Mechanisms of CaMKII activation in the heart

Frontiers in Pharmacology

Volumn 5 APR, Issue , 2014, Pages

  Erickson, Jeffrey R ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

CaMKII; Diabetes; Heart failure; O GlcNAc modification; Oxidative stress

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

BINDING SITE; CARDIOVASCULAR DISEASE; CELL STRESS; CONGESTIVE CARDIOMYOPATHY; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE COURSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME METABOLISM; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; HEART; HEART VENTRICLE HYPERTROPHY; HUMAN; INTRACELLULAR SIGNALING; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

EID: 84901062033     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00059     Document Type: Review

References (46)

1. Barria, A., and Malinow, R. (2005). NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48, 289-301. doi: 10.1016/j.neuron.2005.08.034
2. Bayer, K. U., De Koninck, P., Leonard, A. S., Hell, J. W., and Schulman, H. (2001). Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411, 801-805. doi: 10.1038/35081080
3. Buard, I., Coultrap, S. J., Freund, R. K., Lee, Y. S., Dell'Acqua, M. L., Silva, A. J., et al. (2010). CaMKII "autonomy" is required for initiating but not for maintaining neuronal long-term information storage. J. Neurosci. 30, 8214-8220. doi: 10.1523/JNEUROSCI.1469-10.2010
4. 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
5. Chatham, J. C., and Marchase, R. B. (2010). The role of protein O-linked β-N-acetylglucosamine in mediating cardiac stress responses. Biochim. Biophys. Acta 1800, 57-66. doi: 10.1016/j.bbagen.2009.07.004
6. 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
7. Colbran, R. J. (2004). Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378, 1-16. doi: 10.1042/BJ20031547
8. Coultrap, S. J., and Bayer, K. U. (2011). Improving a natural CaMKII inhibitor by random and rational design. PLoS ONE 6:e25245. doi: 10.1371/journal.pone.0025245
9. Coultrap, S. J., and Bayer, K. U. (2012). CaMKII regulation in information processing and storage. Trends Neurosci. 35, 607-618. doi: 10.1016/j.tins.2012.05.003
10. 2+/calmodulin. J. Biol. Chem. 285, 17930-17937. doi: 10.1074/jbc. M109.069351
11. Curran, J., Ahmed, U., Bers, D. M., Ziolo, M., and Shannon, T. R. (2009). Isoproterenol-enhanced diastolic sarcoplasmic reticulum Ca leak in ventricular myocytes requires activation of nitric oxide synthase. Biophys. J. 96, 120. doi: 10.1016/j.bpj.2008.12.533
12. 2+ oscillations. Science 279, 227-230. doi: 10.1126/science.279.5348.227
13. Dias, W. B., Cheung, W. D., Wang, Z., and Hart, G. W. (2009). Regulation of calcium/calmodulin-dependent kinase IV by O-GlcNAc modification. J. Biol. Chem. 284, 21327-21337. doi: 10.1074/jbc. M109.007310
14. Dixit, S. S., Wang, T., Manzano, E. J., Yoo, S., Lee, J., Chiang, D. Y., et al. (2013). Effects of CaMKII-mediated phosphorylation of ryanodine receptor type 2 on islet calcium handling, insulin secretion, and glucose tolerance. PLoS ONE 8:e58655. doi: 10.1371/journal.pone.0058655
15. 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
16. 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
17. 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
18. Gabbita, S. P., Aksenov, M. Y., Lovell, M. A., and Markesbery, W. R. (1999). Decrease in peptide methionine sulfoxide reductase in Alzheimer's disease brain. J. Neurochem. 73, 1660-1666. doi: 10.1046/j.1471-4159.1999.0731660.x
19. 2+-calmodulin-dependent protein kinase II. J. Biol. Chem. 279, 12484-12494. doi: 10.1074/jbc. M313597200
20. Gao, Y., Wells, L., Comer, F. I., Parker, G. J., and Hart, G. W. (2001). Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic β-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276, 9838-9845. doi: 10.1074/jbc. M010420200
