CaMKIIδ mediates β-adrenergic effects on RyR2 phosphorylation and SR Ca2+ leak and the pathophysiological response to chronic β-adrenergic stimulation

Journal of Molecular and Cellular Cardiology

Volumn 85, Issue , 2015, Pages 282-291

  Grimm, Michael ^a,d   Ling, Haiyun ^a,e   Willeford, Andrew ^a   Pereira, Laetitia ^b   Gray, Charles B B ^a   Erickson, Jeffrey R ^b,f   Sarma, Satyam ^c,g   Respress, Jonathan L ^c   Wehrens, Xander H T ^c   Bers, Donald M ^b   Brown, Joan Heller ^a  

^a San Diego   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d Receptos Inc   (United States)

^e GILEAD SCIENCES   (United States)

^f UNIVERSITY OF OTAGO   (New Zealand)

^g NONE   (United States)

Author keywords

Beta adrenergic; CaMKII; Fibrosis; Hypertrophy; Phosphorylation

Indexed keywords

BETA ADRENERGIC RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II DELTA; PHOSPHOLAMBAN; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CALCIUM; CALCIUM BINDING PROTEIN; ISOPRENALINE; RYANODINE RECEPTOR; RYANODINE RECEPTOR 2. MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETA ADRENERGIC STIMULATION; BINDING SITE; CHRONIC STRESS; CHRONOTROPISM; CONTROLLED STUDY; DISEASE ASSOCIATION; FIGHT OR FLIGHT RESPONSE; GENE DELETION; HEART FUNCTION; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; INOTROPISM; LUNG CONGESTION; MALE; MOUSE; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; C57BL MOUSE; CALCIUM SIGNALING; CARDIAC MUSCLE CELL; CARDIOMEGALY; CARDIOMYOPATHY; CELL CULTURE; DRUG EFFECTS; ENZYMOLOGY; FIBROSIS; HEART VENTRICLE REMODELING; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ADRENERGIC BETA-AGONISTS; ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CARDIOMEGALY; CARDIOMYOPATHIES; CELLS, CULTURED; FIBROSIS; ISOPROTERENOL; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; VENTRICULAR REMODELING;

EID: 84939434166     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.06.007     Document Type: Article

References (56)

