Phospholamban phosphorylation by CaMKII under pathophysiological conditions

Frontiers in Bioscience

Volumn 13, Issue 15, 2008, Pages 5988-6005

  Vittone, Leticia ^a   Mundina Weilenmann, Cecilia ^a   Mattiazzi, Alicia ^a  

^a FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

Acidosis; CaMKII; Heart Failure; Ischemia Reperfusion Injury; Phospholamban phosphorylation; Review; Stunning

Indexed keywords

CALCIUM BINDING PROTEIN; PHOSPHOLAMBAN; PROTEIN KINASE (CALCIUM,CALMODULIN) II; THREONINE;

ACIDOSIS; ENZYME SPECIFICITY; HEART FAILURE; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHOSPHORYLATION; REPERFUSION INJURY; REVIEW; STUNNED HEART MUSCLE; VASOCONSTRICTION; VASODILATATION;

ACIDOSIS; CALCIUM-BINDING PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; HEART FAILURE; HUMANS; MYOCARDIAL STUNNING; PHOSPHORYLATION; REPERFUSION INJURY; SUBSTRATE SPECIFICITY; THREONINE; VASOCONSTRICTION; VASODILATION;

EID: 52049115619     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3131     Document Type: Review

References (129)

1. A Fabiato, F Fabiato: Calcium release from the sarcoplasmic reticulum. Circ Res 40, 119-129 (1977) (Pubitemid 8043430)
2. M Tada, T Toyofuku: Molecular regulation of phospholamban function and expression. Trends Cardiovasc Med 8, 330-340 (1998) (Pubitemid 28565197)
3. B Pieske, LS Maier, DM Bers, G Hasenfuss: Ca2+ handling and sarcoplasmic reticulum Ca2+ content in isolated failing and nonfailing human myocardium. Circ Res 85, 38-46 (1999) (Pubitemid 29321040)
4. J Fujii, A Ueno, K Kitano, S Tanaka, M Kadoma, M Tada: Complete complementary DNA-derived amino acid sequence of canine cardiac phospholamban. J Clin Invest 79, 301-304 (1987) (Pubitemid 17232533)
5. P James, M Inui, M Tada, M Chiesi, E Carafoli: Nature and site of phospholamban regulation of the Ca 2+ pump of sarcoplasmic reticulum. Nature 342, 90-92 (1989) (Pubitemid 19271123)
6. T Cantilina, Y Sagara, G Inesi, LR Jones: Comparative studies of cardiac and skeletal sarcoplasmic reticulum ATPases. Effect of a phospholamban antibody on enzyme activation by Ca2+. J Biol Chem 268, 17018-17025 (1993) (Pubitemid 23236927)
7. Z Chen, BL Akin, LR Jones: Mechanism of reversal of phospholamban inhibition of the cardiac Ca2+-ATPase by protein kinase A and by anti-phospholamban monoclonal antibody 2D12. J Biol Chem 282, 20968-20976 (2007) (Pubitemid 47099943)
8. DH MacLennan, EG Kranias: Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4, 566-577 (2003) (Pubitemid 36773408)
9. M Asahi, E McKenna, K Kurzydlowski, M Tada, DH MacLennan: Physical interactions between phospholamban and sarco (endo)plasmic reticulum Ca2+-ATPases are dissociated by elevated Ca2+, but not by phospholamban phosphorylation, vanadate, or thapsigargin, and are enhanced by ATP. J Biol Chem 275, 5034-5038 (2000)
10. RL Cornea, LR Jones, JM Autry, DDThomas. Mutation and phosphorylation change the oligomeric structure of phospholamban in lipid bilayers. Biochemistry 36, 2960-2967 (1997) (Pubitemid 27138580)
11. LG Reddy, LR Jones, DD Thomas: Depolymerization of phospholamban in the presence of calcium pump: a fluorescence energy transfer study. Biochemistry 38, 3954-3962 (1999)
12. W Luo, IL Grupp, J Harrer, S Ponniah, G Grupp, JJ Duffy, T Doetschman, EG Kranias: Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of β-agonist simulation. Circ Res 75, 401-409 (1994)
13. BD Hoit, SF Khoury, EG Kranias, N Ball, RA Walsh: In vivo echocardiographic detection of enhanced left ventricular function in genetargeted mice with phospholamban deficiency. Circ Res 77, 632-637 (1995)
14. G Chu, W Luo, JP Slack, C Tilgmann, WE Sweet, M Spindler, KW Saupe, GP Boivin, CS Moravec, MA Matlib, IL Grupp, JS Ingwall, EG Kranias: Compensatory mechanisms associated with the hyperdynamic function of phospholamban-deficient mouse hearts. Circ Res 79, 1064-1076 (1996) (Pubitemid 26404139)
