Novel aspects of excitation-contraction coupling in heart failure

Basic Research in Cardiology

Volumn 108, Issue 4, 2013, Pages

  Neef, Stefan ^a   Maier, Lars S ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Calcium; Calcium calmodulin dependent protein kinase II (CaMKII); Protein kinase A (PKA); Sarcoplasmic reticulum (SR); Sodium; SR calcium leak

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CELL PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DRONEDARONE; PHOSPHOLAMBAN; PLACEBO; PROTEIN FKBP12.6; PROTEIN SERCA2A; RANOLAZINE; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM ION; UNCLASSIFIED DRUG;

BIOACCUMULATION; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; DIASTOLIC DYSFUNCTION; EXCITATION CONTRACTION COUPLING; HEART ARRHYTHMIA; HEART ATRIUM FIBRILLATION; HEART ELECTROPHYSIOLOGY; HEART FAILURE; HEART HEMODYNAMICS; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; SARCOPLASMIC RETICULUM; SODIUM CURRENT; SYSTOLIC DYSFUNCTION;

EID: 84878396026     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-013-0360-2     Document Type: Review

References (133)

1. 2+ leak in heart failure. Circ Res 97:1314-1322. doi: 10.1161/01.RES.0000194329.41863.89
2. + exchanger attenuates the deterioration of ventricular function during pacing-induced heart failure in rabbits. Cardiovasc Res 63:273-282. doi: 10.1016/j.cardiores.2004.04.014 (Pubitemid 38906660)
3. Antos CL, Frey N, Marx SO, Reiken S, Gaburjakova M, Richardson JA, Marks AR, Olson EN (2001) Dilated cardiomyopathy and sudden death resulting from constitutive activation of protein kinase A. Circ Res 89:997-1004. doi: 10.1161/hh2301.100003 (Pubitemid 34640866)
4. V1.5 gating by multiple phosphorylation sites. J Biol Chem 287:19856-19869. doi: 10.1074/jbc.M111.322537
5. i and underlies disturbed calcium handling in the rabbit pressure and volume overload heart failure model. Cardiovasc Res 57:1015-1024. doi: 10.1016/S0008-6363(02)00809-X (Pubitemid 36324606)
6. Backs J, Backs T, Neef S, Kreusser MM, Lehmann LH, Patrick DM, Grueter CE, Qi X, Richardson JA, Hill JA, Katus HA, Bassel-Duby R, Maier LS, Olson EN (2009) The δ isoform of CaM kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload. Proc Natl Acad Sci USA 106:2342-2347. doi: 10.1073/pnas.0813013106
7. Belevych AE, Terentyev D, Terentyeva R, Nishijima Y, Sridhar A, Hamlin RL, Carnes CA, Györke S (2011) The relationship between arrhythmogenesis and impaired contractility in heart failure: role of altered ryanodine receptor function. Cardiovasc Res 90:493-502. doi: 10.1093/cvr/cvr025
8. Benkusky NA, Weber CS, Scherman JA, Farrell EF, Hacker TA, John MC, Powers PA, Valdivia HH (2007) Intact beta-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. doi: 10.1161/CIRCRESAHA.107.153007 (Pubitemid 350287197)
9. Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415:198-205. doi: 10.1038/415198a (Pubitemid 34059525)
10. Bers DM (2012) Ryanodine receptor S2808 phosphorylation in heart failure: smoking gun or red herring. Circ Res 110:796-799. doi: 10.1161/CIRCRESAHA.112. 265579
11. Böhm M, Reiger B, Schwinger RH, Erdmann E (1994) cAMP concentrations, cAMP dependent protein kinase activity, and phospholamban in non-failing and failing myocardium. Cardiovasc Res 28:1713-1719. doi: 10.1093/cvr/28.11.1713 (Pubitemid 24344147)
12. 2+ exchanger overexpression impairs frequency- and ouabain-dependent cell shortening in adult rat cardiomyocytes. Am J Physiol Heart Circ Physiol 287:H1435-H1445. doi: 10.1152/ajpheart.00397.2003 (Pubitemid 39313244)
13. Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasová E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, Marks AR (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77:513-523. doi: 10.1016/0092-8674(94)90214-3 (Pubitemid 24153992)
14. Bristow MR, Ginsburg R, Minobe W, Cubiciotti RS, Sageman WS, Lurie K, Billingham ME, Harrison DE, Stinson EB (1982) Decreased catecholamine sensitivity and beta-adrenergic receptor density in failing human hearts. N Engl J Med 307:205-211 (Pubitemid 12079105)
15. 2+ blinks: rapid nanoscopic store calcium signaling. Proc Natl Acad Sci USA 102:3099-3104. doi: 10.1073/pnas.0500059102 (Pubitemid 40299922)
16. 2+ leak promotes atrial fibrillation in mice. J Clin Invest 119:1940-1951. doi: 10.1172/JCI37059
17. 2+-ATPase delays myocardial failure after myocardial infarction in rats at a cost of increased acute arrhythmias. Circulation 109:1898-1903. doi: 10.1161/01.CIR.0000124230.60028.42 (Pubitemid 38509126)
18. i waves in cardiac myocytes. Am J Physiol 270:C148-C159
19. Coppini R, Ferrantini C, Yao L, Fan P, Del Lungo M, Stillitano F, Sartiani L, Tosi B, Suffredini S, Tesi C, Yacoub M, Olivotto I, Belardinelli L, Poggesi C, Cerbai E, Mugelli A (2013) Late sodium current inhibition reverses electro-mechanical dysfunction in human hypertrophic cardiomyopathy. Circulation 127:575-584. doi: 10.1161/CIRCULATIONAHA.112.134932
20. Curran J, Hinton MJ, Rios E, Bers DM, Shannon TR (2007) Beta-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ Res 100:391-398. doi: 10.1161/01.RES.0000258172.74570.e6
21. 2+ ATPase 2a gene delivery to restore electrical stability in the failing heart. Circulation 126:2095-2104. doi: 10.1161/CIRCULATIONAHA.111.071480
22. Czuriga D, Tóth A, Pásztor ET, Balogh A, Bodnár A, Nizsalóczki E, Lionetti V, Recchia FA, Czuriga I, Edes I, Papp Z (2012) Cell-to-cell variability in troponin I phosphorylation in a porcine model of pacing-induced heart failure. Basic Res Cardiol 107:244. doi: 10.1007/s00395-012-0244-x
23. De Keulenaer GW, Brutsaert DL (2011) Systolic and diastolic heart failure are overlapping phenotypes within the heart failure spectrum. Circulation 123:1996-2004. doi: 10.1161/CIRCULATIONAHA.110.981431
24. del Monte F, Harding SE, Schmidt U, Matsui T, Kang ZB, Dec GW, Gwathmey JK, Rosenzweig A, Hajjar RJ (1999) Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation 100:2308-2311. doi: 10.1161/01.CIR.100.23.2308
25. DeSantiago J, Maier LS, Bers DM (2004) Phospholamban is required for CaMKII-dependent recovery of Ca transients and SR Ca reuptake during acidosis in cardiac myocytes. J Mol Cell Cardiol 36:67-74. doi: 10.1016/j.yjmcc.2003.10.012 (Pubitemid 38084792)
26. Despa S, Islam MA, Weber CR, Pogwizd SM, Bers DM (2002) Intracellular Na concentration is elevated in heart failure but Na/K pump function is unchanged. Circulation 105:2543-2548. doi: 10.1161/01.CIR.0000016701.85760.97 (Pubitemid 34568978)
27. Dunlay SM, Weston SA, Jacobsen SJ, Roger VL (2009) Risk factors for heart failure: a population-based case-control study. Am J Med 122:1023-1028. doi: 10.1016/j.amjmed.2009.04.022
28. 2+ handling and increased mortality. J Am Coll Cardiol 57:469-479. doi: 10.1016/j.jacc.2010.08.639
29. Eisner DA, Kashimura T, Venetucci LA, Trafford AW (2009) From the ryanodine receptor to cardiac arrhythmias. Circ J 73:1561-1567. doi: 10.1253/circj.CJ-09-0478