1. Anderson M.E., Brown J.H., Bers D.M. CaMKII in myocardial hypertrophy and heart failure. J Mol Cell Cardiol 2011, 51:468-473.
2. De Koninck P., Schulman H. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 1998, 279:227-230.
3. Erickson J.R., Joiner M.L., Guan X., Kutschke W., Yang J., Oddis C.V., et al. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 2008, 133:462-474.
4. Erickson J.R., Pereira L., Wang L., Han G., Ferguson A., Dao K., et al. Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature 2013, 502:372-376.
5. Wu X., Zhang T., Bossuyt J., Li X., McKinsey T.A., Dedman J.R., et al. Local InsP3-dependent perinuclear Ca2+ signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest 2006, 116:675-682.
6. Grimm M., Brown J.H. Beta-adrenergic receptor signaling in the heart: role of CaMKII. J Mol Cell Cardiol 2010, 48:322-330.
7. Grimm M., Ling H., Brown J.H. Crossing signals: relationships between beta-adrenergic stimulation and CaMKII activation. Heart Rhythm 2011, 8:1296-1298.
8. Xu L., Lai D., Cheng J., Lim H.J., Keskanokwong T., Backs J., et al. Alterations of L-type calcium current and cardiac function in CaMKII{delta} knockout mice. Circ Res 2010, 107:398-407.
9. Pereira L., Metrich M., Fernandez-Velasco M., Lucas A., Leroy J., Perrier R., et al. The cAMP binding protein Epac modulates Ca2+ sparks by a Ca2+/calmodulin kinase signalling pathway in rat cardiac myocytes. J Physiol 2007, 583:685-694.
10. Pereira L., Ruiz-Hurtado G., Morel E., Laurent A.C., Metrich M., Dominguez-Rodriguez A., et al. Epac enhances excitation-transcription coupling in cardiac myocytes. J Mol Cell Cardiol 2012, 52:283-291.
11. Oestreich E.A., Malik S., Goonasekera S.A., Blaxall B.C., Kelley G.G., Dirksen R.T., et al. Epac and phospholipase Cepsilon regulate Ca2+ release in the heart by activation of protein kinase C epsilon and calcium-calmodulin kinase II. J Biol Chem 2009, 284:1514-1522.
12. Mangmool S., Shukla A.K., Rockman H.A. beta-Arrestin-dependent activation of Ca(2+)/calmodulin kinase II after beta(1)-adrenergic receptor stimulation. J Cell Biol 2010, 189:573-587.
13. Ziolo M.T., Katoh H., Bers D.M. Positive and negative effects of nitric oxide on Ca(2+) sparks: influence of beta-adrenergic stimulation. Am J Physiol Heart Circ Physiol 2001, 281:H2295-H2303.
14. Curran J., Tang L., Roof S.R., Velmurugan S., Millard A., Shonts S., et al. Nitric oxide-dependent activation of CaMKII increases diastolic sarcoplasmic reticulum calcium release in cardiac myocytes in response to adrenergic stimulation. PLoS One 2014, 9:e87495.
15. Ling H., Zhang T., Pereira L., Means C.K., Cheng H., Gu Y., et al. Requirement for Ca2+/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.
16. Zhang R., Khoo M.S., Wu Y., Yang Y., Grueter C.E., Ni G., et al. Calmodulin kinase II inhibition protects against structural heart disease. Nat Med 2005, 11:409-417.
17. Bristow M.R. Treatment of chronic heart failure with beta-adrenergic receptor antagonists: a convergence of receptor pharmacology and clinical cardiology. Circ Res 2011, 109:1176-1194.
18. Colomer J.M., Mao L., Rockman H.A., Means A.R. Pressure overload selectively up-regulates Ca2+/calmodulin-dependent protein kinase II in vivo. Mol Endocrinol 2003, 17:183-192.
19. Zhang T., Maier L.S., Dalton N.D., Miyamoto S., Ross J., Bers D.M., et al. The deltaC isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ Res 2003, 92:912-919.
20. Ai X., Curran J.W., Shannon T.R., Bers D.M., Pogwizd S.M. Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 2005, 97:1314-1322.
21. Hoch B., Meyer R., Hetzer R., Krause E.G., Karczewski P. Identification and expression of delta-isoforms of the multifunctional Ca2+/calmodulin-dependent protein kinase in failing and nonfailing human myocardium. Circ Res 1999, 84:713-721.
22. Sossalla S., Fluschnik N., Schotola H., Ort K.R., Neef S., Schulte T., et al. Inhibition of elevated Ca2+/calmodulin-dependent protein kinase II improves contractility in human failing myocardium. Circ Res 2010, 107:1150-1161.
23. Ling H., Gray C.B., Zambon A.C., Grimm M., Gu Y., Dalton N., et al. Ca2+/calmodulin-dependent protein kinase II delta mediates myocardial ischemia/reperfusion injury through nuclear factor-kappaB. Circ Res 2013, 112:935-944.
24. Chelu M.G., Sarma S., Sood S., Wang S., van Oort R.J., Skapura D.G., et al. Calmodulin kinase II-mediated sarcoplasmic reticulum Ca2+ leak promotes atrial fibrillation in mice. J Clin Invest 2009, 119:1940-1951.
25. Pereira L., Cheng H., Lao D.H., Na L., van Oort R.J., Brown J.H., et al. Epac2 mediates cardiac beta1-adrenergic-dependent sarcoplasmic reticulum Ca2+ leak and arrhythmia. Circulation 2013, 127:913-922.
26. Gaspard G.J., Pasumarthi K.B. Quantification of cardiac fibrosis by colour-subtractive computer-assisted image analysis. Clin Exp Pharmacol Physiol 2008, 35:679-686.
27. Respress J.L., Wehrens X.H. Transthoracic echocardiography in mice. J Vis Exp 2010, 39:1738.
28. Witcher D.R., Kovacs R.J., Schulman H., Cefali D.C., Jones L.R. Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J Biol Chem 1991, 266:11144-11152.