15. VJ Kadambi, S Ponniah, J Harrer, B Hoit, GW Dorn, RA Walsh, EG Kranias : Cardiac-specific overexpression of phospholamban alters calcium kinetics and resultant cardiomyocyte mechanics in transgenic mice. J Clin Invest 97, 533-539 (1996) (Pubitemid 26039421)
16. W Luo, BM Wolska, IL Grupp, JM Harrer, K Haghighi, DG Ferguson, JP Slack, G Grupp, T Doetschman, RJ Solaro, EG Kranias: Phospholamban gene dosage effects in the mammalian heart. Circ Res 78, 839-847 (1996) (Pubitemid 26131368)
17. JP Lindemann, LR Jones, DR Hathaway, BG Henry, AM Watanabe: β-adrenergic simulation of phospholamban phosphorylation and Ca2+-ATPase activity in guinea pig ventricles. J Biol Chem 258, 464-471 (1983) (Pubitemid 13165769)
18. JP Lindemann, AM Watanabe: Phosphorylation of phospholamban in intact myocardium. Role of Ca2+-calmodulin-dependent mechanisms. J Biol Chem 260, 4516-4525 (1985) (Pubitemid 15092936)
19. AD Wegener, HKB Zimmermann, JP Lindenmann, LR Jones: Phospholamban phosphorylation in intact ventricles: phosphorylation of serine 16 and threonine 17 in response to beta-adrenergic stimulation. J Biol Chem 261, 5154-5159 (1986)
20. C Mundiña-Weilenmann, L Vittone, G Chiappe de Cingolani, A Mattiazzi: Dissociation between contraction and relaxation: the possible role of phospholamban phosphorylation. Basic Res Cardiol 82, 507-516 (1987) (Pubitemid 18012240)
21. P Karczewski, S Bartel, H Haase, EG Krause: Isoproterenol induces both cAMP-and calcium-dependent phosphorylation of phospholamban in canine heart in vivo. Biomed Biochem Acta 46, S433-S439 (1987) (Pubitemid 18043484)
22. L Vittone, C Mundiña, G Chiappe de Cingolani, A Mattiazzi: cAMP and calcium dependent mechanisms of phospholamban phosphorylation in intact hearts. Am J Physiol Heart Circ Physiol 258, H318-H325 (1990) (Pubitemid 20103152)
23. C Mundiña-Weilenmann, L Vittone, M Ortale, G Chiappe de Cingolani, A Mattiazzi: Immunodetection of phosphorylation sites gives new insights into the mechanisms underlying phospholamban phosphorylation in the intact heart. J Biol Chem 271, 33561-33567 (1996) (Pubitemid 27010172)
24. SC Calaghan, E White, J Colyer: Co-ordinated changes in cAMP, phosphorylated phospholamban, Ca2+ and contraction following beta-adrenergic stimulation of rat heart. Pflugers Arch 436, 948-956 (1998)
25. M Kuschel, P Karczewski, P Hempel, WP Schlegel, EG Krause, S Bartel: Ser16 prevails over Thr17 phospholamban phosphorylation in the beta-adrenergic regulation of cardiac relaxation. Am J Physiol Heart Circ Physiol 276, H1625-H1633 (1999) (Pubitemid 29246550)
26. Bartel, D Vetter, WP Schlegel, G Wallukat, EG Krause, P Karczewski: Phosphorylation of phospholamban at threonine-17 in the absence and presence of beta-adrenergic stimulation in neonatal rat cardiomyocytes. J Mol Cell Cardiol 32, 2173-2185 (2000) (Pubitemid 32039769)
27. M Said, C Mundiña-Weilenmann, L Vittone, A Mattiazzi: The relative relevance of phosphorylation of the Thr17 residue of phospholamban is different at different levels of beta-adrenergic stimulation. Pflugers Arch 444, 801-809 (2002) (Pubitemid 35204029)
28. LK MacDougall, Larry Jones, Philip Cohen: Identification of the major protein phosphatases in mammalian cardiac muscle which dephosphorylate phospholamban. Eur J Biochem 196, 725-734 (1991)
29. C Mundiña-Weilenmann, P Ferrero, M Said, L Vittone, E Kranias, A Mattiazzi: Role of phosphorylation of Thr17 residue of phospholamban in mechanical recovery during hypercapnic acidosis. Cardiovas Res 66, 114-122 (2005) (Pubitemid 40357874)
30. A Mattiazzi, C Mundiña-Weilenmann, C Guoxiang, L Vittone, E Kranias: Role of phospholamban phosphorylation on Thr17 in cardiac physiological and pathological conditions. Cardiovasc Res 68, 366-375 (2005) (Pubitemid 41566556)