30. Eisner D, Bode E, Venetucci L, Trafford A (2012) Calcium flux balance in the heart. J Mol Cell Cardiol. doi: 10.1016/j.yjmcc.2012.11.017 (Epub ahead of print)
31. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133:462-474. doi: 10.1016/j.cell.2008.02.048 (Pubitemid 351608692)
32. Fang J, Mensah GA, Croft JB, Keenan NL (2008) Heart failure-related hospitalization in the U.S., 1979 to 2004. J Am Coll Cardiol 52:428-434. doi: 10.1016/j.jacc.2008.03.061 (Pubitemid 352040814)
33. Fischer TH, Herting J, Renner A, Tirilomis T, Neef S, Gummert J, Schöndube FA, Hasenfuss G, Maier LS, Sossalla S (2012) The contribution of CaMKII and PKA to the development of an increased RyR-dependent SR Ca leak in human cardiac pathology. Circulation 126:A9785 (abstract)
34. Florea S, Anjak A, Cai WF, Qian J, Vafiadaki E, Figueria S, Haghighi K, Rubinstein J, Lorenz J, Kranias EG (2012) Constitutive phosphorylation of inhibitor-1 at Ser67 and Thr75 depresses calcium cycling in cardiomyocytes and leads to remodeling upon aging. Basic Res Cardiol 107:279. doi: 10.1007/s00395-012-0279-z
35. 2+/Calmodulin- dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes. Circ Res 99:398-406. doi: 10.1161/01.RES.0000236756.06252.13 (Pubitemid 44253696)
36. Gyorke I, Hester N, Jones LR, Gyorke S (2004) The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys J 86:2121-2128. doi: 10.1016/S0006-3495(04)74271-X (Pubitemid 38524402)
37. 2+/ calmodulin-dependent protein kinase-II in regulating diastolic stress of normal and failing hearts via titin phosphorylation. Cir Res 112(4):664-674. doi: 10.1161/CIRCRESAHA.111.300105
38. Hasenfuss G, Pieske B (2002) Calcium cycling in congestive heart failure. J Moll Cell Cardiol 34:951-969. doi: 10.1006/jmcc.2002.2037 (Pubitemid 35316143)
39. Hasenfuss G, Holubarsch C, Hermann HP, Astheimer K, Pieske B, Just H (1994) Influence of the force-frequency relationship on haemodynamics and left ventricular function in patients with non-failing hearts and in patients with dilated cardiomyopathy. Eur Heart J 15:164-170 (Pubitemid 24110691)
40. 2+-ATPase in failing and nonfailing human myocardium. Circ Res 75:434-442. doi: 10.1161/01.RES.75.3.434
41. 2+-exchanger protein levels and diastolic function of failing human myocardium. Circulation 99:641-648. doi: 10.1161/01.CIR.99.5.641 (Pubitemid 29077705)
42. He BJ, Joiner ML, Singh MV, Luczak ED, Swaminathan PD, Koval OM, Kutschke W, Allamargot C, Yang J, Guan X, Zimmerman K, Grumbach IM, Weiss RM, Spitz DR, Sigmund CD, Blankesteijn WM, Heymans S, Mohler PJ, Anderson ME (2011) Oxidation of CaMKII determines the cardiotoxic effects of aldosterone. Nat Med 17:1610-1618. doi: 10.1038/nm.2506
43. 2+ release from the sarcoplasmic reticulum in pig ventricular myocytes. Circ Res 91:1023-1030. doi: 10.1161/01.RES.0000045940.67060.DD (Pubitemid 35416639)
44. Hersel J, Jung S, Mohacsi P, Hullin R (2002) Expression of the L-type calcium channel in human heart failure. Basic Res Cardiol 97(Suppl 1):I4-I10. doi: 10.1007/s003950200022
45. Heusch G (2009) Diastolic heart failure: a misNOmer. Basic Res Cardiol 104:465-467. doi: 10.1007/s00395-009-0025-3
46. Heusch G (2011) Heart rate and heart failure. Not a simple relationship. Circ J 75:229-236. doi: 10.1253/circj.CJ-10-0925
47. Heusch G, Schulz R (2011) A radical view on the contractile machinery in human heart failure. J Am Coll Cardiol 57:310-312. doi: 10.1016/j.jacc.2010.06. 057
