CaMKII-dependent responses to ischemia and reperfusion challenges in the heart

Frontiers in Pharmacology

Volumn 5 MAY, Issue , 2014, Pages

  Bell, James R ^a   Vila Petroff, Martin ^b   Delbridge, Lea M D ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

CaMKII; Cardiomyocyte death; Contractile function; Ischemia; Reperfusion

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II INHIBITOR; CALCIUM ION; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; PROTEIN KINASE INHIBITOR; RYANODINE RECEPTOR 2; SODIUM ION; SODIUM PROTON EXCHANGE PROTEIN; UNCLASSIFIED DRUG;

ARRHYTHMOGENESIS; CALCIUM CELL LEVEL; CALCIUM OVERLOAD; CALCIUM TRANSPORT; CELL DEATH; DISEASE EXACERBATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HEART ARRHYTHMIA; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEART VENTRICLE EXTRASYSTOLE; HUMAN; METABOLIC DISORDER; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REPERFUSION INJURY; REVIEW; RNA SPLICING; SARCOPLASMIC RETICULUM; SODIUM CELL LEVEL;

EID: 84904700703     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00096     Document Type: Review

References (54)

1. Bell, J. R., Bernasochi, G. B., Varma, U., Raaijmakers, A. J., and Delbridge, L. M. (2013a). Sex and sex hormones in cardiac stress-Mechanistic insights. J. Steroid Biochem. Mol. Biol. 137, 124-135. doi: 10.1016/j.jsbmb.2013.05.015.
2. Bell, J. R., Raaijmakers, A. J., Reichelt, M. E., Curl, C. L., and Delbridge, L. M. (2013b). Augmented CaMKII recruitment despite less reperfusion arrhythmias in female hearts - a matter of differential post-translational modification of CaMKII splice variants? Proc. Aust. Physiol. Soc. 44:44P (abstract).
3. +/calmodulin-dependent protein kinase inhibition suppresses post-ischemic arrhythmogenesis and mediates sinus bradycardic recovery in reperfusion. Int. J. Cardiol. 159, 112-118. doi: 10.1016/j.ijcard.2011.02.038.
4. Bell, J. R., Raaijmakers, A. J., Reichelt, M. E., Curl, C. L., and Delbridge, L. M. (2014). Differential post-translational modification of CaMKII splice variants may be critical to determining post-ischemic arrhythmia vulnerability in male and female hearts. Global Heart (abstract) in press.
5. +/calmodulin-dependent protein kinase II and epidermal growth factor receptor. Mol. Cell. Biochem. 268, 175-183. doi: 10.1007/s11010-005-3895-1.
6. Chai, Y., Zhang, D. M., and Lin, Y. F. (2011). Activation of cGMP-dependent protein kinase stimulates cardiac ATP-sensitive potassium channels via a ROS/calmodulin/CaMKII signaling cascade. PLoS ONE 6:e18191. doi: 10.1371/journal.pone.0018191.
7. Curran, J., Brown, K. H., Santiago, D. J., Pogwizd, S., Bers, D. M., and Shannon, T. R. (2010). Spontaneous Ca waves in ventricular myocytes from failing hearts depend on Ca(2+)-calmodulin-dependent protein kinase II. J. Mol. Cell. Cardiol. 49, 25-32. doi: 10.1016/j.yjmcc.2010.03.013.
8. Curtis, M. J., Macleod, B. A., and Walker, M. J. (1984). Antiarrhythmic actions of verapamil against ischaemic arrhythmias in the rat. Br. J. Pharmacol. 83, 373-385.
9. Curtis, M. J., and Walker, M. J. (1988). The mechanism of action of calcium antagonists on arrhythmias in early myocardial ischaemia: studies with nifedipine and DHM9. Br. J. Pharmacol. 94, 1275-1286. doi: 10.1111/j.1476-5381.1988.tb11648.x.