31. S Huke, DM Bers: Temporal dissociation of frequencydependent acceleration of relaxation and protein phosphorylation by CaMKII. J Mol Cell Cardiol 42, 590-599 (2007) (Pubitemid 46349126)
32. A Hudmon, H Schulman: Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J 364, 593-611 (2002) (Pubitemid 34680833)
33. CF Edman, H Schulman: Identification and characterization of B-CaM kinase and C-CaM kinase from rat heart, two new multifunctional Ca2+/ calmodulindependent protein kinase isoforms. Biochim Biophys Acta 1221, 89-101 (1994)
34. A Ishida, Y Shigeri, T Taniguchi, I Kameshita: Protein phosphatases that regulate multifunctional Ca2+/calmodulin-dependent protein kinases: from biochemistry to pharmacology. Pharmacol Ther 100, 291-305 (2003) (Pubitemid 37494910)
35. RJ Colbran: Targeting of calcium/calmodulindependent protein kinase II. Biochem J 378, 1-16 (2004)
36. Y Wu, LB MacMillan, RB McNeill, RJ Colbran, ME Anderson: CaM kinase augments cardiac L-type Ca2+ current: a cellular mechanism for long Q-T arrhythmias. Am J Physiol Heart Circ Physiol 276, H2168-H2178 (1999) (Pubitemid 29323505)
37. CE Grueter, SA Abiria, I Dzhura, Y Wu, AJ Ham, PJ Mohler, ME Anderson, RJ Colbran: L-type Ca2+ channel facilitation mediated by phosphorylation of the beta subunit by CaMKII. Mol Cell 23, 641-650 (2006) (Pubitemid 44292555)
38. S Currie, CM Loughrey, MA Craig, GL Smith: Calcium/calmodulin-dependent protein kinase II delta associates with the ryanodine receptor complex and regulates channel function in rabbit heart. Biochem J 377, 357-366 (2004) (Pubitemid 38142191)
39. A Xu, T Netticadan, DL Jones, N Narayanan: Serine phosphorylation of the sarcoplasmic reticulum Ca2+-ATPase in the intact beating rabbit heart. Biochem Biophys Res Commun 264, 241-246 (1999) (Pubitemid 29500495)
40. A Xu, N Narayanan: Reversible inhibition of the calcium-pumping ATPase in native cardiac sarcoplasmic reticulum by a calmodulin-binding peptide. Evidence for calmodulin-dependent regulation of the Vmax of calcium transport. J Biol Chem 275, 4407-4416 (2000) (Pubitemid 30094851)
41. LM Bilezikjian, EG Kranias, JD Potter, A Schwartz: Studies on phosphorylation of canine cardiac sarcoplasmic reticulum by calmodulin-dependent protein kinase. Circ Res 49, 1356-1362 (1981) (Pubitemid 12246605)
42. J Tsui, M Inagaki, H Schulman: Calcium/calmodulindependent protein kinase II (CaMKII) localization acts in concert with substrate targeting to create spatial restriction for phosphorylation. J Biol Chem 280, 9210-9216 (2005) (Pubitemid 40409611)
43. A Hudmon, J Aronowski, SJ Kolb, MN Waxham: Inactivation and self-association of Ca2+/calmodulindependent protein kinase II during autophosphorylation. J Biol Chem 271, 8800-8808 (1996)
44. A Hudmon, E Lebel, H Roy, A Sik, H Schulman, MN Waxham, P De Koninck: A mechanism for Ca2+/calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association. J Neurosci 25, 6971-6983 (2005) (Pubitemid 41077005)
45. W Luo, G Chu, Y Sato, Z Zhou, VJ Kadambi, Evangelia Kranias: Transgenic approaches to define the functional role of dual site phospholamban phosphorylation. J Biol Chem 73, 4734-4739 (1998) (Pubitemid 28103222)
46. G Chu, JW Lester, KB Young, W Luo, J Zhai, Evangelia Kranias: A single site (Ser16) phosphorylation in phospholamban is sufficient in mediating its maximal cardiac responses to beta-agonists. J Biol Chem 275, 38938-38943 (2000) (Pubitemid 32009233)
47. L Pereira, M Metrich, M Fernandez-Velasco, A Lucas, J Leroy, R Perrier, E Morel, R Fischmeister, S Richard, JP Benitah, F Lezoualc'h, AM Gomez: The cAMP binding protein Epac modulates Ca2+ sparks by Ca2+/calmodulin kinase signalling pathway in rat cardiac myocytes. J Physiol 583, 685-694 (2007) (Pubitemid 47343498)