48. 2+/ calmodulin-dependent protein kinase in failing and nonfailing human myocardium. Circ Res 84:713-721. doi: 10.1161/01.RES.84.6.713 (Pubitemid 29157339)
49. Huke S, Bers DM (2008) Ryanodine receptor phosphorylation at Serine 2030, 2808 and 2814 in rat cardiomyocytes. Biochem Biophys Res Commun 376:80-85. doi: 10.1016/j.bbrc.2008.08.084
50. IV-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J Clin Invest 120:3508-3519. doi: 10.1172/JCI43621
51. Jessup M, Greenberg B, Mancini D, Cappola T, Pauly DF, Jaski B, Yaroshinsky A, Zsebo KM, Dittrich H, Hajjar RJ (2011) Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID) investigators. Circulation 124:304-313. doi: 10.1161/CIRCULATIONAHA.111.022889
52. 2+ release, but normal ryanodine receptors, in canine and human heart failure. Circ Res 91:1015-1022. doi: 10.1161/01.RES.0000043663. 08689.05 (Pubitemid 35416638)
53. 2+ sparks. Biophys J 75:595-600 (Pubitemid 28357502)
54. Knöll R, Kostin S, Klede S, Savvatis K, Klinge L, Stehle I, Gunkel S, Kötter S, Babicz K, Sohns M, Miocic S, Didié M, Knöll G, Zimmermann WH, Thelen P, Bickeböller H, Maier LS, Schaper W, Schaper J, Kraft T, Tschöpe C, Linke WA, Chien KR (2010) A common MLP (Muscle LIM Protein) variant is associated with cardiomyopathy. Circ Res 106:695-704. doi: 10.1161/CIRCRESAHA.109.206243
55. 2+ ATPase expression. Circulation 113:2724-2732. doi: 10.1161/CIRCULATIONAHA.105.608828 (Pubitemid 43947990)
56. Kohlhaas M, Zhang T, Seidler T, Zibrova D, Dybkova N, Steen A, Wagner S, Chen L, Brown JH, Bers DM, Maier LS (2006) Increased sarcoplasmic reticulum calcium leak but unaltered contractility by acute CaMKII overexpression in isolated rabbit cardiac myocytes. Circ Res 98:235-244. doi: 10.1161/01.RES. 0000200739.90811.9f
57. 2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice. J Clin Invest 118:2230-2245. doi: 10.1172/JCI35346 (Pubitemid 351872341)
58. +-exchanger with sabiporide attenuates the downregulation and uncoupling of the myocardial beta-adrenoceptor system in failing rabbit hearts. Br J Pharmacol 148:137-146. doi: 10.1038/sj.bjp.0706714 (Pubitemid 43873032)
59. Leineweber K, Böhm M, Heusch G (2006) Cyclic adenosine monophosphate in acute myocardial infarction with heart failure: slayer or savior? Circulation 114:365-367. doi: 10.1161/CIRCULATIONAHA.106.642132
60. + dependent. Cardiovasc Res 57:1052-1061. doi: 10.1016/S0008-6363(02) 00830-1 (Pubitemid 36324610)
61. Li Y, Kranias EG, Mignery GA, Bers DM (2002) Protein kinase A phosphorylation of the ryanodine receptor does not affect calcium sparks in mouse ventricular myocytes. Circ Res 90:309-316. doi: 10.1161/hh0302.105660 (Pubitemid 34633933)
62. 2+/calmodulin- dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. J Clin Invest 119:1230-1240. doi: 10.1172/JCI38022
63. Luo M, Guan X, Luczak ED, Di L, Kutschke W, Gao Z, Yang J, Glynn P, Sossalla S, Swaminathan PD, Weiss RM, Yang B, Rokita AG, Maier LS, Efimov I, Hund TJ, Anderson ME (2013) Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J Clin Invest 123:1262-1274. doi: 10.1172/JCI65268
64. Maack C (2013) Myocardial energetics in heart failure. Basic Res Cardiol (in press)
65. 2+ handling in isolated human atrial myocardium. Am J Physiol Heart Circ Physiol 279:H952-H958. doi: 10.1016/j.cardiores.2006.11.005
66. Maier LS, Bers DM (2007) Role of Ca/calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc Res 73:631-640. doi: 10.1016/j.cardiores.2006.11.005 (Pubitemid 46227343)
