Regulation of CaMKII signaling in cardiovascular disease

Frontiers in Pharmacology

Volumn 6, Issue Aug, 2015, Pages

  Mollova, Mariya Y ^a,b   Katus, Hugo A ^a,b   Backs, Johannes ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Heidelberg   (Germany)

Author keywords

CaMKII; Enzymatic activity; Heart failure; Post translational modifications; Sub cellular localization

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; MICRORNA 145; MICRORNA 214; REACTIVE OXYGEN METABOLITE;

ARTICLE; ATRIAL FIBRILLATION; CARDIOVASCULAR DISEASE; DISEASE COURSE; ENZYME GLYCOSYLATION; ENZYME METABOLISM; ENZYME PHOSPHORYLATION; HEART FAILURE; HUMAN; MOLECULAR INTERACTION; NITROSYLATION; NONHUMAN; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 84941000591     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2015.00178     Document Type: Article

References (95)

1. Anderson, M. E., Brown, J. H., and Bers, D. M. (2011). CaMKII in myocardial hypertrophy and heart failure. J. Mol. Cell. Cardiol. 51, 468-473. doi: 10.1016/j.yjmcc.2011.01.012
2. Aurora, A. B., Mahmoud, A. I., Luo, X., Johnson, B. A., Van Rooij, E., Matsuzaki, S., et al. (2012). MicroRNA-214 protects the mouse heart from ischemic injury by controlling Ca2+ overload and cell death. J. Clin. Invest. 122, 1222-1232. doi: 10.1172/JCI59327
3. Backs, J., Backs, T., Bezprozvannaya, S., Mckinsey, T. A., and Olson, E. N. (2008). Histone deacetylase 5 acquires calcium/calmodulin-dependent kinase II responsiveness by oligomerization with histone deacetylase 4. Mol. Cell. Biol. 28, 3437-3445. doi: 10.1128/MCB.01611-07
4. Backs, J., Song, K., Bezprozvannaya, S., Chang, S., and Olson, E. N. (2006). CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J. Clin. Invest. 116, 1853-1864. doi: 10.1172/JCI27438
5. Backs, J., Worst, B. C., Lehmann, L. H., Patrick, D. M., Jebessa, Z., Kreusser, M. M., et al. (2011). Selective repression of MEF2 activity by PKA-dependent proteolysis of HDAC4. J. Cell Biol. 195, 403-415. doi: 10.1083/jcb.201105063
6. Bathgate-Siryk, A., Dabul, S., Pandya, K., Walklett, K., Rengo, G., Cannavo, A., et al. (2014). Negative impact of β-arrestin-1 on post-myocardial infarction heart failure via cardiac and adrenal-dependent neurohormonal mechanisms. Hypertension 63, 404-412. doi: 10.1161/HYPERTENSIONAHA.113.02043
7. Bayer, K. U., and Schulman, H. (2001). Regulation of signal transduction by protein targeting: the case for CaMKII. Biochem. Biophys. Res. Commun. 289, 917-923. doi: 10.1006/bbrc.2001.6063
8. Capel, R. A., and Terrar, D. A. (2015). The importance of Ca2+-dependent mechanisms for the initiation of the heartbeat. Front. Physiol. 6:80. doi: 10.3389/fphys.2015.00080
9. Cha, M. J., Jang, J. K., Ham, O., Song, B. W., Lee, S. Y., Lee, C. Y., et al. (2013). MicroRNA-145 suppresses ROS-induced Ca2+ overload of cardiomyocytes by targeting CaMKIId. Biochem. Biophys. Res. Commun. 435, 720-726. doi: 10.1016/j.bbrc.2013.05.050
10. Chang, C. W., Lee, L., Yu, D., Dao, K., Bossuyt, J., and Bers, D. M. (2013). Acute β-adrenergic activation triggers nuclear import of histone deacetylase 5 and delays Gq-induced transcriptional activation. J. Biol. Chem. 288, 192-204. doi: 10.1074/jbc.M112.382358
11. Chao, L. H., Pellicena, P., Deindl, S., Barclay, L. A., Schulman, H., and Kuriyan, J. (2010). Intersubunit capture of regulatory segments is a component of cooperative CaMKII activation. Nat. Struct. Mol. Biol. 17, 264-272. doi: 10.1038/nsmb.1751
12. Chiara Andreoli, J. T. P. (2013). "Biomarkers in congestive heart failure," in Biomarkers in Cardiovascular Diseases, ed. Christodoulos Stefanadis (Boca Raton, FL: CRC Press), 101-145.