10. DeSantiago, J., Maier, L. S., and Bers, D. M. (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.
11. 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.
12. Gao, L., Blair, L. A., and Marshall, J. (2006). CaMKII-independent effects of KN93 and its inactive analog KN92: reversible inhibition of L-type calcium channels. Biochem. Biophys. Res. Commun. 345, 1606-1610. doi: 10.1016/j.bbrc.2006.05.066.
13. Gray, C. B. B., Xiang, S., Westenbrink, B. D., Mishra, S., and Brown, J. H. (2013). CaMKIId splice variants exert differential effects on heart failure development and myocardial ischemia/reperfusion injury. J. Mol. Cell. Cardiol. 65, PS1-P49 (Abstract).
14. Halestrap, A. P. (2009). Mitochondria and reperfusion injury of the heart-a holey death but not beyond salvation. J. Bioenerg. Biomembr. 41, 113-121. doi: 10.1007/s10863-009-9206-x.
15. Henry, P. D., Schuchleib, R., Davis, J., Weiss, E. S., and Sobel, B. E. (1977). Myocardial contracture and accumulation of mitochondrial calcium in ischemic rabbit heart. Am. J. Physiol. 233, H677-684.
16. Hidalgo, C. G., Chung, C. S., Saripalli, C., Methawasin, M., Hutchinson, K. R., Tsaprailis, G., et al. (2013). The multifunctional Ca(2+)/calmodulin-dependent protein kinase II delta (CaMKIIdelta) phosphorylates cardiac titin's spring elements. J. Mol. Cell. Cardiol. 54, 90-97. doi: 10.1016/j.yjmcc.2012.11.012.
17. Ho, H. T., Liu, B., Snyder, J. S., Lou, Q., Brundage, E. A., Velez-Cortes, F., et al. (2014). Ryanodine receptor phosphorylation by oxidized CaMKII contributes to the cardiotoxic effects of cardiac glycosides. Cardiovasc. Res. 101, 165-174. doi: 10.1093/cvr/cvt233.
18. +/calmodulin-dependent protein kinases: physiological and pharmacological significance of protein phosphatases. Br. J. Pharmacol. 154, 729-740. doi: 10.1038/bjp.2008.127.
19. 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.
20. Konhilas, J. P., Maass, A. H., Luckey, S. W., Stauffer, B. L., Olson, E. N., and Leinwand, L. A. (2004). Sex modifies exercise and cardiac adaptation in mice. Am. J. Physiol. Heart Circ. Physiol. 287, H2768-H2776. doi: 10.1152/ajpheart.00292.2004.
21. Laver, D. R. (2009). Luminal Ca(2+) activation of cardiac ryanodine receptors by luminal and cytoplasmic domains. Eur. Biophys. J. 39, 19-26. doi: 10.1007/s00249-009-0417-1.
22. Li, J., Marionneau, C., Koval, O., Zingman, L., Mohler, P. J., Nerbonne, J. M., et al. (2007). Calmodulin kinase II inhibition enhances ischemic preconditioning by augmenting ATP-sensitive K+ current. Channels (Austin) 1, 387-394.
23. +/calmodulin-dependent protein kinase II delta mediates myocardial ischemia/reperfusion injury through nuclear factor-kappaB. Circ. Res. 112, 935-944. doi: 10.1161/CIRCRESAHA.112.276915.
24. +/calmodulin-dependent protein kinase II. Br. J. Pharmacol. 157, 705-715. doi: 10.1111/j.1476-5381.2009.00212.x.
25. + load. Heart Rhythm 8, 784-787. doi: 10.1016/j.hrthm.2010.11.035.
26. Mattiazzi, A., and Kranias, E. G. (2014). The role of CaMKII regulation of phospholamban activity in heart disease. Front. Pharmacol. 5:5. doi: 10.3389/fphar.2014.00005.
