Reactive oxygen species-activated Ca/calmodulin kinase IIδ is required for late INa augmentation leading to cellular Na and Ca overload

Circulation Research

Volumn 108, Issue 5, 2011, Pages 555-565

  Wagner, Stefan ^a   Ruff, Hanna M ^a   Weber, Sarah L ^a   Bellmann, Sarah ^a   Sowa, Thomas ^a   Schulte, Timo ^a   Anderson, Mark E ^e   Grandi, Eleonora ^d   Bers, Donald M ^d   Backs, Johannes ^b   Belardinelli, Luiz ^c   Maier, Lars S ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c Gilead Sciences   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

Ca2+ calmodulin dependent protein kinase II; Na+ current; reactive oxygen species; sarcoplasmic reticulum; sodium channels

Indexed keywords

BROMINE; CAFFEINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; SODIUM CHANNEL; THAPSIGARGIN;

ADENOVIRUS; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME METABOLISM; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART MUSCLE CONTRACTURE; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; SARCOPLASMIC RETICULUM; SODIUM CELL LEVEL; SODIUM CURRENT; VIRAL GENE DELIVERY SYSTEM; WILD TYPE;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELLS, CULTURED; HYDROGEN PEROXIDE; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; MYOCYTES, CARDIAC; PATCH-CLAMP TECHNIQUES; RABBITS; REACTIVE OXYGEN SPECIES; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SODIUM; SODIUM CHANNELS;

EID: 79952772425     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.221911     Document Type: Article

References (62)

