Oxidative stress-induced afterdepolarizations and calmodulin kinase II signaling

Circulation Research

Volumn 104, Issue 1, 2009, Pages 79-86

  Xie, Lai Hua ^a   Chen, Fuhua ^b   Karagueuzian, Hrayr S ^b   Weiss, James N ^b  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arrhythmia; CaM kinase; Early afterdepolarization; Reactive oxidative species; Triggered activity

Indexed keywords

CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; HYDROGEN PEROXIDE; NIFEDIPINE; TETRODOTOXIN; AUTOCAMPTIDE 2 RELATED INHIBITORY PEPTIDE II; AUTOCAMPTIDE-2-RELATED INHIBITORY PEPTIDE II; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; COELENTERATE VENOM; PEPTIDE; SODIUM CHANNEL BLOCKING AGENT; TOXIN II (ANEMONIA SULCATA);

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPOLARIZATION; ENZYME ACTIVATION; EXPERIMENTAL RABBIT; HEART MUSCLE CELL; HEART VENTRICLE; HEART VENTRICLE ARRHYTHMIA; NONHUMAN; OXIDATIVE STRESS; PATCH CLAMP; PRIORITY JOURNAL; REPOLARIZATION; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; ACTIVE TRANSPORT; ANIMAL; CALCIUM SIGNALING; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; RABBIT;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CNIDARIAN VENOMS; HEART VENTRICLES; HYDROGEN PEROXIDE; MYOCYTES, CARDIAC; NIFEDIPINE; OXIDATIVE STRESS; PATCH-CLAMP TECHNIQUES; PEPTIDES; RABBITS; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN;

EID: 59649127713     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.183475     Document Type: Article

References (46)