48. JL Bos: Epac: A new cAMP target and new avenues in cAMP research. Nat Rev Mol Cell Biol 4, 733-738 (2003) (Pubitemid 37082188)
49. J Curran, MJ Hinton, Eduardo Rios, Donald Bers, TR Shannon: Beta-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ Res 100, 391-398 (2007)
50. P Ferrero, M Said, G Sanchez, L Vittone, C Valverde, P Donoso, A Mattiazzi, C Mundiña-Weilenmann. Ca2+/calmodulin kinase II increases ryanodine binding and Ca2+-induced sarcoplasmic reticulum Ca2+ release kinetics during beta-adrenergic stimulation. J Mol Cell Cardiol 43, 281-291 (2007) (Pubitemid 47301934)
51. De Koninck, H Schulman: Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 79, 227-230 (1998) (Pubitemid 28103880)
52. D Hagemann, M Kuschel, T Kuramochi, W Zhu, H Cheng, RP Xiao: Frequency-encoding Thr17 phospholamban phosphorylation is independent of Ser16 phosphorylation in cardiac myocytes. J Biol Chem 275, 22532-22536 (2000) (Pubitemid 30621843)
53. C Valverde, C Mundiña-Weilenmann, M Said, P Ferrero, L Vittone, M Salas, J Palomeque, M Vila Petroff, A Mattiazzi: Frequency-dependent acceleration of relaxation in mammalian heart: a property not relying on phospholamban and SERCA2a phosphorylation. J Physiol 562, 801-813 (2005) (Pubitemid 40246794)
54. DM Bers: Excitation-contraction coupling and cardiac contractile force. 2nd ed. Dordrecht, Netherlands: Kluwer Academic Publishers (2001)
55. J DeSantiago, LS Maier, DM Bers: Frequencydependent acceleration of relaxation in the heart depends on CaMKII, but not phospholamban. J Mol Cell Cardiol 34, 975-984 (2002) (Pubitemid 35316145)
56. WH Gaskell: On the tonicity of the heart and blood vessels. J Physiol 3, 48-75 (1980)
57. A Fabiato, F Fabiato: Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J Physiol 276, 233-255 (1978) (Pubitemid 8298525)
58. EM Blanchard, RJ Solaro: Inhibition of the activation and troponin calcium binding of dog cardiac myofibrils by acidic pH. Circ Res 55, 382-391 (1984) (Pubitemid 14047499)
59. CH Orchard: The role of the sarcoplasmic reticulum in the response of ferret and rat heart muscle to acidosis. J Physiol 384, 431-449 (1987) (Pubitemid 17026528)
60. F Mandel, EG Kranias, A Grassi de Gende, M Sumida, A Schwartz: The effect of pH on the transient-state kinetics of Ca2+-Mg2+-ATPase of cardiac sarcoplasmic reticulum. A comparison with skeletal sarcoplasmic reticulum. Circ Res 50, 310-317 (1982) (Pubitemid 12168323)
61. A Mattiazzi, HE Cingolani: Biphasic effect of hypercapnia in myocardial contractility. Arch Int Physiol Biochim 85, 11-25 (1977) (Pubitemid 8069221)
62. A Mattiazzi, HE Cingolani: Paradoxical effect of hypercapnia on toad heart muscle. Circ Res 41, 117-122 (1977) (Pubitemid 8132092)
63. CH Fry, PA Poole-Wilson: Effects of acid-base changes on excitation-contraction coupling in guinea-pig and rabbit cardiac ventricular muscle. J Physiol 313, 141-160 (1981) (Pubitemid 11125566)
64. DG Allen, CH Orchard: The effects of changes of pH on intracellular calcium transients in mammalian cardiac muscle. J Physiol 335, 555-567 (1983) (Pubitemid 13148387)
65. C Bountra, RD Vaughan-Jones: Effect of intracellular and extracellular pH on contraction in isolated, mammalian cardiac muscle. J Physiol 418, 163-187 (1989) (Pubitemid 19276926)
66. HE Cingolani, Y Koretsune, E Marbán: Recovery of contractility and pHi during respiratory acidosis in ferret hearts: role of Na+-H+ exchange. Am J Physiol Heart Circ Physiol 259, H843-H848 (1990) (Pubitemid 20310490)
67. SM Harrison, JE Frampton, E McCall, MR Boyett, CH Orchard: Contraction and intracellular Ca2+, Na+, and H+ during acidosis in rat ventricular myocytes. Am J Physiol Cell Physiol 262, C348-C357 (1992)
68. NG Perez, A Mattiazzi, MC. Camilión de Hurtado, HE Cingolani: Myocardial contractility recovery during hypercapnic acidosis: its dissociation from recovery in pHi by ryanodine. Can J Cardiol 11, 553-560 (1995)