27. Mundina-Weilenmann, C., Ferrero, P., Said, M., Vittone, L., Kranias, E. G., and Mattiazzi, A. (2005). Role of phosphorylation of Thr(17) residue of phospholamban in mechanical recovery during hypercapnic acidosis. Cardiovasc. Res. 66, 114-122. doi: 10.1016/j.cardiores.2004.12.028.
28. Murphy, E., and Steenbergen, C. (2008). Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol. Rev. 88, 581-609. doi: 10.1152/physrev.00024.2007.
29. Nicolaou, P., Hajjar, R. J., and Kranias, E. G. (2009). Role of protein phosphatase-1 inhibitor-1 in cardiac physiology and pathophysiology. J. Mol. Cell. Cardiol. 47, 365-371. doi: 10.1016/j.yjmcc.2009.05.010.
30. Osada, M., Netticadan, T., Kawabata, K., Tamura, K., and Dhalla, N. S. (2000). Ischemic preconditioning prevents I/R-induced alterations in SR calcium-calmodulin protein kinase II. Am. J. Physiol. Heart Circ. Physiol. 278, H1791-H1798.
31. +-calmodulin protein kinase II and promotes a death pathway conserved across different species. Circ. Res. 105, 1204-1212. doi: 10.1161/CIRCRESAHA.109.204172.
32. Peng, W., Zhang, Y., Zheng, M., Cheng, H., Zhu, W., Cao, C. M., et al. (2010). Cardioprotection by CaMKII-deltaB is mediated by phosphorylation of heat shock factor 1 and subsequent expression of inducible heat shock protein 70. Circ. Res. 106, 102-110. doi: 10.1161/CIRCRESAHA.109.210914.
33. +/calmodulin dependent protein kinase phosphatase (CaMKP) in pressure-overloaded mouse heart. PLoS ONE 9:e90822. doi: 10.1371/journal.pone.0090822.
34. Rezazadeh, S., Claydon, T. W., and Fedida, D. (2006). KN-93 (2-[N-(2-hydroxyethyl)]-N-(4-methoxybenzenesulfonyl)]amino-N-(4-chlorocinnamyl)-N-methylbenzylamine), a calcium/calmodulin-dependent protein kinase II inhibitor, is a direct extracellular blocker of voltage-gated potassium channels. J. Pharmacol. Exp. Ther. 317, 292-299. doi: 10.1124/jpet.105.097618.
35. +] in cardiac cells. EMBO J. 20, 4998-5007. doi: 10.1093/emboj/20.17.4998.
36. +/calmodulin-dependent kinase II (CaMKII). Circulation 126, 2125-2139. doi: 10.1161/CIRCULATIONAHA.112.124990.
37. +/calmodulin-dependent protein kinase II. Am. J. Physiol. Heart Circ. Physiol. 295, H1669-H1683. doi: 10.1152/ajpheart.00010.2008.
38. Said, M., Becerra, R., Valverde, C. A., Kaetzel, M. A., Dedman, J. R., Mundina-Weilenmann, C., et al. (2011). Calcium-calmodulin dependent protein kinase II (CaMKII): a main signal responsible for early reperfusion arrhythmias. J. Mol. Cell. Cardiol. 51, 936-944. doi: 10.1016/j.yjmcc.2011.08.010.
39. Said, M., Vittone, L., Mundina-Weilenmann, C., Ferrero, P., Kranias, E. G., and Mattiazzi, A. (2003). 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. doi: 10.1152/ajpheart.00209.2003.
40. Salas, M. A., Valverde, C. A., Sanchez, G., Said, M., Rodriguez, J. S., Portiansky, E. L., et al. (2010). The signalling pathway of CaMKII-mediated apoptosis and necrosis in the ischemia/reperfusion injury. J. Mol. Cell. Cardiol. 48, 1298-1306. doi: 10.1016/j.yjmcc.2009.12.015.
41. + leak-load relationship. Circ. Res. 91, 594-600. doi: 10.1161/01.RES.0000036914.12686.28.