13. Choi, H., Tostes, R. C., and Webb, R. C. (2011). S-nitrosylation Inhibits protein kinase C-mediated contraction in mouse aorta. J. Cardiovasc. Pharmacol. 57, 65-71. doi: 10.1097/FJC.0b013e3181fef9cb
14. Christensen, M. D., Dun, W., Boyden, P. A., Anderson, M. E., Mohler, P. J., and Hund, T. J. (2009). Oxidized calmodulin kinase II regulates conduction following myocardial infarction: a computational analysis. PLoS Comput. Biol. 5:e1000583. doi: 10.1371/journal.pcbi.1000583
15. Cipolletta, E., Rusciano, M. R., Maione, A. S., Santulli, G., Sorriento, D., Del Giudice, C., et al. (2015). Targeting the CaMKII/ERK interaction in the heart prevents cardiac hypertrophy. PLoS ONE 10:e0130477. doi: 10.1371/journal.pone.0130477
16. Couchonnal, L. F., and Anderson, M. E. (2008). The role of calmodulin kinase II in myocardial physiology and disease. Physiology (Bethesda) 23, 151-159. doi: 10.1152/physiol.00043.2007
17. Dhalla, N., and Müller, A. (2010). Protein kinases as drug development targets for heart disease therapy. Pharmaceuticals 3, 2111-2145. doi: 10.3390/ph3072111
18. Erickson, J. R. (2014). Mechanisms of CaMKII activation in the heart. Front. Pharmacol. 5:59. doi: 10.3389/fphar.2014.00059
19. Erickson, J. R., Joiner, M. L., Guan, X., Kutschke, W., Yang, J., Oddis, C. V., et al. (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
20. Erickson, J. R., Patel, R., Ferguson, A., Bossuyt, J., and Bers, D. M. (2011). Fluorescence resonance energy transfer-based sensor Camui provides new insight into mechanisms of calcium/calmodulin-dependent protein kinase II activation in intact cardiomyocytes. Circ. Res. 109, 729-738. doi: 10.1161/CIRCRESAHA.111.247148
21. Erickson, J. R., Pereira, L., Wang, L., Han, G., Ferguson, A., Dao, K., et al. (2013). Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature 502, 372-376. doi: 10.1038/nature12537
22. Gaston, B. M., Carver, J., Doctor, A., and Palmer, L. A. (2003). S-nitrosylation signaling in cell biology. Mol. Interv. 3, 253-263. doi: 10.1124/mi.3.5.253
23. Graves, P. R., and Haystead, T. A. (2003). A functional proteomics approach to signal transduction. Recent Prog. Horm. Res. 58, 1-24. doi: 10.1210/rp.58.1.1
24. Gray, C. B., and Heller Brown, J. (2014). CaMKIId subtypes: localization and function. Front. Pharmacol. 5:15. doi: 10.3389/fphar.2014.00015
25. Gurevich, V. V., Gurevich, E. V., and Cleghorn, W. M. (2008). Arrestins as multi-functional signaling adaptors. Handb. Exp. Pharmacol. 186, 15-37. doi: 10.1007/978-3-540-72843-6_2
26. Gutierrez, D. A., Fernandez-Tenorio, M., Ogrodnik, J., and Niggli, E. (2013). NO-dependent CaMKII activation during β-adrenergic stimulation of cardiac muscle. Cardiovasc. Res. 100, 392-401. doi: 10.1093/cvr/cvt201
27. Ha, C. H., Kim, J. Y., Zhao, J., Wang, W., Jhun, B. S., Wong, C., et al. (2010). PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 107, 15467-15472. doi: 10.1073/pnas.1000462107
28. Hafstad, A. D., Nabeebaccus, A. A., and Shah, A. M. (2013). Novel aspects of ROS signalling in heart failure. Basic Res. Cardiol. 108, 359. doi: 10.1007/s00395-013-0359-8