69. N Nomura, H Satoh, H Terada, M Matsunaga, H Watanabe, H Hayashi: CaMKII-dependent reactivation of SR Ca2+ uptake and contractile recovery during intracellular acidosis. Am J Physiol Heart Circ Physiol 283, H193-H203 (2002) (Pubitemid 34705340)
70. J DeSantiago, LS Maier, DM Bers: 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 (2004) (Pubitemid 38084792)
71. JT Hulme, J Colyer, CH Orchard: Acidosis alters the phosphorylation of Ser16 and Thr17 of phospholamban in rat cardiac muscle. Pflugers Arch 434, 475-483 (1997) (Pubitemid 27292573)
72. K Komukai, C Pascarel, CH Orchard: Compensatory role of CaMKII on ICa and SR function during acidosis in rat ventricular myocytes. Pflugers Arch 442, 353-361 (2001) (Pubitemid 32591976)
73. JT Hulme, CH Orchard: Effect of acidosis on Ca2+ uptake and release by sarcoplasmic reticulum of intact rat ventricular myocytes. Am J Physiol Heart Circ Physiol 275, H977-H987 (1998).
74. C Mundiña-Weilenmann, L Vittone, HE Cingolani, CH Orchard: Effects of acidosis on phosphorylation of phospholamban and troponin I in rat cardiac muscle. Am J Physiol Cell Physiol 270, C107-C114 (1996)
75. L Vittone, C Mundiña-Weilenmann, M Said, A Mattiazzi: Mechanisms involved in the acidosis enhancement of the isoproterenol-induced phosphorylation of phospholamban in the intact heart. J Biol Chem 273, 9804-9811 (1998). (Pubitemid 28183075)
76. E Braunwald, RA Kloner: The stunned myocardium: prolonged, postischemic ventricular dysfunction. Circulation 66, 1146-1149 (1982) (Pubitemid 13238825)
77. GR Heyndrickx, RW Millard, RJ McRitchie, PR Maroko, SF Vatner: Regional myocardial functional and electrophysiological alterations after brief coronary artery occlusion in conscious dogs. J Clin Invest 56, 978-985 (1975)
78. R Bolli, E Marbán: Molecular and cellular mechanism of myocardial stunning. Physiol Rev 79, 609-634 (1999) (Pubitemid 29210931)
79. SJ Kim, C Depre, SF Vatner: Novel mechanisms mediating stunned myocardium. Heart Fail Rev 8, 143-153 (2003) (Pubitemid 36559669)
80. R Bolli: Mechanism of myocardial "stunning". Circulation 82, 723-738 (1990)
81. Z Tatarková, P Aplán, M Matejovicová, J Lehotský, D Dobrota, W Flameng: Effect of ischemia and reperfusion on protein oxidation in isolated rabbit hearts. Physiol Res 54, 185-191 (2005) (Pubitemid 40686265)
82. JP Carrozza Jr, LA Bentivegna, CP Williams, RE Kuntz, W Grossman, JP Morgan: Decreased myofilament responsiveness in myocardial stunning follows transient calcium overload during ischemia and reperfusion. Circ Res 71, 1334-1340 (1992)
83. WD Gao, D Atar, P Backx, E Marbán: Relationship between intracellular calcium and contractile force in stunned myocardium. Direct evidence for decreased myofilament Ca2+ responsiveness and altered diastolic function in intact ventricular muscle. Circ Res 76, 1036-1048 (1995)
84. JM Canty, TC Lee: Troponin I proteolisis and myofilament sensitivity: Now you see it-now you don't. J Mol Cell Cardiol 34, 401-411 (2002)
85. SM Krause, WE Jacobus, LC Becker: Alterations in cardiac sarcoplasmic reticulum calcium transport in the postischemic "stunned" myocardium. Circ Res 65, 526-530 (1989) (Pubitemid 19194639)
86. U Limbruno, R Zucchi, S Ronca-Testoni, P Galbani, G Ronca, M Mariani: Sarcoplasmic reticulum function in the "stunned" myocardium. J Mol Cell Cardiol 21, 1063-1072 (1989) (Pubitemid 19274198)
87. R Zucchi, S Ronca-Testoni, P Di Napoli, G Yu, S Gallina, G Bosco, G Ronca, AM Calafiore, M Mariani, A Barsotti: Sarcoplasmic reticulum calcium uptake in human myocardium subjected to ischemia and reperfusion during cardiac surgery. J Mol Cell Cardiol 28, 1693-1701 (1996) (Pubitemid 26300569)
