Differential modulation of Kv4.2 and Kv4.3 channels by calmodulin-dependent protein kinase II in rat cardiac myocytes

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 291, Issue 4, 2006, Pages

  Colinas, Olaia ^a   Gallego, Mónica ^b   Setién, Raúl ^b   López López, José Ramón ^a   Pérez García, M Teresa ^a,c   Casis, Oscar ^b  

^a CSIC   (Spain)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c Universidad de Valladolid and Consejo Superior de Investigaciones Científicas   (Spain)

Author keywords

Cardiac electrophysiology; Immunoprecipitation; Transient outward current

Indexed keywords

AUTOCAMTIDE 2 RELATED INHIBITORY PEPTIDE 2; CALMIDAZOLIUM; CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN DERIVATIVE; CALMODULIN INHIBITOR; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; PROTEIN KINASE; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL STRAIN HEK293; CONTROLLED STUDY; DRUG INHIBITION; ELECTROPHYSIOLOGY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ACTION POTENTIALS; ANIMALS; BENZYLAMINES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CELL LINE; ELECTROPHYSIOLOGY; GENE EXPRESSION REGULATION; HUMANS; IMIDAZOLES; MYOCYTES, CARDIAC; PEPTIDES; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; SHAL POTASSIUM CHANNELS; SULFONAMIDES; TRANSFECTION;

EID: 33749316969     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01373.2005     Document Type: Article

References (46)