67. Maier LS, Layug B, Karwatowska-Prokopczuk E, Belardinelli L, Lee S, Sander J, Lang C, Wachter R, Edelmann F, Hasenfuss G, Jacobshagen C (2013) RAnoLazIne for the treatment of diastolic heart failure in patients with preserved ejection fraction: the RALI-DHF proof-of-concept study. JACC: Heart Fail 1:115-122.2013. doi: 10.1016/j.jchf.2012.12.002
68. i and contractile function in Langendorff-perfused rat heart. Am J Physiol 273:H1246-H1254
69. 2+ cycling contributes to improved contractile performance in SERCA2a-overexpressing transgenic rats. Cardiovasc Res 67:636-646. doi: 10.1016/j.cardiores.2005.05.006 (Pubitemid 41033359)
70. 2+ release. Circ Res 92:904-911. doi: 10.1161/01.RES.0000069685. 20258.F1 (Pubitemid 36542532)
71. Maier LS, Ziolo MT, Bossuyt J, Persechini A, Mestril R, Bers DM (2006) Dynamic changes in free Ca-calmodulin levels in adult cardiac myocytes. J Mol Cell Cardiol 41:451-458. doi: 10.1016/j.yjmcc.2006.04.020 (Pubitemid 44344277)
72. Maltsev VA, Sabbah HN, Higgins RSD, Silverman N, Lesch M, Undrovinas AI (1998) Novel, ultraslow inactivating sodium current in human ventricular cardiomyocytes. Circulation 98:2545-2552. doi: 10.1161/01.CIR.98.23.2545 (Pubitemid 29001193)
73. Marx SO, Reiken S, Hisamatsu Y, Gaburjakova M, Gaburjakova J, Yang YM, Rosemblit N, Marks AR (2001) Phosphorylation-dependent regulation of ryanodine receptors: a novel role for leucine/isoleucine zippers. J Cell Biol 153:699-708. doi: 10.1083/jcb.153.4.699 (Pubitemid 34286103)
74. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101:365-376. doi: 10.1016/S0092-8674(00)80847-8
75. 2+-ATPase and modulates excitation-contraction coupling in the heart. Basic Res Cardiol 100:250-262. doi: 10.1007/s00395-005-0518-7 (Pubitemid 41348816)
76. Meyer M, Schillinger W, Pieske B, Holubarsch C, Heilmann C, Posival H, Kuwajima G, Mikoshiba K, Just H, Hasenfuss G (1995) Alterations of sarcoplasmic reticulum proteins in failing human dilated cardiomyopathy. Circulation 92:778-784. doi: 10.1161/01.CIR.92.4.778
77. 2+-dependent ion channels in single myocytes from rat portal vein. Cell Calcium 20:153-160 (Pubitemid 26326567)
78. 2+-calmodulin-dependent protein kinase activity and expression in LV myocardium of dogs with heart failure. Am J Physiol Heart Circ Physiol 284:H876-H883. doi: 10.1152/ajpheart.00266.2002
79. Mosterd A, Cost B, Hoes AW, de Bruijne MC, Deckers JW, Hofman A, Grobbee DE (2001) The prognosis of heart failure in the general population: the Rotterdam study. Eur Heart J 22:1318-1327. doi: 10.1053/euhj.2000.2533 (Pubitemid 32737624)
80. Nattel S, Dobrev D (2012) The multidimensional role of calcium in atrial fibrillation pathophysiology: mechanistic insights and therapeutic opportunities. Eur Heart J 33:1870-1877. doi: 10.1093/eurheartj/ehs079
81. Neef S, Sag CM, Daut M, Bäumer H, Grefe C, El-Armouche A, DeSantiago J, Pereira L, Bers DM, Backs J, Maier LS (2013) While systolic cardiomyocyte function is preserved, diastolic myocyte function and recovery from acidosis are impaired in CaMKIIδ-KO mice. J Mol Cell Cardiol 59:107-116. doi: 10.1016/j.yjmcc.2013.02.014
82. 2+ levels in right atrial myocardium of patients with atrial fibrillation. Circ Res 106:1134-1144. doi: 10.1161/CIRCRESAHA.109.203836
83. 2+ leak as a novel therapeutic approach. Curr Heart Fail Rep. 4:11-17. doi: 10.1007/s11897-007- 0020-7 (Pubitemid 46663314)
84. 2+/Calmodulin-dependent protein kinase is altered in heart failure. Circ Res 86:596-605. doi: 10.1161/01.RES.86.5.596 (Pubitemid 30165052)