21. 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
22. Halt, A. R., Dallapiazza, R. F., Zhou, Y., Stein, I. S., Qian, H., Juntti, S., et al. (2012). CaMKII binding to GluN2B is critical during memory consolidation. EMBO J. 31, 1203-1216. doi: 10.1038/emboj.2011.482
23. Hart, G. W., Housley, M. P., and Slawson, C. (2007). Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022. doi: 10.1038/nature05815
24. 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
25. 2+/calmodulin-dependent kinase II. Mol. Cell 11, 1241-1251. doi: 10.1016/S1097-2765(03)00171-0
26. 2+/calmodulin-dependent protein kinase II. Biochem. J. 364, 593-611. doi: 10.1042/BJ20020228
27. Jalan-Sakrikar, N., Bartlett, R. K., Baucum, A. J. II, and Colbran, R. J. (2012). Substrate-selective and calcium-independent activation of CaMKII by a-actinin. J. Biol. Chem. 287, 15275-15283. doi: 10.1074/jbc. M112.351817
28. Joiner, M. L., Koval, O. M., Li, J., He, B. J., Allamargot, C., Gao, Z., et al. (2012). CaMKII determines mitochondrial stress responses in heart. Nature 491, 269-273. doi: 10.1038/nature11444
29. Keskanokwong, T., Lim, H. J., Zhang, P., Cheng, J., Xu, L., Lai, D., et al. (2011). Dynamic Kv4.3-CaMKII unit in heart: an intrinsic negative regulator for CaMKII activation. Eur. Heart J. 32, 305-315. doi: 10.1093/eurheartj/ehq469
30. 2+/calmodulin-independence. Proc. Natl. Acad. Sci. U.S.A. 84, 5710-5714. doi: 10.1073/pnas.84.16.5710
31. 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
32. 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
33. Petropoulos, I., Mary, J., Perichon, M., and Friguet, B. (2001). Rat peptide methionine sulphoxide reductase: cloning of the cDNA, and down-regulation of gene expression and enzyme activity during aging. Biochem. J. 355, 819-825.
34. 2+/calmodulin-dependent protein kinase II triggers atrial fibrillation. Circulation 128, 1748-1757. doi: 10.1161/CIRCULATIONAHA.113.003313
35. Rellos, P., Pike, A. C., Niesen, F. H., Salah, E., Lee, W. H., von Delft, F., et al. (2010). Structure of the CaMKIIdelta/calmodulin complex reveals the molecular mechanism of CaMKII kinase activation. PLoS Biol. 8:e1000426. doi: 10.1371/journal.pbio.1000426
36. 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
37. Rostas, J. A., and Dunkley, P. R. (1992). Multiple forms and distribution of calcium/calmodulin-stimulated protein kinase II in brain. J. Neuorchem. 59, 1191-1202. doi: 10.1111/j.1471-4159.1992.tb08428.x
38. 2+ in cardiac myocytes. Biophys. J. 95, 4597-4612. doi: 10.1529/biophysj.108.128728
39. Song, T., Hatano, N., Kambe, T., Miyamoto, Y., Ihara, H., Yamamoto, H., et al. (2008). Nitric oxide-mediated modulation of calcium/calmodulin-dependent protein kinase II. Biochem. J. 412, 223-231. doi: 10.1042/BJ20071195
40. 2+/calmodulin-dependent protein kinase II by protein phosphatases 1 and 2A. J. Neurochem. 68, 2119-2128. doi: 10.1046/j.1471-4159.1997.68052119.x
41. Strack, S., and Colbran, R. J. (1998). Autophosphorylation-dependent targeting of calcium/calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 273, 20689-20692. doi: 10.1074/jbc.273.33.20689
42. 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
43. 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
44. Na augmentation leading to cellular Na and Ca overload. Circ. Res. 108, 555-565. doi: 10.1161/CIRCRESAHA.110.221911
45. Zhang, D. M., Chai, Y., Erickson, J. R., Heller Brown, J., Bers, D. M., and Lin, Y. F. (2013). Modulation of sarcolemmal ATP-sensitive potassium channels by nitric oxide via sGC/PKG/ROS/ERK1/2/CaMKII signaling in ventricular cardiomyocytes. J. Physiol. 592, 971-990. doi: 10.1113/jphysiol.2013.264697
46. Zhang, T., Maier, L. S., Dalton, N. D., Miyamoto, S., Ross, J. Jr., Bers, D. M., et al. (2003). The deltaC 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