29. Haghighi, K., Bidwell, P., and Kranias, E. G. (2014). Phospholamban interactome in cardiac contractility and survival: a new vision of an old friend. J. Mol. Cell. Cardiol. 77, 160-167. doi: 10.1016/j.yjmcc.2014.10.005
30. Haworth, R. S., Stathopoulou, K., Candasamy, A. J., and Avkiran, M. (2012). Neurohormonal regulation of cardiac histone deacetylase 5 nuclear localization by phosphorylation-dependent and phosphorylation-independent mechanisms. Circ. Res. 110, 1585-1595. doi: 10.1161/CIRCRESAHA.111.263665
31. He, B. J., Joiner, M. L., Singh, M. V., Luczak, E. D., Swaminathan, P. D., Koval, O. M., et al. (2011). Oxidation of CaMKII determines the cardiotoxic effects of aldosterone. Nat. Med. 17, 1610-1618. doi: 10.1038/nm.2506
32. Heijman, J., Voigt, N., Wehrens, X. H., and Dobrev, D. (2014). Calcium dysregulation in atrial fibrillation: the role of CaMKII. Front. Pharmacol. 5:30. doi: 10.3389/fphar.2014.00030
33. Heist, E. K., Srinivasan, M., and Schulman, H. (1998). Phosphorylation at the nuclear localization signal of Ca2+/calmodulin-dependent protein kinase II blocks its nuclear targeting. J. Biol. Chem. 273, 19763-19771. doi: 10.1074/jbc.273.31.19763
34. Hoch, B., Haase, H., Schulze, W., Hagemann, D., Morano, I., Krause, E. G., et al. (1998). Differentiation-dependent expression of cardiac d-CaMKII isoforms. J. Cell. Biochem. 68, 259-268.
35. Hubbard, M. J., and Cohen, P. (1993). On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18, 172-177. doi: 10.1016/0968-0004(93)90109-Z
36. Hudmon, A., and Schulman, H. (2002). Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem. J. 364, 593-611. doi: 10.1042/bj20020228
37. Koitabashi, N., and Kass, D. A. (2012). Reverse remodeling in heart failure-mechanisms and therapeutic opportunities. Nat. Rev. Cardiol. 9, 147-157. doi: 10.1038/nrcardio.2011.172
38. Kreusser, M. M., and Backs, J. (2014). Integrated mechanisms of CaMKII-dependent ventricular remodeling. Front. Pharmacol. 5:36. doi: 10.3389/fphar.2014.00036
39. Kreusser, M. M., Lehmann, L. H., Keranov, S., Hoting, M. O., Oehl, U., Kohlhaas, M., et al. (2014). Cardiac CaM Kinase II genes δ and γ contribute to adverse remodeling but redundantly inhibit calcineurin-induced myocardial hypertrophy. Circulation 130, 1262-1273. doi: 10.1161/CIRCULATIONAHA.114.006185
40. Kushnir, A., Shan, J., Betzenhauser, M. J., Reiken, S., and Marks, A. R. (2010). Role of CaMKIId phosphorylation of the cardiac ryanodine receptor in the force frequency relationship and heart failure. Proc. Natl. Acad. Sci. U.S.A. 107, 10274-10279. doi: 10.1073/pnas.1005843107
41. Lai, Y., Nairn, A. C., Gorelick, F., and Greengard, P. (1987). Ca2+/calmodulin-dependent protein kinase II: identification of autophosphorylation sites responsible for generation of Ca2+/calmodulin-independence. Proc. Natl. Acad. Sci. U.S.A. 84, 5710-5714. doi: 10.1073/pnas.84.16.5710
42. Lander, H. M., Hajjar, D. P., Hempstead, B. L., Mirza, U. A., Chait, B. T., Campbell, S., et al. (1997). A molecular redox switch on p21ras. Structural basis for the nitric oxide-p21ras interaction. J. Biol. Chem. 272, 4323-4326. doi: 10.1074/jbc.272.7.4323
