) (Pubitemid 32095402)
106. 2+ leak through ryanodine receptor in heart failure. Circulation 102, 2131-2136(2000)
107. 2+/calmodulin-dependent protein kinase II. Circ Res 99, 333-335(2006) (Pubitemid 44253684)
108. Currie S. and Smith G. L: Calcium/calmodulindependent protein kinase II activity is increased in sarcoplasmic reticulum from coronary artery ligated rabbit hearts. FEBS Lett 459, 244-248(1999) (Pubitemid 29475040)
109. Maier L. S: CaMKIIδ overexpression in hypertrophy and heart failure: cellular consequences for excitationcontraction coupling. Braz J Med Biol Res 38, 1293-1302(2005) (Pubitemid 41288413)
110. 2+/calmodulin-dependent protein kinase II in vivo. Mol Endocrinol 17, 183-192(2003) (Pubitemid 36183143)
111. 2+/calmodulin-dependent protein kinase in failing and nonfailing human myocardium. Circ Res 84, 713-721(1999) (Pubitemid 29157339)
112. Currie S., Quinn F. R., Sayeed R. A., Duncan A. M., Kettlewell S. and Smith G. L: Selective down-regulation of sub-endocardial ryanodine receptor expression in a rabbit model of left ventricular dysfunction. J Mol Cell Cardiol 39, 309-317(2005) (Pubitemid 40995020)
113. Hittinger L, Ghaleh B., Chen J., Edwards J. G., Kudej R. K., Iwase M., Kim S. J., Vatner S. F. and Vatner D. E: Reduced subendocardial ryanodine receptors and consequent effects on cardiac function in conscious dogs with left ventricular hypertrophy. Circ Res 84, 999-1006(1999) (Pubitemid 29227679)
114. 2+ release, but normal ryanodine receptors, in canine and human heart failure. Circ Res 91, 1015-1022(2002) (Pubitemid 35416638)
115. 2+ channel in SR from dogs with heart failure. Am J Physiol 264, H926-H937 (1993) (Pubitemid 23109887)
116. Milnes J. Y. and MacLeod K. T: Reduced ryanodine receptor to dihydropyridine receptor ratio may underlie slower contraction in a rabbit model of left ventricular cardiac hypertrophy. J Mol Cell Cardiol 33, 473-485(2001) (Pubitemid 32539004)
117. Benkusky N. A., Farrell E. F. and Valdivia H. H: Ryanodine receptor channelopathies. Biochem Biophys Res Commun 322, 1280-1285(2004) (Pubitemid 39164657)
118. 2+ handling proteins in normal rabbit hearts and hearts with left ventricular dysfunction. J Physiol 513 P, 281 (1999)
119. Go L. O., Moschella M. C., Watras J., Handa K. K., Fyfe B. S. and Marks A. R: Differential regulation of two types of intracellular calcium release channels during endstage heart failure. J Clin Invest 95, 888-894(1995)
120. Anthony D. F., Smith G. L. and Currie S: Progression of heart failure correlates with a progressive increase in protein expression and activity of CaMKIIδ. Proc Life Sci PC102 (2007)
121. 2+ channel erupts and dribbles. Circ Res 97, 1213-1215(2005)
122. Pogwizd S. M., Schlotthauer K., Li L., Yuan W. and Bers D. M: Arrhythmogenesis and contractile dysfunction in heart failure: roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circ Res 88, 1159-1167(2001) (Pubitemid 34132516)
123. Wu Y., Roden D. M. and Anderson M. E: Calmodulin kinase inhibition prevents development of the arrhythmogenic transient inward current. Circ Res 84, 906-912(1999) (Pubitemid 29196735)
124. Anderson M. E., Braun A. P., Wu Y., Lu T., Schulman H. and Sung R. J. KN-93, an inhibitor of multifunctional CaMKII, decreases early afterdepolarisations in rabbit heart. J Pharmacol Exp Ther 287, 996-1006(1998) (Pubitemid 29131613)
125. Zhang R., Khoo M. S. C., Wu Y., Yang Y., Grueter C. E., Ni G., Price Jr E. E., Thiel W., Guatimosim S., Song L. S., Madu E. C., Shah A. N., Vishnivetskaya T. A., Atkinson J. B., Gurevich V. V., Salama G., Lederer W. J., Colbran R. J. and. Anderson M. E: Calmodulin kinase II inhibition protects against structural heart disease. Nature Med. 11, 409-417(2005) doi:10.1038/nm1215 (Pubitemid 40562331)
126. 2+ pump stimulation. Biochem J 316, 201-207(1996)
127. 2+ current in rabbit cardiomyocytes. J Physiol 554, 145-155(2004) (Pubitemid 38081449)
128. 2+/calmodulin-dependent protein kinase II regulates cardiac Na+ channels. J Clin Invest 116, 3127-3138(2006) (Pubitemid 44878627)
129. Ji Y., Li B., Reed T. D., Lorenz J. N., Kaetzel M. A. and Dedman J. R: Targeted inhibition of CaMKII in cardiac longitudinal sarcoplasmic reticulum results in decreased phospholamban phosphorylation at threonine 17. J Biol Chem 278, 25063-25071(2003) (Pubitemid 37548670)
130. 2+ current facilitation. J Mol Cell Cardiol 42, 196-205(2007) (Pubitemid 44958618)
131. Wang M. C., Dolphin A. and Kitmitto A: L-type voltage gated calcium channels: understanding function through structure. FEBS Lett 564, 245-250(2004) (Pubitemid 38520928)
132. 2+ transient amplitude in adult ventricular myocytes. Circ Res 98, 1299-1305(2006) (Pubitemid 43948085)
133. Kaneko N: New 1, 4-benzothiazepine derivative, K201, demonstrates cardioprotective effects against sudden cardiac death and intracellular calcium blocking action. Drug Dev Res 33, 429-438(1994)
134. 2 irrespective of FKBP12.6 association. Biochem J 404, 431-438(2007) (Pubitemid 46953917)
135. 2+ release in normal adult rabbit ventricular cardiomyocytes. Cardiovasc Res 76, 236-246(2007) (Pubitemid 350198587)
136. Strand M. A., Louis C. F. and Mickelson J. R: Phosphorylation of the porcine skeletal and cardiac muscle sarcoplasmic reticulum ryanodine receptor. Biochem Biophys Acta 1175, 319-326(1993) (Pubitemid 23054320)