85. Neumann J, Eschenhagen T, Jones LR, Linck B, Schmitz W, Scholz H, Zimmermann N (1997) Increased expression of cardiac phosphatases in patients with end-stage heart failure. J Mol Cell Cardiol 29:265-272. doi: 10.1006/jmcc.1996.0271 (Pubitemid 27129150)
86. Neumann T, Ravens U, Heusch G (1998) Characterization of excitation-contraction coupling in conscious dogs with pacing-induced heart failure. Cardiovasc Res 37:456-466 (Pubitemid 28166005)
87. Packer M (1985) Sudden unexpected death in patients with congestive heart failure: a second frontier. Circulation 72:681-685. doi: 10.1161/01.CIR.72.4. 681 (Pubitemid 16245173)
88. 2+ leak and arrhythmia. Circulation 127:913-922. doi: 10.1161/CIRCULATIONAHA.12.148619
89. 2+ content in isolated failing and nonfailing human myocardium. Circ Res 85:38-46. doi: 10.1161/01.RES.85.1.38 (Pubitemid 29321040)
90. i and contractility in nonfailing and failing human myocardium. Circulation 106:447-453. doi: 10.1161/01.CIR.0000023042.50192.F4 (Pubitemid 34803689)
91. 2+ exchanger expression and function in an arrhythmogenic rabbit model of heart failure. Circ Res 85:1009-1019. doi: 10.1161/01.RES.85.11.1009
92. 2+ current in cardiac excitation-contraction coupling during action potentials. Basic Res Cardiol 106:967-977. doi: 10.1007/s00395-011-0202-z
93. Respress JL, van Oort RJ, Li N, Rolim N, Dixit SS, deAlmeida A, Voigt N, Lawrence WS, Skapura DG, Skårdal K, Wisløff U, Wieland T, Ai X, Pogwizd SM, Dobrev D, Wehrens XH (2012) Role of RyR2 phosphorylation at S2814 during heart failure progression. Circ Res 110:1474-1483. doi: 10.1161/CIRCRESAHA.112.268094
94. Rienzo M, Bizé A, Pongas D, Michineau S, Melka J, Chan HL, Sambin L, Su JB, Dubois-Randé JL, Hittinger L, Berdeaux A, Ghaleh B (2012) Impaired left ventricular function in the presence of preserved ejection in chronic hypertensive conscious pigs. Basic Res Cardiol 107:298. doi: 10.1007/s00395-012-0298-9
95. 2+/calmodulin-dependent kinase II (CaMKII). Circulation 126:2125-2139. doi: 10.1161/CIRCULATIONAHA.112.124990
96. 2+ overload in murine and human non-failing myocardium. Br J Pharmacol 167:493-504. doi: 10.1111/j.1476-5381.2012.01995.x
97. Sag CM, Dybkova N, Neef S, Maier LS (2007) Effects on recovery during acidosis in cardiac myocytes overexpressing CaMKII. J Mol Cell Cardiol 43:696-709. doi: 10.1016/j.yjmcc.2007.09.008 (Pubitemid 350166388)
98. Sag CM, Köhler AC, Anderson ME, Backs J, Maier LS (2011) CaMKII-dependent SR Ca leak contributes to doxo-rubicin-induced impaired Ca handling in isolated cardiac myocytes. J Mol Cell Cardiol 51:749-759. doi: 10.1016/j.yjmcc.2011.07.016
99. Sag CM, Wadsack DP, Khabbazzadeh S, Abesser M, Grefe C, Neumann K, Opiela MK, Backs J, Olson EN, Brown JH, Neef S, Maier SK, Maier LS (2009) Calcium/calmodulin-dependent protein kinase II contributes to cardiac arrhythmogenesis in heart failure. Circ Heart Fail 2:664-675. doi: 10.1161/CIRCHEARTFAILURE.109.865279
100. Sande JB, Sjaastad I, Hoen IB, Bøkenes J, Tønnessen T, Holt E, Lunde PK, Christensen G (2002) Reduced level of serine(16) phosphorylated phospholamban in the failing rat myocardium: a major contributor to reduced SERCA2 activity. Cardiovasc Res 53:382-391. doi: 10.1016/S0008-6363(01)00489-8 (Pubitemid 34117689)
101. 2+-exchanger on the force-frequency relation. Basic Res Cardiol 93(Suppl 1):38-45. doi: 10.1007/s003950050208 (Pubitemid 28499468)
102. 2+ transients in failing human myocardium assessed with ryanodine. J Mol Cell Cardiol 30:1285-1294. doi: 10.1006/jmcc.1998.0690 (Pubitemid 28345030)