43. Larson, M. G., Atwood, L. D., Benjamin, E. J., Cupples, L. A., D'Agostino, R. B. Sr., Fox, C. S., et al. (2007). Framingham Heart Study 100K project: genome-wide associations for cardiovascular disease outcomes. BMC Med. Genet. 8(Suppl. 1):S5. doi: 10.1186/1471-2350-8-s1-s5
44. Liddy, K. A., White, M. Y., and Cordwell, S. J. (2013). Functional decorations: post-translational modifications and heart disease delineated by targeted proteomics. Genome Med. 5, 20. doi: 10.1186/gm424
45. Lima, B., Forrester, M. T., Hess, D. T., and Stamler, J. S. (2010). S-nitrosylation in cardiovascular signaling. Circ. Res. 106, 633-646. doi: 10.1161/CIRCRESAHA.109.207381
46. Ling, H., Zhang, T., Pereira, L., Means, C. K., Cheng, H., Gu, Y., et al. (2009). Requirement for Ca2+/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
47. Liu, Q., and Molkentin, J. D. (2011). Protein kinase Ca as a heart failure therapeutic target. J. Mol. Cell. Cardiol. 51, 474-478. doi: 10.1016/j.yjmcc.2010.10.004
48. Luo, M., Guan, X., Luczak, E. D., Lang, D., Kutschke, W., Gao, Z., et al. (2013). Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J. Clin. Invest. 123, 1262-1274. doi: 10.1172/JCI65268
49. Maier, L. S. (2005). CaMKIId overexpression in hypertrophy and heart failure: cellular consequences for excitation-contraction coupling. Braz. J. Med. Biol. Res. 38, 1293-1302. doi: 10.1590/S0100-879X2005000900002
50. Maier, L. S., and Bers, D. M. (2002). Calcium, calmodulin, and calcium-calmodulin kinase II: heartbeat to heartbeat and beyond. J. Mol. Cell. Cardiol. 34, 919-939. doi: 10.1006/jmcc.2002.2038
51. Mangmool, S., Shukla, A. K., and Rockman, H. A. (2010). β-Arrestin-dependent activation of Ca2+/calmodulin kinase II after β1-adrenergic receptor stimulation. J. Cell Biol. 189, 573-587. doi: 10.1083/jcb.200911047
52. Marx, S. O., and Marks, A. R. (2013). Dysfunctional ryanodine receptors in the heart: new insights into complex cardiovascular diseases. J. Mol. Cell. Cardiol. 58, 225-231. doi: 10.1016/j.yjmcc.2013.03.005
53. Mattiazzi, A., Bassani, R. A., Escobar, A. L., Palomeque, J., Valverde, C. A., Vila Petroff, M., et al. (2015). Chasing cardiac physiology and pathology down the CaMKII cascade. Am. J. Physiol. Heart Circ. Physiol. 308, H1177-H1191. doi: 10.1152/ajpheart.00007.2015
54. Meyer, T., Hanson, P. I., Stryer, L., and Schulman, H. (1992). Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256, 1199-1202. doi: 10.1126/science.256.5060.1199
55. Mika, D., Richter, W., and Conti, M. (2015). A CaMKII/PDE4D negative feedback regulates cAMP signaling. Proc. Natl. Acad. Sci. U.S.A. 112, 2023-2028. doi: 10.1073/pnas.1419992112
56. Mishra, S., Gray, C. B., Miyamoto, S., Bers, D. M., and Brown, J. H. (2011). Location matters: clarifying the concept of nuclear and cytosolic CaMKII subtypes. Circ. Res. 109, 1354-1362. doi: 10.1161/CIRCRESAHA.111.248401
57. Mishra, S., Ling, H., Grimm, M., Zhang, T., Bers, D. M., and Brown, J. H. (2010). Cardiac hypertrophy and heart failure development through Gq and CaM kinase II signaling. J. Cardiovasc. Pharmacol. 56, 598-603. doi: 10.1097/FJC.0b013e3181e1d263