1. Tsutsui H, Ide T, Hayashidani S, Suematsu N, Utsumi H, Nakamura R, Egashira K, Takeshita A. Greater susceptibility of failing cardiac myocytes to oxygen free radical-mediated injury. Cardiovasc Res. 2001; 49:103-109.
2. Kinugawa S, Tsutsui H, Hayashidani S, Ide T, Suematsu N, Satoh S, Utsumi H, Takeshita A. Treatment with dimethylthiourea prevents left ventricular remodeling and failure after experimental myocardial infarction in mice: role of oxidative stress. Circ Res. 2000;87:392-398.
3. Mallat Z, Philip I, Lebret M, Chatel D, Maclouf J, Tedgui A. Elevated levels of 8-iso-prostaglandin F2alpha in pericardial fluid of patients with heart failure: a potential role for in vivo oxidant stress in ventricular dilatation and progression to heart failure. Circulation. 1998;97: 1536-1539. (Pubitemid 28186180)
4. Josephson R, Silverman H, Lakatta E, Stern M, Zweier J. Study of the mechanisms of hydrogen-peroxide and hydroxyl free radical-induced cellular injury and calcium overload in cardiac myocytes. J Biol Chem. 1991;266:2354-2361. (Pubitemid 21909071)
5. Wagner S, Seidler T, Picht E, Maier LS, Kazanski V, Teucher N, Schillinger W, Pieske B, Isenberg G, Hasenfuss G, Kögler H. Na-Ca2exchanger overexpression predisposes to reactive oxygen species-induced injury. Cardiovasc Res. 2003;60:404-412. (Pubitemid 37412374)
6. Song Y, Shryock J, Wagner S, Maier L, Belardinelli L. Blocking late sodium current reduces hydrogen peroxide-induced arrhythmogenic activity and contractile dysfunction. J Pharmacol Exp Ther. 2006;318: 214-222.
7. Corretti M, Koretsune Y, Kusuoka H, Chacko V, Zweier J, Marban E. Glycolytic inhibition and calcium overload as consequences of exogenously generated free-radicals in rabbit hearts. J Clin Invest. 1991;88: 1014-1025.
8. Haigney MC, Lakatta EG, Stern MD, Silverman HS. Sodium channel blockade reduces hypoxic sodium loading and sodium-dependent calcium loading. Circulation. 1994;90:391-399.
9. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell. 2008;133:462-474. (Pubitemid 351608692)
10. Ward CA, Giles WR. Ionic mechanism of the effects of hydrogen peroxide in rat ventricular myocytes. J Physiol. 1997;500:631-642. (Pubitemid 27207825)
11. Zeitz O, Maass AE, Van Nguyen P, Hensmann G, Kogler H, Moller K, Hasenfuss G, Janssen PM. Hydroxyl radical-induced acute diastolic dysfunction is due to calcium overload via reverse-mode Na-Ca2exchange. Circ Res. 2002;90:988-995. (Pubitemid 34633865)
12. Inserte J, Garcia-Dorado D, Ruiz-Meana M, Padilla F, Barrabes JA, Pina P, Agullo L, Piper HM, Soler-Soler J. Effect of inhibition of Na/Ca2exchanger at the time of myocardial reperfusion on hypercontracture and cell death. Cardiovasc Res. 2002;55:739-748.
13. Wagner S, Dybkova N, Rasenack ECL, Jacobshagen C, Fabritz L, Kirchhof P, Maier SKG, Zhang T, Hasenfuss G, Brown JH, Bers DM, Maier LS. Ca2/calmodulin-dependent protein kinase II regulates cardiac Nachannels. J Clin Invest. 2006;116:3127-3138. (Pubitemid 44878627)
14. Hudmon A, Schulman H. Structure-function of the multifunctional Ca2/ calmodulin-dependent protein kinase II. Biochem J. 2002;364:593-611. (Pubitemid 34680833)
15. Maier LS, Zhang T, Chen L, DeSantiago J, Brown JH, Bers DM. Transgenic CaMKII-c overexpression uniquely alters cardiac myocyte Ca2handling: reduced SR Ca2load and activated SR Ca2release. Circ Res. 2003;92:904-911.
16. Zhang R, Khoo MS, Wu Y, Yang Y, Grueter CE, Ni G, Price EE Jr, Thiel W, Guatimosim S, Song LS, Madu EC, Shah AN, Vishnivetskaya TA, Atkinson JB, Gurevich VV, Salama G, Lederer WJ, Colbran RJ, Anderson ME. Calmodulin kinase II inhibition protects against structural heart disease. Nat Med. 2005;11:409-417. (Pubitemid 40562331)
17. Backs J, Backs T, Neef S, Kreusser MM, Lehmann LH, Patrick DM, Grueter CE, Qi X, Richardson JA, Hill JA, Katus HA, Bassel-Duby R, Maier LS, Olson EN. Theisoform of CaM Kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload. Proc Natl Acad Sci USA. 2009;106:2342-2347.
18. Ling H, Zhang T, Pereira L, Means CK, Cheng H, Gu Y, Dalton ND, Peterson KL, Chen J, Bers D, Heller Brown J. Requirement for Ca2/ calmodulin-dependent kinase II in the transition from pressure overloadinduced cardiac hypertrophy to heart failure in mice. J Clin Invest. 2009;119:1230-1240.
19. Xie LH, Chen F, Karagueuzian HS, Weiss JN. Oxidative-stress-induced afterdepolarizations and calmodulin kinase II signaling. Circ Res. 2009; 104:79-86.
20. Xu L, Eu JP, Meissner G, Stamler JS. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-s-nitrosylation. Science. 1998;279:234-237. (Pubitemid 28103882)
