CaMKII-dependent phosphorylation of cardiac ryanodine receptors regulates cell death in cardiac ischemia/reperfusion injury

Journal of Molecular and Cellular Cardiology

Volumn 74, Issue , 2014, Pages 274-283

  Di Carlo, Mariano N ^a   Said, Matilde ^a   Ling, Haiyun ^b   Valverde, Carlos A ^a   De Giusti, Verónica C ^a   Sommese, Leandro ^a   Palomeque, Julieta ^a   Aiello, Ernesto A ^a   Skapura, Darlene G ^c   Rinaldi, Gustavo ^a   Respress, Jonathan L ^c   Brown, Joan Heller ^b   Wehrens, Xander H T ^c   Salas, Margarita A ^a   Mattiazzi, Alicia ^a  

^a FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

^b San Diego   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; CaMKII; Ischemia reperfusion injury; Myocardium; Necrosis; RyR2 PLN

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; LACTATE DEHYDROGENASE; PHOSPHOLAMBAN; RYANODINE RECEPTOR 2; CALCIUM; CALCIUM BINDING PROTEIN; RYANODINE RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RELEASE; HEART INFARCTION SIZE; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART MUSCLE CONTRACTILITY; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REPERFUSION INJURY; ANIMAL; CALCIUM SIGNALING; CYTOLOGY; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; HEART MUSCLE CELL; HEART VENTRICLE; METABOLISM; MUTATION; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PHOSPHORYLATION; PRIMARY CELL CULTURE; SARCOPLASMIC RETICULUM; TRANSGENIC MOUSE;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL DEATH; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; HEART VENTRICLES; MALE; MICE; MICE, TRANSGENIC; MUTATION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; ORGAN CULTURE TECHNIQUES; PHOSPHORYLATION; PRIMARY CELL CULTURE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 84904738389     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.06.004     Document Type: Article

References (38)

1. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D., Blaha M.J., et al. Heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 2014, 129:e28-e292.
2. Braunwald E., Kloner R.A. Myocardial reperfusion: a double-edged sword?. J Clin Invest 1985, 76:1713-1719.
3. Garcia-Dorado D., Ruiz-Meana M., Inserte J., Rodriguez-Sinovas A., Piper H.M. Calcium-mediated cell death during myocardial reperfusion. Cardiovasc Res 2012, 94:168-180.
4. Said M., Becerra R., Valverde C.A., Kaetzel M.A., Dedman J.R., Mundina-Weilenmann C., et al. Calcium-calmodulin dependent protein kinase II (CaMKII): a main signal responsible for early reperfusion arrhythmias. J Mol Cell Cardiol 2011, 51:936-944.
5. Piper H.M., Kasseckert S., Abdallah Y. The sarcoplasmic reticulum as the primary target of reperfusion protection. Cardiovasc Res 2006, 70:170-173.
6. 2+ after perfusion arrest in isolated, perfused mouse heart. Cardiovasc Res 2006, 70:335-345.
7. Steenbergen C., Murphy E., Watts J.A., London R.E. Correlation between cytosolic free calcium, contracture, ATP, and irreversible ischemic injury in perfused rat heart. Circ Res 1990, 66:135-146.
8. Fabiato A., Fabiato F. Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cells from adult human, dog, cat, rabbit, rat, and frog hearts and from fetal and new-born rat ventricles. Ann N Y Acad Sci 1978, 307:491-522.
9. Kranias E.G., Hajjar R.J. Modulation of cardiac contractility by the phospholamban/SERCA2a regulatome. Circ Res 2012, 110:1646-1660.
10. Lam C.K., Zhao W., Cai W., Vafiadaki E., Florea S.M., Ren X., et al. Novel role of HAX-1 in ischemic injury protection involvement of heat shock protein 90. Circ Res 2013, 112:79-89.
11. Salas M.A., Valverde C.A., Sanchez G., Said M., Rodriguez J.S., Portiansky E.L., et al. The signalling pathway of CaMKII-mediated apoptosis and necrosis in the ischemia/reperfusion injury. J Mol Cell Cardiol 2010, 48:1298-1306.
12. Vila-Petroff M., Salas M.A., Said M., Valverde C.A., Sapia L., Portiansky E., et al. CaMKII inhibition protects against necrosis and apoptosis in irreversible ischemia-reperfusion injury. Cardiovasc Res 2007, 73:689-698.
13. del Monte F., Lebeche D., Guerrero J.L., Tsuji T., Doye A.A., Gwathmey J.K., et al. Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc Natl Acad Sci U S A 2004, 101:5622-5627.
14. 2+ ATPase pump overexpression in a porcine model of ischemia reperfusion. Circulation 2008, 118:614-624.
15. Kumada Y., Yamamoto F., Yamamoto H., Ishikawa T., Kagisaki K., Hirose H. Decreasing sarcoplasmic reticular calcium gives rise to myocardial protection-the effect of thapsigargin for myocardial protection under conditions of normothermia. Jpn J Thorac Cardiovasc Surg 1998, 46:368-374.
16. Zucchi R., Ronca F., Ronca-Testoni S. Modulation of sarcoplasmic reticulum function: a new strategy in cardioprotection?. Pharmacol Ther 2001, 89:47-65.
17. Avellanal M., Rodriguez P., Barrigon S. Protective effects of cyclopiazonic acid on ischemia-reperfusion injury in rabbit hearts. J Cardiovasc Pharmacol 1998, 32:845-851.
18. Cross H.R., Kranias E.G., Murphy E., Steenbergen C. Ablation of PLB exacerbates ischemic injury to a lesser extent in female than male mice: protective role of NO. Am J Physiol 2003, 284:H683-H690.
19. 2+ handling but exacerbates cardiac dysfunction in CaMKIIdelta(C) transgenic mice. Circ Res 2010, 106:354-362.
20. Zhao W., Waggoner J.R., Zhang Z.G., Lam C.K., Han P., Qian J., et al. The anti-apoptotic protein HAX-1 is a regulator of cardiac function. Proc Natl Acad Sci U S A 2009, 106:20776-20781.
21. van Oort R.J., McCauley M.D., Dixit S.S., Pereira L., Yang Y., Respress J.L., et al. Ryanodine receptor phosphorylation by calcium/calmodulin-dependent protein kinase II promotes life-threatening ventricular arrhythmias in mice with heart failure. Circulation 2010, 122:2669-2679.
22. 2+ leak promotes atrial fibrillation in mice. J Clin Invest 2009, 119:1940-1951.
23. 2+/calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. J Clin Invest 2009, 119:1230-1240.
24. Brittsan A.G., Kranias E.G. Phospholamban and cardiac contractile function. J Mol Cell Cardiol 2000, 32:2131-2139.
25. 2+/calmodulin-dependent protein kinase II delta mediates myocardial ischemia/reperfusion injury through nuclear factor-kappaB. Circ Res 2013, 112:935-944.
26. Said M., Vittone L., Mundina-Weilenmann C., Ferrero P., Kranias E.G., Mattiazzi A. Role of dual-site phospholamban phosphorylation in the stunned heart: insights from phospholamban site-specific mutants. Am J Physiol 2003, 285:H1198-H1205.
27. 2+ handling determine the negative staircase in a cellular heart failure model. J Card Fail 2007, 13:143-154.
28. 2+-calmodulin protein kinase II and promotes a death pathway conserved across different species. Circ Res 2009, 105:1204-1212.
29. 2+- and protein kinase C-dependent mechanism. Am J Physiol 2001, 280:H1528-H1536.
30. 2+/calmodulin-dependent protein kinase II induces hypertrophy and dilated cardiomyopathy associated with increased protein phosphatase 2A activity. J Biol Chem 2002, 277:1261-1267.
31. Vittone L., Mundina-Weilenmann C., Said M., Ferrero P., Mattiazzi A. Time course and mechanisms of phosphorylation of phospholamban residues in ischemia-reperfused rat hearts. Dissociation of phospholamban phosphorylation pathways. J Mol Cell Cardiol 2002, 34:39-50.
32. 2+ depletion of the sarcoplasmic reticulum at the onset of reperfusion. Cardiovasc Res 2010, 85:671-680.
33. Pedrozo Z., Sanchez G., Torrealba N., Valenzuela R., Fernandez C., Hidalgo C., et al. Calpains and proteasomes mediate degradation of ryanodine receptors in a model of cardiac ischemic reperfusion. Biochim Biophys Acta 1802, 2010:356-362.
34. Cohen M.V., Yang X.M., Downey J.M. Smaller infarct after preconditioning does not predict extent of early functional improvement of reperfused heart. Am J Physiol 1999, 277:H1754-H1761.
35. 2+ release kinetics during beta-adrenergic stimulation. J Mol Cell Cardiol 2007, 43:281-291.
36. Nicolaou P., Rodriguez P., Ren X., Zhou X., Qian J., Sadayappan S., et al. Inducible expression of active protein phosphatase-1 inhibitor-1 enhances basal cardiac function and protects against ischemia/reperfusion injury. Circ Res 2009, 104:1012-1020.
37. Yang Y., Zhu W.Z., Joiner M.L., Zhang R., Oddis C.V., Hou Y., et al. Calmodulin kinase II inhibition protects against myocardial cell apoptosis in vivo. Am J Physiol 2006, 291:H3065-H3075.
38. Luo W., Grupp I.L., Harrer J., Ponniah S., Grupp G., Duffy J.J., et al. Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation. Circ Res 1994, 75:401-409.