58. Murray, C. J., and Lopez, A. D. (1996). Evidence-based health policy-lessons from the Global Burden of Disease Study. Science 274, 740-743. doi: 10.1126/science.274.5288.740
59. Noma, T., Lemaire, A., Naga Prasad, S. V., Barki-Harrington, L., Tilley, D. G., Chen, J., et al. (2007). β-Arrestin-mediated β1-adrenergic receptor transactivation of the EGFR confers cardioprotection. J. Clin. Invest. 117, 2445-2458. doi: 10.1172/JCI31901
60. Palaniyandi, S. S., Sun, L., Ferreira, J. C., and Mochly-Rosen, D. (2009). Protein kinase C in heart failure: a therapeutic target?. Cardiovasc. Res. 82, 229-239. doi: 10.1093/cvr/cvp001
61. Palomeque, J., Rueda, O. V., Sapia, L., Valverde, C. A., Salas, M., Petroff, M. V., et al. (2009). Angiotensin II-induced oxidative stress resets the Ca2+ dependence of Ca2+-calmodulin protein kinase II and promotes a death pathway conserved across different species. Circ. Res. 105, 1204-1212. doi: 10.1161/CIRCRESAHA.109.204172
62. Patel, P. A., Tilley, D. G., and Rockman, H. A. (2008). Beta-arrestin-mediated signaling in the heart. Circ. J. 72, 1725-1729. doi: 10.1253/circj.CJ-08-0734
63. Pereira, L., Cheng, H., Lao, D. H., Na, L., van Oort, R. J., Brown, J. H., et al. (2013). Epac2 mediates cardiac β1-adrenergic-dependent sarcoplasmic reticulum Ca2+ leak and arrhythmia. Circulation 127, 913-922. doi: 10.1161/CIRCULATIONAHA.12.148619
64. Perry, S. J., Baillie, G. S., Kohout, T. A., Mcphee, I., Magiera, M. M., Ang, K. L., et al. (2002). Targeting of cyclic AMP degradation to β2-adrenergic receptors by β-arrestins. Science 298, 834-836. doi: 10.1126/science.1074683
65. Purohit, A., Rokita, A. G., Guan, X., Chen, B., Koval, O. M., Voigt, N., et al. (2013). Oxidized Ca2+/calmodulin-dependent protein kinase II triggers atrial fibrillation. Circulation 128, 1748-1757. doi: 10.1161/CIRCULATIONAHA.113.003313
66. Reiter, E., Ahn, S., Shukla, A. K., and Lefkowitz, R. J. (2012). Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 52, 179-197. doi: 10.1146/annurev.pharmtox.010909.105800
67. Respress, J. L., van Oort, R. J., Li, N., Rolim, N., Dixit, S. S., Dealmeida, A., et al. (2012). Role of RyR2 phosphorylation at S2814 during heart failure progression. Circ. Res. 110, 1474-1483. doi: 10.1161/CIRCRESAHA.112.268094
68. Roe, N. D., and Ren, J. (2013). Oxidative activation of Ca2+/calmodulin-activated kinase II mediates ER stress-induced cardiac dysfunction and apoptosis. Am. J. Physiol. Heart Circ. Physiol. 304, H828-H839. doi: 10.1152/ajpheart.00752.2012
69. Rosenberg, O. S., Deindl, S., Comolli, L. R., Hoelz, A., Downing, K. H., Nairn, A. C., et al. (2006). Oligomerization states of the association domain and the holoenyzme of Ca2+/CaM kinase II. FEBS J. 273, 682-694. doi: 10.1111/j.1742-4658.2005.05088.x
70. Rosenberg, O. S., Deindl, S., Sung, R. J., Nairn, A. C., and Kuriyan, J. (2005). Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme. Cell 123, 849-860. doi: 10.1016/j.cell.2005.10.029
71. Rusciano, M. R., Maione, A. S., and Illario, M. (2012). Sisters Acts: Converging Signaling Between CaMKII and CaMKIV, Two Members of the Same Family. Transl. Med. UniSa 4, 66-72.