21. Wagner S, Hacker E, Grandi E, Weber SL, Dybkova N, Sossalla S, Sowa T, Fabritz L, Kirchhof P, Bers DM, Maier LS. Ca/calmodulin kinase II differentially modulates potassium currents. Circ Arrhythm Electrophysiol. 2009; 2:285-294.
22. Schroder E, Eaton P. Hydrogen peroxide as an endogenous mediator and exogenous tool in cardiovascular research: issues and considerations. Curr Opin Pharmacol. 2008;8:153-159.
23. Wang GK, Wang SY. Modifications of human cardiac sodium channel gating by uva light. J Membr Biol. 2002;189:153-165. (Pubitemid 36026627)
24. Fukuda K, Davies SS, Nakajima T, Ong BH, Kupershmidt S, Fessel J, Amarnath V, Anderson ME, Boyden PA, Viswanathan PC, Roberts LJ II, Balser JR. Oxidative mediated lipid peroxidation recapitulates proarrhythmic effects on cardiac sodium channels. Circ Res. 2005;97:1262-1269.
25. Gao L, Blair L, Marshall J. CaMKII-independent effects of KN93 and its inactive analog KN92: reversible inhibition of L-type calcium channels. Biochem Biophys Res Comm. 2006;345:1606-1610. (Pubitemid 43817913)
26. Kohlhaas M, Zhang T, Seidler T, Zibrova D, Dybkova N, Steen A, Wagner S, Chen L, Brown J, Bers D, Maier L. Increased sarcoplasmic reticulum calcium leak but unaltered contractility by acute CaMKII overexpression in isolated rabbit cardiac myocytes. Circ Res. 2006;98: 235-244.
27. Song YH, Cho H, Ryu SY, Yoon JY, Park SH, Noh CI, Lee SH, Ho WK. L-type Ca2channel facilitation mediated by H2O2-induced activation of CaMKII in rat ventricular myocytes. J Mol Cell Cardiol. 2010;48: 773-780.
28. Palomeque J, Rueda OV, Sapia L, Valverde CA, Salas M, Petroff MV, Mattiazzi A. Angiotensin II-induced oxidative stress resets the Ca2dependence of Ca2-calmodulin protein kinase II and promotes a death pathway conserved across different species. Circ Res. 2009;105: 1204-1212.
29. Boraso A, Williams AJ. Modification of the gating of the cardiac sarcoplasmic reticulum Ca2-release channel by H2O2 and dithiothreitol. Am J Physiol. 1994;267:H1010-H1016.
30. Favero TG, Zable AC, Abramson JJ. Hydrogen peroxide stimulates the Ca2release channel from skeletal muscle sarcoplasmic reticulum. J Biol Chem. 1995;270:25557-25563.
31. Anzai K, Ogawa K, Kuniyasu A, Ozawa T, Yamamoto H, Nakayama H. Effects of hydroxyl radical and sulfhydryl reagents on the open probability of the purified cardiac ryanodine receptor channel incorporated into planar lipid bilayers. Biochem Biophys Res Comm. 1998;249:938-942. (Pubitemid 28441942)
32. Zissimopoulos S, Docrat N, Lai FA. Redox sensitivity of the ryanodine receptor interaction with FK506-binding protein. J Biol Chem. 2007;282: 6976-6983. (Pubitemid 47093660)
33. Rowe GT, Manson NH, Caplan M, Hess ML. Hydrogen peroxide and hydroxyl radical mediation of activated leukocyte depression of cardiac sarcoplasmic reticulum. Participation of the cyclooxygenase pathway. Circ Res. 1983;53:584-591. (Pubitemid 14248483)
34. Kourie J. Interaction of reactive oxygen species with ion transport mechanisms. Am J Physiol Cell Physiol. 1998;275:C1-C24. (Pubitemid 28381298)
35. Barrington P, Meier C, Weglicki W. Abnormal electrical-activity induced by free-radical generating systems in isolated cardiocytes. J Mol Cell Cardiol. 1988;20:1163-1178. (Pubitemid 19059026)
36. Kassmann M, Hansel A, Leipold E, Birkenbeil J, Lu SQ, Hoshi T, Heinemann SH. Oxidation of multiple methionine residues impairs rapid sodium channel inactivation. Pflugers Arch. 2008;456:1085-1095.
37. Aiba T, Hesketh G, Liu T, Carlisle R, Villa-Abrille M, O'Rourke B, Akar F, Tomaselli G. Nachannel regulation by Ca2/calmodulin and Ca2/ calmodulin-dependent protein kinase II in guinea-pig ventricular myocytes. Cardiovasc Res. 2010;85:454-463.
38. Hund T, Koval O, Li J, Wright P, Dian L, Snyder J, Gudmundsson H, Kline C, Davidson N, Cardona N, Rasband M, Anderson M, Mohler P. A-iv-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J Clin Invest. 2010;120:3508-3519.
39. Maltsev VA, Kyle JW, Undrovinas A. Late Nacurrent produced by human cardiac Nachannel isoform Nav1.5 is modulated by its1 subunit. J Physiol Sci. 2009;59:217-225.
40. Brennan J, Bardswell S, Burgoyne J, Fuller W, Schroder E, Wait R, Begum S, Kentish J, Eaton P. Oxidant-induced activation of type I protein kinase A is mediated by RI subunit interprotein disulfide bond formation. J Biol Chem. 2006;281:21827-21836. (Pubitemid 44191910)