88. L Vittone, C Mundiña-Weilenmann, M Said, P Ferrero, A Mattiazzi: Time course and mechanisms of phosphorylation of phospholamban residues in ischemiareperfused rat hearts. Dissociation of phospholamban phosphorylation pathways. J Mol Cell Cardiol 34, 39-50 (2002) (Pubitemid 34146394)
89. M Said, L Vittone, C Mundiña-Weilenmann, P Ferrero, EG Kranias, A Mattiazzi: Role of dual-site phospholamban phosphorylation in the stunned heart: insights from phospholamban site-specific mutants. Am J Physiol Heart Circ Physiol 285, H1198-H1205 (2003) (Pubitemid 37048177)
90. CA Valverde, C Mundiña-Weilenmann, M Reyes, EG Kranias, AL Escobar, A Mattiazzi: Phospholamban phosphorylation sites enhance the recovery of intracellular Ca2+ after perfusion arrest in isolated, perfused mouse heart. Cardiovasc Res 70, 335-345 (2006)
91. Y Xie, Y Zhu, W-Z Zhu, L Chen, Z-N Zhou, W-J Yuan, H-T Yang: Role of dual-site phospholamban phosphorylation in intermittent hypoxia-induced cardioprotection against ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 288, H2594-H2602 (2005) (Pubitemid 40720635)
92. Y Abdallah, A Gkatzoflia, H Pieper, E Zoga, S Walther, S Kasseckert, M Schäfer, KD Schlüter, HM Piper, C Schäfer: Mechanism of cGMP-mediated protection in a cellular model of myocardial reperfusion injury. Cardiovasc Res 66, 123-131 (2005) (Pubitemid 40357875)
93. Y Abdallah, A Gkatzoflia, D Gligorievski, S Kasseckert, G Euler, KD Schlüter, M Schäfer, HM Piper, C Schäfer: Insulin protects cardiomyocytes against reoxygenation-induced hypercontracture by a survival pathway targeting SR Ca2+ storage. Cardiovasc Res 70, 346-353 (2006)
94. Y Yang, WZ Zhu, ML Joiner, R Zhang, CV Oddis, Y Hou, J Yang, EE Price, L Gleaves, M Eren, G Ni, DE Vaughan, RP Xiao, ME Anderson: Calmodulin kinase II inhibition protects against myocardial cell apoptosis in vivo. Am J Physiol Heart Circ Physiol 291, 3065-3075 (2006)
95. M Vila-Petroff, MA Salas, M Said , CA Valverde, L Sapia, E Portiansky, RJ Hajjar, EG Kranias, C Mundiña-Weilenmann, A Mattiazzi: CaMKII inhibition protects against necrosis and apoptosis in irreversible ischemiareperfusion injury. Cardiovasc Res 73, 689-698 (2007) (Pubitemid 46227351)
96. R Zhang, MS Khoo, Y Wu, Y Yang, CE Grueter, G Ni, EE Price Jr, W Thiel, S Guatimosim, LS Song, EC Madu, AN Shah, TA Vishnivetskaya, JB Atkinson, VV Gurevich, G Salama, WJ Lederer, RJ Colbran, ME Anderson: Calmodulin kinase II inhibition protects against structural heart disease. Nat Med 11, 409-417 (2005) (Pubitemid 40562331)
97. M Lindner, E Erdmann, DJ Beuckelmann: Calcium content of the sarcoplasmic reticulum in isolated ventricular myocytes from patients with terminal heart failure. J Mol Cel Cardiol 30, 743-749 (1998) (Pubitemid 28190718)
98. B O'Rourke, Kass DA, Tomaselli GF, Kääb S, Tunin R, Marbán E: Mechanisms of altered excitation-contraction coupling in canine tachicardia-induced heart failure. I. Experimental studies. Circ Res 84, 562-570 (1999) (Pubitemid 29138593)
99. G Hasenfuss: Alterations in calcium regulatory proteins in heart failure. Cardiovasc Res 37, 279-289 (1998) (Pubitemid 28165990)
100. SO Marx, S Reiken, Y Hisamatsu, T Jayaraman, D Burkhoff, N Rosemblit, AR Marks: PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101, 365-376 (2000)
101. X Ai, JW Curran, TR Shannon, DM Bers, SM Pogwizd: Ca2+/calmodulin- dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 97, 1314-1322 (2005)
102. RHG Schwinger, G Munch, B Bolk, P Karczewski, EG Krause, E Erdmann: Reduced Ca2+-sensitivity of SERCA2a in failing human myocardium due to reduced Serin-16 phospholamban phosphorylation. J Mol Cell Cardiol 31, 479-491 (1999) (Pubitemid 29121635)
103. JB Sande, I Sjaastad, IB Hoen, J Bokenes, T Tonnessen, E Holt, PK Lunde, G Christensen: Reduced level of serine16 phosphorylated phospholamban in the failing rat myocardium: A major contributor to reduced SERCA2 activity. Cardiovasc Res 53, 383-391 (2002).