72. Rybakowska, I. M., Slominska, E. M., Romaszko, P., Olkowicz, M., Kaletha, K., and Smolenski, R. T. (2015). AMP-regulated protein kinase activity in the hearts of mice treated with low-or high-fat diet measured using novel LC-MS method. Mol. Cell. Biochem. 404, 5-10. doi: 10.1007/s11010-015-2360-z
73. Santulli, G., Cipolletta, E., Sorriento, D., Del Giudice, C., Anastasio, A., Monaco, S., et al. (2012). CaMK4 gene deletion induces hypertension. J. Am. Heart Assoc. 1, e001081. doi: 10.1161/JAHA.112.001081
74. Santulli, G., and Marks, A. R. (2015). Essential roles of intracellular calcium release channels in muscle, brain, metabolism, and aging. Curr. Mol. Pharmacol. [Epub ahead of print].
75. Schulman, H., and Anderson, M. E. (2010). Ca/calmodulin-dependent protein kinase ii in heart failure. Drug Discov. Today Dis. Mech. 7, e117-e122. doi: 10.1016/j.ddmec.2010.07.005
76. Sossalla, S., Fluschnik, N., Schotola, H., Ort, K. R., Neef, S., Schulte, T., et al. (2010). Inhibition of elevated Ca2+/calmodulin-dependent protein kinase II improves contractility in human failing myocardium. Circ. Res. 107, 1150-1161. doi: 10.1161/CIRCRESAHA.110.220418
77. Stamler, J. S., Lamas, S., and Fang, F. C. (2001). Nitrosylation. the prototypic redox-based signaling mechanism. Cell 106, 675-683. doi: 10.1016/S0092-8674(01)00495-0
78. Sucharov, C. C., Dockstader, K., Nunley, K., Mckinsey, T. A., and Bristow, M. (2011). β-Adrenergic receptor stimulation and activation of protein kinase A protect against a1-adrenergic-mediated phosphorylation of protein kinase D and histone deacetylase 5. J. Card. Fail. 17, 592-600. doi: 10.1016/j.cardfail.2011.03.006
79. Swaminathan, P. D., Purohit, A., Hund, T. J., and Anderson, M. E. (2012). Calmodulin-dependent protein kinase II: linking heart failure and arrhythmias. Circ. Res. 110, 1661-1677. doi: 10.1161/CIRCRESAHA.111.243956
80. Swaminathan, P. D., Purohit, A., Soni, S., Voigt, N., Singh, M. V., Glukhov, A. V., et al. (2011). Oxidized CaMKII causes cardiac sinus node dysfunction in mice. J. Clin. Invest. 121, 3277-3288. doi: 10.1172/JCI57833
81. Tohgo, A., Choy, E. W., Gesty-Palmer, D., Pierce, K. L., Laporte, S., Oakley, R. H., et al. (2003). The stability of the G protein-coupled receptor-β-arrestin interaction determines the mechanism and functional consequence of ERK activation. J. Biol. Chem. 278, 6258-6267. doi: 10.1074/jbc.M212231200
82. Tremper-Wells, B., and Vallano, M. L. (2005). Nuclear calpain regulates Ca2+-dependent signaling via proteolysis of nuclear Ca2+/calmodulin-dependent protein kinase type IV in cultured neurons. J. Biol. Chem. 280, 2165-2175. doi: 10.1074/jbc.M410591200
83. Tsai, N. P. (2014). Ubiquitin proteasome system-mediated degradation of synaptic proteins: an update from the postsynaptic side. Biochim. Biophys. Acta 1843, 2838-2842. doi: 10.1016/j.bbamcr.2014.08.006