41. Hallaq H, Yang Z, Viswanathan P, Fukuda K, Shen W, Wang D, Wells K, Zhou J, Yi J, Murray K. Quantitation of protein kinase A-mediated trafficking of cardiac sodium channels in living cells. Cardiovasc Res. 2006;72:250-261. (Pubitemid 44511919)
42. Murphy BJ, Rogers J, Perdichizzi AP, Colvin AA, Catterall WA. cAMPdependent phosphorylation of two sites in thesubunit of the cardiac sodium channel. J Biol Chem. 1996;271:28837-28843. (Pubitemid 26382582)
43. Frohnwieser B, Chen L, Schreibmayer W, Kallen R. Modulation of the human cardiac sodium channel-subunit by cAMP-dependent protein kinase and the responsible sequence domain. J Physiol (Lond). 1997;498: 309-318. (Pubitemid 27073377)
44. Gopalakrishna R, Anderson W. Ca2-independent and phospholipidindependent activation of protein kinase C by selective oxidative modification of the regulatory domain. Proc Nat Acad Sci. 1989;86:6758-6762.
45. Qu Y, Rogers J, Tanada T, Scheuer T, Catterall W. Modulation of cardiac Nachannels expressed in a mammalian cell line and in ventricular myocytes by protein kinase C. Proc Nat Acad Sci. 1994;91:3289-3293. (Pubitemid 24130222)
46. Murray KT, Hu N, Daw JR, Shin HG, Watson MT, Mashburn AB, George AL Jr. Functional effects of protein kinase C activation on the human cardiac Nachannel. Circ Res. 1997;80:370-376. (Pubitemid 27093351)
47. Qu Y, Rogers J, Tanada T, Catterall W, Scheuer T. Phosphorylation of S1505 in the cardiac Nachannel inactivation gate is required for modulation by protein kinase C. J Gen Physiol. 1996;108:375-379. (Pubitemid 26374748)
48. Williams IA, Xiao XH, Ju YK, Allen DG. The rise of [Na]i during ischemia and reperfusion in the rat heart-underlying mechanisms. Pflugers Arch. 2007;454:903-912. (Pubitemid 47338451)
49. Shattock MJ, Matsuura H. Measurement of Na-Kpump current in isolated rabbit ventricular myocytes using the whole-cell voltage-clamp technique. Inhibition of the pump by oxidant stress. Circ Res. 1993;72: 91-101.
50. Goldhaber J, Liu E. Excitation-contraction coupling in single guinea-pig ventricular myocytes exposed to hydrogen-peroxide. J Physiol (Lond). 1994:477(Pt 1):135-147. (Pubitemid 24163279)
51. Goldhaber J. Free radicals enhance Na/Ca2exchange in ventricular myocytes. Am J Physiol Heart Circ Physiol. 1996;271:H823-H833.
52. Soliman D, Hamming K, Matemisz L, Light P. Reactive oxygen species directly modify sodium-calcium exchanger activity in a splice variantdependent manner. J Mol Cell Cardiol. 2009;47:595-602.
53. Grandi E, Puglisi J, Wagner S, Maier L, Severi S, Bers D. Simulation of Ca-calmodulin-dependent protein kinase II on rabbit ventricular myocyte ion currents and action potentials. Biophys J. 2007;93:3835-3847. (Pubitemid 350223802)
54. Despa S, Islam MA, Weber CR, Pogwizd SM, Bers DM. Intracellular Naconcentration is elevated in heart failure but Na/K pump function is unchanged. Circulation. 2002;105:2543-2548. (Pubitemid 34568978)
55. Weber C, Piacentino V, Houser S, Bers D. Dynamic regulation of sodium/ calcium exchange function in human heart failure. Circulation. 2003; 108:2224-2229. (Pubitemid 37363039)
56. Haigney MC, Miyata H, Lakatta EG, Stern MD, Silverman HS. Dependence of hypoxic cellular calcium loading on Na-Ca2exchange. Circ Res. 1992;71:547-557.
57. Undrovinas N, Maltsev V, Belardinelli L, Sabbah HN, Undrovinas A. Late sodium current contributes to diastolic cell Ca2accumulation in chronic heart failure. J Physiol Sci. 2010;60:245-257.
58. Lu Z, Abe J, Taunton J, Lu Y, Shishido T, McClain C, Yan C, Xu SP, Spangenberg TM, Xu H. Reactive oxygen species-induced activation of p90 ribosomal S6 kinase prolongs cardiac repolarization through inhibiting outward Kchannel activity. Circ Res. 2008;103:269-278.
59. Hoch B, Meyer R, Hetzer R, Krause EG, Karczewski P. Identification and expression of-isoforms of the multifunctional Ca2/calmodulindependent protein kinase in failing and nonfailing human myocardium. Circ Res. 1999;84:713-721. (Pubitemid 29157339)
60. Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM. Ca2/calmodulin- dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2leak in heart failure. Circ Res. 2005;97:1314-1322.
61. Currie S, Loughrey CM, Craig MA, Smith GL. Calcium/calmodulindependent protein kinase IIassociates with the ryanodine receptor complex and regulates channel function in rabbit heart. Biochem J. 2004;377:357-366. (Pubitemid 38142191)
62. Valdivia CR, Chu WW, Pu J, Foell JD, Haworth RA, Wolff MR, Kamp TJ, Makielski JC. Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. J Mol Cell Cardiol. 2005;38:475-483. (Pubitemid 40331938)