1. Lakatta EG, Sollott SJ. The "heartbreak" of older age. Mol Interv. 2002; 2:431-446.
2. Slezak J, Tribulova N, Pristacova J, Uhrik B, Thomas T, Khaper N, Kaul N, Singal PK. Hydrogen peroxide changes in ischemic and reperfused heart. Cytochemistry and biochemical and X-ray microanalysis. Am J Pathol. 1995;147:772-781.
3. Corretti MC, Koretsune Y, Kusuoka H, Chacko VP, Zweier JL, Marban E. Glycolytic inhibition and calcium overload as consequences of exog-enously generated free radicals in rabbit hearts. J Clin Invest. 1991;88: 1014-1025.
4. Ward CA, Giles WR. Ionic mechanism of the effects of hydrogen peroxide in rat ventricular myocytes. J Physiol. 1997;500:631-642.
5. Song Y, Shryock JC, Wagner S, Maier LS, Belardinelli L. Blocking late sodium current reduces hydrogen peroxide-induced arrhythmogenic activity and contractile dysfunction. J Pharmacol Exp Ther. 2006;318: 214-222.
6. Barrington PL, Meier CF Jr, Weglicki WB. Abnormal electrical activity induced by H2O2 in isolated canine myocytes. Basic Life Sci. 1988;49: 927-932.
7. Guo J, Giles WR, Ward CA. Effect of hydrogen peroxide on the membrane currents of sinoatrial node cells from rabbit heart. Am J Physiol Heart Circ Physiol. 2000;279:H992-H999.
8. Hudasek K, Brown ST, Fearon IM. H2O2 regulates recombinant Ca2 + channel alpha1C subunits but does not mediate their sensitivity to acute hypoxia. Biochem Biophys Res Commun. 2004;318:135-141.
9. Goldhaber JI, Liu E. Excitation-contraction coupling in single guinea-pig ventricular myocytes exposed to hydrogen peroxide. J Physiol. 1994;477: 135-147.
10. Berube J, Caouette D, Daleau P. Hydrogen peroxide modifies the kinetics of HERG channel expressed in a mammalian cell line. J Pharmacol Exp Ther. 2001;297:96-102.
11. Anzai K, Ogawa K, Ozawa T, Yamamoto H. Oxidative modification of ion channel activity of ryanodine receptor. Antioxid Redox Signal. 2000; 2:35-40.
12. Zissimopoulos S, Docrat N, Lai FA. Redox sensitivity of the ryanodine receptor interaction with FK506-binding protein. J Biol Chem. 2007;282: 6976-6983.
13. Morris TE, Sulakhe PV. Sarcoplasmic reticulum Ca(2 + )-pump dysfunction in rat cardiomyocytes briefly exposed to hydroxyl radicals. Free Radic Biol Med. 1997;22:37-47.
14. Hinata M, Matsuoka I, Iwamoto T, Watanabe Y, Kimura J. Mechanism of Na+/Ca2+ exchanger activation by hydrogen peroxide in guinea-pig ventricular myocytes. J Pharmacol Sci. 2007;103:283-292.
15. Goldhaber JI. Free radicals enhance Na+/Ca2+ exchange in ventricular myocytes. Am J Physiol. 1996;271:H823-H833.
16. Zhu W, Woo AY, Yang D, Cheng H, Crow MT, Xiao RP. Activation of CaMKIIdeltaC is a common intermediate of diverse death stimuli-induced heart muscle cell apoptosis. J Biol Chem. 2007;282:10833-10839.
17. Howe CJ, Lahair MM, McCubrey JA, Franklin RA. Redox regulation of the calcium/calmodulin-dependent protein kinases. J Biol Chem. 2004; 279:44573-44581.
18. 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.
19. Wu Y, Temple J, Zhang R, Dzhura I, Zhang W, Trimble R, Roden DM, Passier R, Olson EN, Colbran RJ, Anderson ME. Calmodulin kinase II and arrhythmias in a mouse model of cardiac hypertrophy. Circulation. 2002;106:1288-1293.
20. Wu Y, MacMillan LB, McNeill RB, Colbran RJ, Anderson ME. CaM kinase augments cardiac L-type Ca2 + current: a cellular mechanism for long Q-T arrhythmias. Am J Physiol. 1999;276:H2168-H2178.
21. Wagner S, Dybkova N, Rasenack EC, Jacobshagen C, Fabritz L, Kirchhof P, Maier SK, Zhang T, Hasenfuss G, Brown JH, Bers DM, Maier LS. Ca2+/calmodulin-dependent protein kinase II regulates cardiac Na + channels. J Clin Invest. 2006;116:3127-3138.
22. Anderson ME, Braun AP, Wu Y, Lu T, Schulman H, Sung RJ. KN-93, an inhibitor of multifunctional Ca+ +/calmodulin-dependent protein kinase, decreases early afterdepolarizations in rabbit heart. J Pharmacol Exp Ther. 1998;287:996-1006.
23. Mantegazza M, Franceschetti S, Avanzini G. Anemone toxin (ATX II)-induced increase in persistent sodium current: effects on the firing properties of rat neocortical pyramidal neurones. J Physiol. 1998;507:105-116.