103. Schwinger RH, Brixius K, Bavendiek U, Hoischen S, Müller-Ehmsen J, Bölck B, Erdmann E (1997) Effect of cyclopiazonic acid on the force-frequency relationship in human nonfailing myocardium. J Pharmacol Exp Ther 283:286-292 (Pubitemid 27438973)
104. 2+-sensitivity of SERCA 2a in failing human myocardium due to reduced serin-16 phospholamban phosphorylation. J Mol Cell Cardiol 31:479-491. doi: 10.1006/jmcc.1998.0897 (Pubitemid 29121635)
105. Seidler T, Teucher N, Hellenkamp K, Unsöld B, Grebe C, Kramps P, Schotola H, Wagner S, Schöndube FA, Hasenfuss G, Maier LS (2011) Limitations of FKBP12.6-directed treatment strategies for maladaptive cardiac remodeling and heart failure. J Mol Cell Cardiol 50:33-42. doi: 10.1016/j.yjmcc.2010.08.016
106. 2+ signaling mechanism in cardiac myocytes. Proc Natl Acad Sci USA 101:16683-16688. doi: 10.1073/pnas.0407537101 (Pubitemid 39557773)
107. Shan J, Betzenhauser MJ, Kushnir A, Reiken S, Meli AC, Wronska A, Dura M, Chen BX, Marks AR (2010) Role of chronic ryanodine receptor phosphorylation in heart failure and beta-adrenergic receptor blockade in mice. J Clin Invest 120:4375-4387. doi: 10.1172/JCI37649
108. 2+ leak in intact ventricular myocytes from rabbits in heart failure. Circ Res 93:592-594. doi: 10.1161/01.RES.0000093399.11734.B3 (Pubitemid 37222154)
109. 2+/calmodulin-dependent protein kinase II improves contractility in human failing myocardium. Circ Res 107:1150-1161. doi: 10.1161/CIRCRESAHA.110.220418
110. + currents in atrial fibrillation: effects of ranolazine on arrhythmias and contractility in human atrial myocardium. J Am Coll Cardiol 55:2330-2342. doi: 10.1016/j.jacc.2009.12.055
111. + current. Basic Res Cardiol 106:263-272. doi: 10.1007/s00395-010-0136-x
112. Sossalla S, Wagner S, Rasenack EC, Ruff H, Weber SL, Schöndube FA, Tirilomis T, Tenderich G, Hasenfuss G, Belardinelli L, Maier LS (2008) Ranolazine improves diastolic dysfunction in isolated myocardium from failing human hearts-role of late sodium current and intracellular ion accumulation. J Mol Cell Cardiol 45:32-43. doi: 10.1016/j.yjmcc.2008.03.006
113. 2+ leak from the sarcoplasmic reticulum. Basic Res Cardiol 105:279-287. doi: 10.1007/s00395-009-0057-8
114. Toischer K, Rokita AG, Unsöld B, Zhu W, Kararigas G, Sossalla S, Reuter SP, Becker A, Teucher N, Seidler T, Grebe C, Preuß L, Gupta SN, Schmidt K, Lehnart SE, Krüger M, Linke WA, Backs J, Regitz-Zagrosek V, Schäfer K, Field LJ, Maier LS, Hasenfuss G (2010) Differential cardiac remodeling in preload versus afterload. Circulation 122:993-1003. doi: 10.1161/CIRCULATIONAHA.110.943431
115. Ungerer M, Böhm M, Elce JS, Erdmann E, Lohse MJ (1993) Altered expression of beta-adrenergic receptor kinase and beta 1-adrenergic receptors in the failing human heart. Circulation 87:454-463 (Pubitemid 23040915)
116. Vinet L, Pezet M, Bito V, Briec F, Biesmans L, Rouet-Benzineb P, Gellen B, Prévilon M, Chimenti S, Vilaine JP, Charpentier F, Sipido KR, Mercadier JJ (2012) Cardiac FKBP12.6 overexpression protects against triggered ventricular tachycardia in pressure overloaded mouse hearts. Basic Res Cardiol 107:246. doi: 10.1007/s00395-012-0246-8
117. 2+-exchanger function underlie delayed afterdepolarizations in patients with chronic atrial fibrillation. Circulation 125:2059-2070. doi: 10.1161/CIRCULATIONAHA.111.067306