104. T Netticadan, R Temsah, K Kawabata, NS Dallha: Sarcoplasmic reticulum Ca2+/calmodulin-dependent kinase is altered in heart failure. Circ Res 86, 596-605 (2000) (Pubitemid 30165052)
105. S Mishra, HN Sabbah, JC Jain, RC Gupta: Reduced Ca2+-calmodulin-dependent protein kinase activity and expression of LV myocardium of dogs with heart failure. Am J Physiol Heart Circ Physiol 284, H876-H883 (2003) (Pubitemid 36228235)
106. B Huang, S Wang, D Qin, M Boutjdir, N El-Sherif: Dimished basal phosphorylation level of phospholamban in the postinfarctium remodeled rat ventricle. Role of betaadrenergic pathway, Gi protein, phosphodiesterase and phosphatases. Circ Res 85, 848-855 (1999) (Pubitemid 29504160)
107. MR Bristow, R Ginsburg, V Umans: Beta1-and beta2-adrenergic -receptor subpopulations in nonfailing and failing human ventricular myocardium: coupling of both receptor subtypes to muscle contraction and selective beta1-receptor down regulation in heart failure. Circ Res 59, 248-254 (1986)
108. RC Gupta, S Mishra, S Rastogi, M Imai, O Habib, HN Sabbah: Cardiac SR-coupled PP1 and expression are increased and inhibitor-1 protein expression is decreased in failing hearts. Am J Physiol Heart Circ Physiol 285, H2373-H2381 (2003) (Pubitemid 37443053)
109. F del Monte F, RJ Ajar: Targeting calcium cycling proteins in heart failure through gene transfer. J Physiol 546, 49-61 (2003)
110. S Boateng, AM Seymour, M Dunn, M Yacoub, K Boheler: Inhibition of endogenous cardiac phosphatase activity and measurement of sarcoplasmic reticulum calcium uptake: a possible role of phospholamban phosphorylation in the hypertrophied myocardium. Biochem Biophys Res Commun 239, 701-705 (1997) (Pubitemid 27504165)
111. JD Molkentin, JR Lu, CL Antos, B Markham, J Richardson, J Robbins, SR Grant, EN Olson: A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228 (1998) (Pubitemid 28180855)
112. P Cohen: The structure and regulation of protein phosphatases. Annu Rev Biochem 58, 453-508 (1989) (Pubitemid 19172978)
113. JM Bradshaw, Y Kubota, T Meyer, H Schulman: An ultrasensitive Ca2+/calmodulin-dependent protein kinase IIprotein phosphatase 1 switch facilitates specificity in postsynaptic calcium signaling. Proc Natl Acad Sci U S A 100, 10512-10517 (2003) (Pubitemid 37071909)
114. B Hoch, R Meyer, R Hetzer, EG Krause, P Karczewski: Identification and expression of delta-isoforms of the multifunctional Ca2+/calmodulin-dependent protein kinase in failing and non failing human myocardium. Circ Res 84, 713-721 (1999) (Pubitemid 29157339)
115. U Kirchhefer, W Schmitz, H Scholtz, J Newmann: Activity of cAMP-dependent protein kinase and Ca2+/calmodulin-dependent protein kinase in failing and non failing human hearts. Cardiovasc Res 42, 254-261 (1999) (Pubitemid 29167092)
116. T Zhang , JH Brown: Role of Ca2+/calmodulindependent protein kinase II in cardiac hypertrophy and heart failure. Cardiovasc Res 63, 476-486 (2004) (Pubitemid 38970192)
117. D de la Bastie, D Levitsky, L Rappaport, JJ Mercadier, F Marotte, C Wisnewsky, V Brovkovich, K Schwartz, AM Lompre: Function of the sarcoplasmic reticulum and expression of its Ca2+-ATPase gene in pressure overload-induced cardiac hypertrophy in the rat. Circ Res 66, 554-564 (1990) (Pubitemid 20041186)