24. January CT, Riddle JM, Salata JJ. A model for early afterdepolarizations: induction with the Ca2+ channel agonist Bay K 8644. Circ Res. 1988; 62:563-571.
25. January CT, Riddle JM. Early afterdepolarizations: mechanism of induction and block. A role for L-type Ca2+ current. Circ Res. 1989;64:977-990.
26. Pott C, Yip M, Goldhaber JI, Philipson KD. Regulation of cardiac L-type Ca2+ current in Na +-Ca2+ exchanger knockout mice: functional coupling of the Ca2 + channel and the Na +-Ca2 + exchanger. Biophys J. 2007;92:1431-1437.
27. Gao L, Blair LA, Marshall J. CaMKII-independent effects of KN93 and its inactive analog KN92: reversible inhibition of L-type calcium channels. Biochem Biophys Res Commun. 2006;345:1606-1610.
28. Rezazadeh S, Claydon TW, Fedida D. KN-93 [(2-[N-(2-hydroxyethyl)]-N-(4- methoxybenzenesulfonyl)]amino-N-(4-chlorocinn amyl)-N-methylbenzylamine), a calcium/calmodulin-dependent protein kinase II inhibitor, is a direct extracellular blocker of voltage-gated potassium channels. J Pharmacol Exp Ther. 2006;317:292-299.
29. Choi BR, Burton F, Salama G. Cytosolic Ca2+ triggers early afterdepolarizations and Torsade de Pointes in rabbit hearts with type 2 long QT syndrome. J Physiol. 2002;543:615-631.
30. Salama G. Arrhythmia genesis: aberrations of voltage or Ca2+ cycling? Heart Rhythm. 2006;3:67-70.
31. Volders PG, Kulcsar A, Vos MA, Sipido KR, Wellens HJ, Lazzara R, Szabo B. Similarities between early and delayed afterdepolarizations induced by isoproterenol in canine ventricular myocytes. Cardiovasc Res. 1997;34:348-359.
32. Ferrier GR, Howlett SE. Cardiac excitation-contraction coupling: role of membrane potential in regulation of contraction. Am J Physiol Heart Circ Physiol. 2001;280:H1928-H1944.
33. Hobai IA, Howarth FC, Pabbathi VK, Dalton GR, Hancox JC, Zhu JQ, Howlett SE, Ferrier GR, Levi AJ. "Voltage-activated Ca release" in rabbit, rat and guinea-pig cardiac myocytes, and modulation by internal cAMP. Pflugers Arch. 1997;435:164-173.
34. Guo T, Zhang T, Mestril R, Bers DM. Ca2+/Calmodulin-dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes. Circ Res. 2006;99:398-406.
35. Curran J, Hinton MJ, Rios E, Bers DM, Shannon TR. 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.
36. Yang D, Zhu WZ, Xiao B, Brochet DX, Chen SR, Lakatta EG, Xiao RP, Cheng H. Ca2+/calmodulin kinase II-dependent phosphorylation of ryanodine receptors suppresses Ca2 + sparks and Ca2 + waves in cardiac myocytes. Circ Res. 2007;100:399-407.
37. Guo D, Zhao X, Wu Y, Liu T, Kowey PR, Yan GX. L-type calcium current reactivation contributes to arrhythmogenesis associated with action potential triangulation. J Cardiovasc Electrophysiol. 2007;18:196-203.
38. Wu Y, Kimbrough JT, Colbran RJ, Anderson ME. Calmodulin kinase is functionally targeted to the action potential plateau for regulation of L-type Ca2+ current in rabbit cardiomyocytes. J Physiol. 2004;554:145-155.
39. Priori SG, Corr PB. Mechanisms underlying early and delayed afterdepolarizations induced by catecholamines. Am J Physiol. 1990;258: H1796-H1805.
40. Song Y, Shryock JC, Belardinelli L. An increase of late sodium current induces delayed afterdepolarizations and sustained triggered activity in atrial myocytes. Am J Physiol Heart Circ Physiol. 2008;294: H2031-H2039.
41. Bers DM, Guo T. Calcium signaling in cardiac ventricular myocytes. Ann N Y Acad Sci. 2005;1047:86-98.
42. Couchonnal LF, Anderson ME. The role of calmodulin kinase II in myocardial physiology and disease. Physiology (Bethesda). 2008;23:151-159.
43. Halliwell B, Clement MV, Long LH. Hydrogen peroxide in the human body. FEBS Lett. 2000;486:10-13.
44. Dhalla NS, Duhamel TA. The paradoxes of reperfusion in the ischemic heart. Heart Metab. 2007;37:31-34.
45. Maurel A, Hernandez C, Kunduzova O, Bompart G, Cambon C, Parini A, Frances B. Age-dependent increase in hydrogen peroxide production by cardiac monoamine oxidase A in rats. Am J Physiol Heart Circ Physiol. 2003;284:H1460-H1467.
46. Maier LS, Bers DM. Role of Ca2 +/calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc Res. 2007;73:631-640.