118. Wagner S, Dybkova N, Rasenack EC, Jacobshagen C, Fabritz L, Kirchhof P, Maier SK, Zhang T, Hasenfuss G, Brown JH, Bers DM, Maier LS (2006) Ca/calmodulin-dependent protein kinase II regulates cardiac Na channels. J Clin Invest 116:3127-3138. doi: 10.1172/JCI26620 (Pubitemid 44878627)
119. Wagner S, Hacker E, Grandi E, Weber SL, Dybkova N, Sossalla S, Sowa T, Bers DM, Maier LS (2009) Ca/calmodulin kinase II differentially modulates potassium currents. Circ Arrhythm Electrophysiol 2:285-294. doi: 10.1161/CIRCEP.108.842799
120. Na augmentation leading to cellular Na and Ca overload. Circ Res 108:555-565. doi: 10.1161/CIRCRESAHA.110.221911
121. 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, Marks AR (2003) FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 113:829-840. doi: 10.1016/S0092-8674(03)00434-3 (Pubitemid 36792028)
122. Wehrens XH, Lehnart SE, Marks AR (2005) Intracellular calcium release and cardiac disease. Annu Rev Physiol 67:69-98. doi: 10.1146/annurev.physiol.67. 040403.114521 (Pubitemid 40404486)
123. Wehrens XH, Lehnart SE, Reiken SR, Deng SX, Vest JA, Cervantes D, Coromilas J, Landry DW, Marks AR (2004) Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science 304:292-296. doi: 10.1126/science.1094301 (Pubitemid 38452182)
124. 2+/ calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94:61-70. doi: 10.1161/01.RES.0000125626.33738.E2
125. Wittköpper K, Fabritz L, Neef S, Ort KR, Grefe C, Unsöld B, Kirchhof P, Maier LS, Hasenfuss G, Dobrev D, Eschenhagen T, El-Armouche A (2010) Constitutively active phosphatase inhibitor-1 improves cardiac contractility in young mice but is deleterious after catecholaminergic stress and with aging. J Clin Invest 120:617-626. doi: 10.1172/JCI40545
126. Xiao B, Jiang MT, Zhao M, Yang D, Sutherland C, Lai FA, Walsh MP, Warltier DC, Cheng H, Chen SR (2005) Characterization 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. doi: 10.1161/01.RES.0000163276.26083.e8 (Pubitemid 40604968)
127. 2+-release channel (ryanodine receptor) does not dissociate 12.6-kDa FK506-binding protein (FKBP12.6). Circ Res 94:487-495. doi: 10.1161/01.RES.0000115945.89741.22 (Pubitemid 38326284)
128. 2+ handling in heart failure. J Clin Invest 115:556-564. doi: 10.1172/JCI200524159 (Pubitemid 40322225)
129. Yano M, Kobayashi S, Kohno M, Doi M, Tokuhisa T, Okuda S, Suetsugu M, Hisaoka T, Obayashi M, Ohkusa T, Kohno M, Matsuzaki M (2003) FKBP 12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation 107:477-484. doi: 10.1161/01.CIR.0000044917.74408.BE (Pubitemid 36158052)
130. Zhang H, Makarewich CA, Kubo H, Wang W, Duran JM, Li Y, Berretta RM, Koch WJ, Chen X, Gao E, Valdivia HH, Houser SR (2012) Hyperphosphorylation of the cardiac ryanodine receptor at serine 2808 is not involved in cardiac dysfunction after myocardial infarction. Circ Res 110:831-840. doi: 10.1161/CIRCRESAHA.111. 255158
131. Zhang L, Kelley J, Schmeisser G, Kobayashi YM, Jones LR (1997) Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J Biol Chem 272:23389-23397. doi: 10.1074/jbc.272.37.23389 (Pubitemid 27392481)
132. Zhang R, Khoo MS, Wu Y, Yang Y, Grueter CE, Ni G, Price EE Jr, Thiel W, Guatimosim S, Song LS, Madu EC, Shah AN, Vishnivetskaya TA, Atkinson JB, Gurevich VV, Salama G, Lederer WJ, Colbran RJ, Anderson ME (2005) Calmodulin kinase II inhibition protects against structural heart disease. Nat Med 11:409-417. doi: 10.1038/nm1215 (Pubitemid 40562331)
133. 2+/calmodulin kinase II. J Clin Invest 111:617-625. doi: 10.1172/JCI16326 (Pubitemid 36278580)