29. Davis B.A., Schwartz A., Samaha F.J., Kranias E.G. Regulation of cardiac sarcoplasmic reticulum calcium transport by calcium-calmodulin-dependent phosphorylation. J Biol Chem 1983, 258:13587-13591.
30. Respress J.L., van Oort R.J., Li N., Rolim N., Dixit S.S., deAlmeida A., et al. Role of RyR2 phosphorylation at S2814 during heart failure progression. Circ Res 2012, 110:1474-1483.
31. 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.
32. Guo T., Zhang T., Mestril R., Bers D.M. Ca2+/calmodulin-dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes. Circ Res 2006, 99:398-406.
33. Xiang S.Y., Vanhoutte D., Del Re D.P., Purcell N.H., Ling H., Banerjee I., et al. RhoA protects the mouse heart against ischemia/reperfusion injury. J Clin Invest 2011, 121:3269-3276.
34. Neef S., Sag C.M., Daut M., Baumer H., Grefe C., El-Armouche A., et al. While systolic cardiomyocyte function is preserved, diastolic myocyte function and recovery from acidosis are impaired in CaMKIIdelta-KO mice. J Mol Cell Cardiol 2013, 59:107-116.
35. Kudej R.K., Iwase M., Uechi M., Vatner D.E., Oka N., Ishikawa Y., et al. Effects of chronic beta-adrenergic receptor stimulation in mice. J Mol Cell Cardiol 1997, 29:2735-2746.
36. Faulx M.D., Ernsberger P., Vatner D., Hoffman R.D., Lewis W., Strachan R., et al. Strain-dependent beta-adrenergic receptor function influences myocardial responses to isoproterenol stimulation in mice. Am J Physiol Heart Circ Physiol 2005, 289:H30-H36.
37. Hohimer A.R., Davis L.E., Hatton D.C. Repeated daily injections and osmotic pump infusion of isoproterenol cause similar increases in cardiac mass but have different effects on blood pressure. Can J Physiol Pharmacol 2005, 83:191-197.
38. Westenbrink B.D., Ling H., Divakaruni A.S., Gray C.B., Zambon A.C., Dalton N.D., et al. Mitochondrial reprogramming induced by CaMKIIdelta mediates hypertrophy decompensation. Circ Res 2015, 116:e28-e39.
39. Kreusser M.M., Lehmann L.H., Keranov S., Hoting M.O., Kohlhaas M., Reil J.C., et al. The cardiac CaMKII genes delta and gamma contribute redundantly to adverse remodeling but inhibit calcineurin-induced myocardial hypertrophy. Circulation 2014, 130:1262-1273.
40. Berthonneche C., Peter B., Schupfer F., Hayoz P., Kutalik Z., Abriel H., et al. Cardiovascular response to beta-adrenergic blockade or activation in 23 inbred mouse strains. PLoS One 2009, 4:e6610.
41. 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.
42. Wehrens X.H., Lehnart S.E., Reiken S.R., Marks A.R. Ca2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 2004, 94:e61-e70.
43. Curran J., Hinton M.J., Rios E., Bers D.M., Shannon T.R. Beta-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ Res 2007, 100:391-398.
44. Ferrero P., Said M., Sanchez G., Vittone L., Valverde C., Donoso P., et al. Ca2+/calmodulin kinase II increases ryanodine binding and Ca2+-induced sarcoplasmic reticulum Ca2+ release kinetics during beta-adrenergic stimulation. J Mol Cell Cardiol 2007, 43:281-291.
45. 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.
46. Zhang T., Guo T., Mishra S., Dalton N.D., Kranias E.G., Peterson K.L., et al. Phospholamban ablation rescues sarcoplasmic reticulum Ca(2+) handling but exacerbates cardiac dysfunction in CaMKIIdelta(C) transgenic mice. Circ Res 2010, 106:354-362.
47. Joiner M.L., Koval O.M., Li J., He B.J., Allamargot C., Gao Z., et al. CaMKII determines mitochondrial stress responses in heart. Nature 2012, 491:269-273.
48. 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 Heart Circ Physiol 2006, 291:H3065-H3075.
49. Zhang X., Szeto C., Gao E., Tang M., Jin J., Fu Q., et al. Cardiotoxic and cardioprotective features of chronic beta-adrenergic signaling. Circ Res 2013, 112:498-509.
50. Zhu W., Woo A.Y., Yang D., Cheng H., Crow M.T., Xiao R.P. Activation of CaMKIIdeltaC is a common intermediate of diverse death stimuli-induced heart muscle cell apoptosis. J Biol Chem 2007, 282:10833-10839.
51. Zhu W.Z., Wang S.Q., Chakir K., Yang D., Zhang T., Brown J.H., et al. Linkage of beta1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+/calmodulin kinase II. J Clin Invest 2003, 111:617-625.
52. Wang W., Zhang H., Gao H., Kubo H., Berretta R.M., Chen X., et al. {beta}1-Adrenergic receptor activation induces mouse cardiac myocyte death through both L-type calcium channel-dependent and -independent pathways. Am J Physiol Heart Circ Physiol 2010, 299:H322-H331.
53. Dolmatova E., Spagnol G., Boassa D., Baum J.R., Keith K., Ambrosi C., et al. Cardiomyocyte ATP release through pannexin 1 aids in early fibroblast activation. Am J Physiol Heart Circ Physiol 2012, 303:H1208-H1218.
54. Koitabashi N., Danner T., Zaiman A.L., Pinto Y.M., Rowell J., Mankowski J., et al. Pivotal role of cardiomyocyte TGF-beta signaling in the murine pathological response to sustained pressure overload. J Clin Invest 2011, 121:2301-2312.
55. Taimor G., Schluter K.D., Frischkopf K., Flesch M., Rosenkranz S., Piper H.M. Autocrine regulation of TGF beta expression in adult cardiomyocytes. J Mol Cell Cardiol 1999, 31:2127-2136.
56. Lijnen P.J., Petrov V.V., Fagard R.H. Induction of cardiac fibrosis by transforming growth factor-beta(1). Mol Genet Metab 2000, 71:418-435.