42. Stokke, M. K., Briston, S. J., Jolle, G. F., Manzoor, I., Louch, W. E., Oyehaug, L., et al. (2011). Ca(2+) wave probability is determined by the balance between SERCA2-dependent Ca(2+) reuptake and threshold SR Ca(2+) content. Cardiovasc. Res. 90, 503-512. doi: 10.1093/cvr/cvr013.
43. + after perfusion arrest in isolated, perfused mouse heart. Cardiovasc. Res. 70, 335-345. doi: 10.1016/j.cardiores.2006.01.018.
44. Van der Heiden, K., Cuhlmann, S., Luong Le, A., Zakkar, M., and Evans, P. C. (2010). Role of nuclear factor kappaB in cardiovascular health and disease. Clin. Sci. (Lond.) 118, 593-605. doi: 10.1042/CS20090557.
45. van Echteld, C. J., Kirkels, J. H., Eijgelshoven, M. H., Van Der Meer, P., and Ruigrok, T. J. (1991). Intracellular sodium during ischemia and calcium-free perfusion: a 23Na NMR study. J. Mol. Cell. Cardiol. 23, 297-307. doi: 10.1016/0022-2828(91)90066-U.
46. Venetucci, L. A., Trafford, A. W., and Eisner, D. A. (2007). Increasing ryanodine receptor open probability alone does not produce arrhythmogenic calcium waves: threshold sarcoplasmic reticulum calcium content is required. Circ. Res. 100, 105-111. doi: 10.1161/01.RES.0000252828.17939.00.
47. Vila-Petroff, M., Mundina-Weilenmann, C., Lezcano, N., Snabaitis, A. K., Huergo, M. A., Valverde, C. A., et al. (2010). Ca(2+)/calmodulin-dependent protein kinase II contributes to intracellular pH recovery from acidosis via Na(+)/H(+) exchanger activation. J. Mol. Cell. Cardiol. 49, 106-112. doi: 10.1016/j.yjmcc.2009.12.007.
48. Vila-Petroff, M., Salas, M. A., Said, M., Valverde, C. A., Sapia, L., Portiansky, E., et al. (2007). CaMKII inhibition protects against necrosis and apoptosis in irreversible ischemia-reperfusion injury. Cardiovasc. Res. 73, 689-698. doi: 10.1016/j.cardiores.2006.12.003.
49. Vittone, L., Mundina-Weilenmann, C., Said, M., Ferrero, P., and Mattiazzi, A. (2002). Time course and mechanisms of phosphorylation of phospholamban residues in ischemia-reperfused rat hearts. Dissociation of phospholamban phosphorylation pathways. J. Mol. Cell. Cardiol. 34, 39-50. doi: 10.1006/jmcc.2001.1488.
50. Wehrens, X. H. (2011). CaMKII regulation of the cardiac ryanodine receptor and sarcoplasmic reticulum calcium release. Heart Rhythm 8, 323-325. doi: 10.1016/j.hrthm.2010.09.079.
51. + signaling in cardiac myocyte excitation-transcription coupling. J. Clin. Invest. 116, 675-682. doi: 10.1172/JCI27374.
52. Xie, L. H., Chen, F., Karagueuzian, H. S., and Weiss, J. N. (2009). Oxidative-stress-induced afterdepolarizations and calmodulin kinase II signaling. Circ. Res. 104, 79-86. doi: 10.1161/CIRCRESAHA.108.183475.
53. Yang, Y., Zhu, W. Z., Joiner, M. L., Zhang, R., Oddis, C. V., Hou, Y., et al. (2006). Calmodulin kinase II inhibition protects against myocardial cell apoptosis in vivo. Am. J. Physiol. Heart Circ. Physiol. 291, H3065-H3075. doi: 10.1152/ajpheart.00353.2006.
54. Zhang, D. M., Chai, Y., Erickson, J. R., Heller Brown, J., Bers, D. M., and Lin, Y. F. (2014). Modulation of sarcolemmal ATP-sensitive potassium channels by nitric oxide via sGC/PKG/ROS/ERK1/2/CaMKII signaling in ventricular cardiomyocytes. J. Physiol. 592(Pt 5), 971-990. doi: 10.1113/jphysiol.2013.264697.