118. G Hasenfuss, H Reinecke, R Studer, M Meyer, B Pieske, J Holtz, C Holubarsch, H Posival, H Just, H Drexler: Relation between myocardial function and expression of sarcoplasmic reticulum Ca2+-ATPase in failing and nonfailing human myocardium.Circ Res 75, 434-442 (1994)
119. M Meyer, W Schillinger, B Pieske, C Holubarsch, C Heilmann, H Posival, G Kuwajima, K Mikoshiba, H Just, G Hasenfuss: Alterations of sarcoplasmic reticulum proteins in failing human dilated cardiomyopathy. Circulation 92, 778-784 (1995)
120. MA Movsesian, M Karimi, K Green, LR Jones: Ca2+-transporting ATPase, phospholamban, and calsequestrin levels in nonfailing and failing human myocardium. Circulation 90, 653-657 (1994)
121. RH Schwinger, M Böhm, U Schmidt, P Karczewski, U Bavendiek, M Flesch, EG Krause, E Erdmann: Unchanged protein levels of SERCA II and phospholamban but reduced Ca2+ uptake and Ca2+-ATPase activity of cardiac sarcoplasmic reticulum from dilated cardiomyopathy patients compared with patients with nonfailing hearts. Circulation 92, 3220-3228 (1995)
122. B Linck, P Bokník, T Eschenhagen, FU Müller, J Neumann, M Nose, LR Jones, W Schmitz, H Scholz: Messenger RNA expression and immunological quantification of phospholamban and SR-Ca2+-ATPase in failing and nonfailing human hearts. Cardiovasc Res 31, 625-632 (1996)
123. B Stein, S Bartel, U Kirchhefer, S Kokott, EG Krause, J Neumann, W Schmitz, H Scholz: Relation between contractile function and regulatory cardiac proteins in hypertrophied hearts. Am J Physiol Heart Circ Physiol 270, H2021-2028 (1996)
124. S Currie, GL Smith: Enhanced phosphorylation of phospholamban and downregulation of sarco/endoplasmic reticulum Ca2+ ATPase type 2 (SERCA 2) in cardiac sarcoplasmic reticulum from rabbits with heart failure. Cardiovasc Res 41, 135-146 (1999) (Pubitemid 29016053)
125. U Schmidt, RJ Hajjar, CS Kim, D Lebeche, AA Doye, JK Gwathmey: Human heart failure: cAMP stimulation of SR Ca2+-ATPase activity and phosphorylation level of phospholamban. Am J Physiol Heart Circ Physiol 277, H474-H480 (1999) (Pubitemid 29415959)
126. P Bokník, I Heinroth-Hoffmann, U Kirchhefer, J Knapp, B Linck, H Lüss, T Müller, W Schmitz, O Brodde, J Neumann: Enhanced protein phosphorylation in hypertensive hypertrophy. Cardiovasc Res 51, 717-728 (2001) (Pubitemid 32800713)
127. R Dash, KF Frank, AN Carr, CS Moravec, EG Kranias: Gender influences on sarcoplasmic reticulum Ca2+-handling in failing human myocardium. J Mol Cell Cardiol 33, 1345-1353 (2001) (Pubitemid 32613426)
128. GD Mills, H Kubo, DM Harris, RM Berretta, V Piacentino 3rd, SR Houser: Phosphorylation of phospholamban at threonine-17 reduces cardiac adrenergic contractile responsiveness in chronic pressure overloadinduced hypertrophy. Am J Physiol Heart Circ Physiol 291, H61-H70 (2006)
129. AA Armoundas, J Rose, R Aggarwal, BD Stuyvers, B O'rourke, DA Kass, E Marbán, SR Shorofsky, GF Tomaselli, C William Balke: Cellular and molecular determinants of altered Ca2+ handling in the failing rabbit heart: primary defects in SR Ca2+ uptake and release mechanisms. Am J Physiol Heart Circ Physiol 292, H1607-H1618 (2007) (Pubitemid 46377149)