84. van Oort, R. J., Mccauley, M. D., Dixit, S. S., Pereira, L., Yang, Y., Respress, J. L., et al. (2010). Ryanodine receptor phosphorylation by calcium/calmodulin-dependent protein kinase II promotes life-threatening ventricular arrhythmias in mice with heart failure. Circulation 122, 2669-2679. doi: 10.1161/CIRCULATIONAHA.110.982298
85. Velez Rueda, J. O., Palomeque, J., and Mattiazzi, A. (2012). Early apoptosis in different models of cardiac hypertrophy induced by high renin-angiotensin system activity involves CaMKII. J. Appl. Physiol. 112, 2110-2120. doi: 10.1152/japplphysiol.01383.2011
86. Viatchenko-Karpinski, S., Kornyeyev, D., El-Bizri, N., Budas, G., Fan, P., Jiang, Z., et al. (2014). Intracellular Na+ overload causes oxidation of CaMKII and leads to Ca2+ mishandling in isolated ventricular myocytes. J. Mol. Cell. Cardiol. 76, 247-256. doi: 10.1016/j.yjmcc.2014.09.009
87. Wagner, S., Ruff, H. M., Weber, S. L., Bellmann, S., Sowa, T., Schulte, T., et al. (2011). Reactive oxygen species-activated Ca/calmodulin kinase IId is required for late INa augmentation leading to cellular Na and Ca overload. Circ. Res. 108, 555-565. doi: 10.1161/CIRCRESAHA.110.221911
88. Wang, Z. W. (2008). Regulation of synaptic transmission by presynaptic CaMKII and BK channels. Mol. Neurobiol. 38, 153-166. doi: 10.1007/s12035-008-8039-7
89. Weinreuter, M., Kreusser, M. M., Beckendorf, J., Schreiter, F. C., Leuschner, F., Lehmann, L. H., et al. (2014). CaM Kinase II mediates maladaptive post-infarct remodeling and pro-inflammatory chemoattractant signaling but not acute myocardial ischemia/reperfusion injury. EMBO Mol. Med. 6, 1231-1245. doi: 10.15252/emmm.201403848
90. Wu, N., Hanson, S. M., Francis, D. J., Vishnivetskiy, S. A., Thibonnier, M., Klug, C. S., et al. (2006). Arrestin binding to calmodulin: a direct interaction between two ubiquitous signaling proteins. J. Mol. Biol. 364, 955-963. doi: 10.1016/j.jmb.2006.09.075
91. Xiao, K., Mcclatchy, D. B., Shukla, A. K., Zhao, Y., Chen, M., Shenoy, S. K., et al. (2007). Functional specialization of β-arrestin interactions revealed by proteomic analysis. Proc. Natl. Acad. Sci. U.S.A. 104, 12011-12016. doi: 10.1073/pnas.0704849104
92. Zhai, P., Yamamoto, M., Galeotti, J., Liu, J., Masurekar, M., Thaisz, J., et al. (2005). Cardiac-specific overexpression of AT1 receptor mutant lacking Gaq/Gai coupling causes hypertrophy and bradycardia in transgenic mice. J. Clin. Invest. 115, 3045-3056. doi: 10.1172/JCI25330
93. Zhang, T., and Brown, J. H. (2004). Role of Ca2+/calmodulin-dependent protein kinase II in cardiac hypertrophy and heart failure. Cardiovasc. Res. 63, 476-486. doi: 10.1016/j.cardiores.2004.04.026
94. Zhang, T., Kohlhaas, M., Backs, J., Mishra, S., Phillips, W., Dybkova, N., et al. (2007). CaMKIId isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses. J. Biol. Chem. 282, 35078-35087. doi: 10.1074/jbc.M707083200
95. Zhang, T., Maier, L. S., Dalton, N. D., Miyamoto, S., Ross, J. Jr., Bers, D. M., et al. (2003). The dC isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ. Res. 92, 912-919. doi: 10.1161/01.RES.0000069686.31472.C5