1. An WF, Bowlby MR, Betty M, Cao J, Ling HP, Mendoza G, Hinson JW, Mattsson KI, Strassle BW, Trimmer JS, and Rhodes KJ. Modulation of A-type potassium channels by a family of calcium sensors. Nature 403: 553-556, 2000.
2. Anderson ME. Calmodulin kinase signaling in heart: an intriguing candidate target for therapy of myocardial dysfunction and arrhythmias. Pharmacol Ther 106: 39-55, 2005.
3. Apkon M and Nerbonne JM. Alpha 1-adrenergic agonists selectively suppress voltage-dependent K+ current in rat ventricular myocytes. Proc Natl Acad Sci USA 85: 8756-8760, 1988.
4. Bayer KU, De Koninck P, Leonard AS, Hell JW, and Schulman H. Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411: 801-805, 2001.
5. Braun AP, Fedida D, Clark RB, and Giles WR. Intracellular mechanisms for alpha 1-adrenergic regulation of the transient outward current in rabbit atrial myocytes. J Physiol 431: 689-712, 1990.
6. Caballero R, Gomez R, Moreno I, Nunez L, Gonzalez T, Arias C, Guizy M, Valenzuela C, Tamargo J, and Delpon E. Interaction of angiotensin II with the angiotensin type 2 receptor inhibits the cardiac transient outward potassium current. Cardiovasc Res 62: 86-95, 2004.
7. Casis O, Gallego M, López-López JR, and Pérez-García, MT. CamKII phosphorylates Ito and Kv4.2/Kv4.3 expressed in HEK cells (Abstract). Biophys J 84: 414a, 2004.
8. Casis O, Iriarte M, Gallego M, and Sanchez-Chapula JA. Differences in regional distribution of K+ current densities in rat ventricle. Life Sci 63: 391-400, 1998.
9. Castle NA. Differential inhibition of potassium currents in rat ventricular myocytes by capsaicin. Cardiovasc Res 26: 1137-1144, 1992.
10. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
11. Colbran RJ. Targeting of calcium/calmodulin-dependent protein kinase II. Biochem J 378: 1-16, 2004.
12. Currie S, Loughrey CM, Craig MA, and Smith GL. Calcium/calmodulin- dependent protein kinase IIdelta associates with the ryanodine receptor complex and regulates channel function in rabbit heart. Biochem J 377: 357-366, 2004.
13. Edman CF and Schulman H. Identification and characterization of delta B-CaM kinase and delta C-CaM kinase from rat heart, two new multifunctional Ca2+/calmodulin-dependent protein kinase isoforms. Biochim Biophys Acta 1221: 89-101, 1994.
14. + current via a cAMP/PKA-mediated pathway in the rat heart. Am J Physiol Cell Physiol 288: C577-C585, 2005.
15. Greenstein JL, Wu R, Po S, Tomaselli GF, and Winslow RL. Role of the calcium-independent transient outward current Ito1 in shaping action potential morphology and duration. Circ Res 87: 1026-1033, 2000.
16. Guo W, Li H, Aimond F, Johns DC, Rhodes KJ, Trimmer JS, and Nerbonne JM. Role of heteromultimers in the generation of myocardial transient outward K+ currents. Circ Res 90: 586-593, 2002.
17. Guo W, Xu H, London B, and Nerbonne JM. Molecular basis of transient outward K+ current diversity in mouse ventricular myocytes. J Physiol 521: 587-599, 1999.
18. Hagiwara K, Nunoki K, Ishii K, Abe T, and Yanagisawa T. Differential inhibition of transient outward currents of Kv1.4 and Kv43 by endothelin. Biochem Biophys Res Commun 310: 634-640, 2003.
19. Hudmon A and Schulman H. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J 364: 593-611, 2002.
20. Isenberg G and Klockner U. Calcium tolerant ventricular myocytes prepared by preincubation in a "KB medium". Pflügers Arch 395: 6-18, 1982.
21. Ishida A, Shigeri Y, Tatsu Y, Uegaki K, Kameshita I, Okuno S, Kitani T, Yumoto N, and Fujisawa H. Critical amino acid residues of AIP, a highly specific inhibitory peptide of calmodulin-dependent protein kinase II. FEBS Lett 427: 115-118, 1998.
22. Jerng HH, Qian Y, and Pfaffinger PJ. Modulation of Kv4.2 channel expression and gating by dipeptidyl peptidase 10 (DPP10). Biophys J 87: 2380-2396, 2004.
23. Ledoux J, Chartier D, and Leblanc N. Inhibitors of calmodulin-dependent protein kinase are nonspecific blockers of voltage-dependent K+ Channels in vascular myocytes. J Pharmacol Exp Ther 290: 1165-1174, 1999.
24. Maier LS and Bers DM. Calcium, calmodulin, and calcium-calmodulin kinase II: heartbeat to heartbeat and beyond. J Mol Cell Cardiol 34: 919-939, 2002.
25. Michel JJC and Scott JD. AKAP mediated signal transduction. Annu Rev Pharmacol Toxicol 42: 235-257, 2002.
26. Nerbonne JM and Kass RS. Molecular physiology of cardiac repolarization. Physiol Rev 85: 1205-1253, 2005.
27. Oudit GY, Kassiri Z, Sah R, Ramirez RJ, Zobel C, and Backx PH. The molecular physiology of the cardiac transient outward potassium current (I(to)) in normal and diseased myocardium. J Mol Cell Cardiol 33: 851-872, 2001.
28. Pandit SV, Clark RB, Giles WR, and Demir SS. A mathematical model of action potential heterogeneity in adult rat left ventricular myocytes. Biophys J 81: 3029-3051, 2001.
29. Patel SP and Campbell DL. Transient outward potassium current, "Ito", phenotypes in the mammalian left ventricle: underlying molecular, cellular and biophysical mechanisms. J Physiol 569: 7-39, 2005.
30. Puglisi JL and Bers DM. LabHEART: an interactive computer model of rabbit ventricular myocyte ion channels and Ca transport. Am J Physiol Cell Physiol 281: C2049-C2060, 2001.
31. Rezazadeh S, Claydon TW, and Fedida D. KN-93, a calcium/calmodulin- dependent protein kinase II inhibitor, is a direct extracellular blocker of voltage-gated potassium channels. J Pharmacol Exp Ther 2005.
32. Roeper J, Lorra C, and Pongs O. Frequency-dependent inactivation of mammalian A-type K+ channel KV1.4 regulated by Ca2+/calmodulin-dependent protein kinase. J Neurosci 17: 3379-3391, 1997.
33. Sah R, Ramirez RJ, Oudit GY, Gidrewicz D, Trivieri MG, Zobel C, and Backx PH. Regulation of cardiac excitation-contraction coupling by action potential repolarization: role of the transient outward potassium current (I(to)). J Physiol 546: 5-18, 2003.
34. Sanchez D, Lopez-Lopez JR, Perez-Garcia MT, Sanz-Alfayate G, Obeso A, Ganfornina MD, and Gonzalez C. Molecular identification of Kvalpha subunits that contribute to the oxygen-sensitive K+ current of chemoreceptor cells of the rabbit carotid body. J Physiol 542: 369-382, 2002.
35. Schoenmakers JM, Visser GJ, Flik G, and Theuvenet APR. CHELATOR: An improved method for computing metal ion concentrations in physiological solutions. Biotechniques 12: 870-879, 1992.
36. 2+/calmodulin-dependent protein kinase II. Am J Physiol Cell Physiol 288: C304-C313, 2005.
37. Sumi M, Kiuchi K, Ishikawa T, Ishii A, Hagiwara M, Nagatsu T, and Hidaka H. The newly synthesized selective Ca2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem Biophys Res Commun 181: 968-975, 1991.
38. Sun XX, Hodge JJ, Zhou Y, Nguyen M, and Griffith LC. The eag potassium channel binds and locally activates calcium/calmodulin-dependent protein kinase II. J Biol Chem 279: 10206-10214, 2004.
39. Tessier S, Karczewski P, Krause EG, Pansard Y, Acar C, Lang-Lazdunski M, Mercadier JJ, and Hatem SN. Regulation of the transient outward K(+) current by Ca(2+)/calmodulin-dependent protein kinases II in human atrial myocytes. Circ Res 85: 810-819, 1999.
40. Varga AW, Yuan LL, Anderson AE, Schrader LA, Wu GY, Gatchel JR, Johnston D, and Sweatt JD. Calcium-calmodulin-dependent kinase II modulates Kv4.2 channel expression and upregulates neuronal A-type potassium currents. J Neurosci 24: 3643-3654, 2004.
41. Wang S, Bondarenko VE, Qu Yj Bett GCL, Morales MJ, Rasmusson RL, and Strauss HC. Time- and voltage-dependent components of Kv4.3 inactivation. Biophys J 89: 3026-3041, 2005.
42. + current in rat ventricle. Am J Physiol Heart Circ Physiol 276: H1599-H1607, 1999.
43. Wu Y, Colbran RJ, and Anderson ME. Calmodulin kinase is a molecular switch for cardiac excitation-contraction coupling. Proc Natl Acad Sci USA 98: 2877-2881, 2001.
44. Xu H, Guo W, and Nerbonne JM. Four kinetically distinct depolarization-activated K+ currents in adult mouse ventricular myocytes. J Gen Physiol 113: 661-678, 1999.
45. YuanWand Bers DM. Ca-dependent facilitation of cardiac Ca current is due to Ca-calmodulin-dependent protein kinase. Am J Physiol Heart Circ Physiol 267: H982-H993, 1994.
46. Zhang T and Brown JH. Role of Ca2+/calmodulin-dependent protein kinase II in cardiac hypertrophy and heart failure. Cardiovasc Res 63: 476-486, 2004.