Ca2+/calmodulin potentiates IKs in sinoatrial node cells by activating Ca2+/calmodulin-dependent protein kinase II

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 2, 2015, Pages 241-251

  Xie, Yu ^a   Ding, Wei Guang ^a   Matsuura, Hiroshi ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Calmodulin; CaMKII; Delayed rectifier K+ current; KCNQ1; Sinoatrial node cells

Indexed keywords

BENZYLAMINE DERIVATIVE; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN; CAMKII INHIBITOR AIP; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; PEPTIDE; POTASSIUM CHANNEL KCNQ1; PROTEIN KINASE INHIBITOR; SULFONAMIDE;

ACTION POTENTIAL; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; GUINEA PIG; HEART MUSCLE CELL; METABOLISM; PHYSIOLOGY; SINUS NODE;

ACTION POTENTIALS; ANIMALS; BENZYLAMINES; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALMODULIN; CELLS, CULTURED; GUINEA PIGS; KCNQ1 POTASSIUM CHANNEL; MYOCYTES, CARDIAC; PEPTIDES; PROTEIN KINASE INHIBITORS; SINOATRIAL NODE; SULFONAMIDES;

EID: 84939896314     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1507-1     Document Type: Article

References (39)

1. Aiba T, Hesketh GG, Liu T, Carlisle R, Villa-Abrille MC, O'Rourke B, Akar FG, Tomaselli GF (2010) Na+ channel regulation by Ca2+/calmodulin and Ca2+/calmodulin-dependent protein kinase II in guinea-pig ventricular myocytes. Cardiovasc Res 85(3):454–463
2. Anderson ME, Braun AP, Wu Y, Lu T, Wu Y, Schulman H, Sung RJ (1998) KN-93, an inhibitor of multifunctional Ca++/calmodulin-dependent protein kinase, decreases early after depolarizations in rabbit heart. J Pharmacol Exp Ther 287(3):996–1006
3. Anderson ME, Brown JH, Bers DM (2011) CaMKII in myocardial hypertrophy and heart failure. J Mol Cell Cardiol 51(4):468–473
4. Ashpole NM, Herren AW, Ginsburg KS, Brogan JD, Johnson DE, Cummins TR, Bers DM, Hudmon A (2012) Ca2+/calmodulin-dependent protein kinase II (CaMKII) regulates cardiac sodium channel NaV1.5 gating by multiple phosphorylation sites. J Biol Chem 287(24):19856–19869
5. Bai CX, Namekata I, Kurokawa J, Tanaka H, Shigenobu K, Furukawa T (2005) Role of nitric oxide in Ca2+ sensitivity of the slowly activating delayed rectifier K+ current in cardiac myocytes. Circ Res 96(1):64–72
6. Barhanin J, Lesage F, Guillemare E, Fink M, Lazdunski M, Romey G (1996) K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature 384(6604):78–80
7. Boucherot A, Schreiber R, Kunzelmann K (2001) Regulation and properties of KCNQ1 (K(V)LQT1) and impact of the cystic fibrosis transmembrane conductance regulator. J Membr Biol 182(1):39–47
8. Braun AP, Schulman H (1995) The multifunctional calcium/calmodulin-dependent protein kinase: from form to function. Annu Rev Physiol 57:417–445
9. DiFrancesco D, Ferroni A, Mazzanti M, Tromba C (1986) Properties of the hyperpolarizing-activated current (if) in cells isolated from the rabbit sino-atrial node. J Physiol 377:61–88
10. Ding WG, Toyoda F, Matsuura H (2002) Blocking action of chromanol 293B on the slow component of delayed rectifier K(+) current in guinea-pig sino-atrial node cells. Br J Pharmacol 137(2):253–262
11. Doerr T, Denger R, Trautwein W (1989) Calcium currents in single SA nodal cells of the rabbit heart studied with action potential clamp. Pflugers Arch 413(6):599–603
12. Fabiato A (1981) Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle. J Gen Physiol 78(5):457–497
13. Gamper N, Li Y, Shapiro MS (2005) Structural requirements for differential sensitivity of KCNQ K+ channels to modulation by Ca2+/calmodulin. Mol Biol Cell 16(8):3538–3551
14. Ghosh S, Nunziato DA, Pitt GS (2006) KCNQ1 assembly and function is blocked by long-QT syndrome mutations that disrupt interaction with calmodulin. Circ Res 98(8):1048–1054
15. Hagiwara N, Irisawa H, Kameyama M (1988) Contribution of two types of calcium currents to the pacemaker potentials of rabbit sino-atrial node cells. J Physiol 395:233–253
16. Irisawa H, Brown HF, Giles W (1993) Cardiac pacemaking in the sinoatrial node. Physiol Rev 73(1):197–227
17. Kerst G, Beschorner U, Unsold B, von Hahn T, Schreiber R, Greger R, Gerlach U, Lang HJ, Kunzelmann K, Bleich M (2001) Properties and function of KCNQ1 K+ channels isolated from the rectal gland of Squalus acanthias. Pflugers Arch 443(1):146–154
18. Lakatta EG, Maltsev VA, Vinogradova TM (2010) A coupled SYSTEM of intracellular Ca2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart's pacemaker. Circ Res 106(4):659–673
19. Lee A, Wong ST, Gallagher D, Li B, Storm DR, Scheuer T, Catterall WA (1999) Ca2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature 399(6732):155–159
20. Li L, Satoh H, Ginsburg KS, Bers DM (1997) The effect of Ca(2+)-calmodulin-dependent protein kinase II on cardiac excitation-contraction coupling in ferret ventricular myocytes. J Physiol 501(Pt 1):17–31
21. Maltsev VA, Lakatta EG (2010) A novel quantitative explanation for the autonomic modulation of cardiac pacemaker cell automaticity via a dynamic system of sarcolemmal and intracellular proteins. Am J Physiol Heart Circ Physiol 298(6):H2010–H2023
22. Matsuura H, Ehara T, Ding WG, Omatsu-Kanbe M, Isono T (2002) Rapidly and slowly activating components of delayed rectifier K(+) current in guinea-pig sino-atrial node pacemaker cells. J Physiol 540(Pt 3):815–830
23. Nitta J, Furukawa T, Marumo F, Sawanobori T, Hiraoka M (1994) Subcellular mechanism for Ca(2+)-dependent enhancement of delayed rectifier K+ current in isolated membrane patches of guinea pig ventricular myocytes. Circ Res 74(1):96–104
24. Peterson BZ, DeMaria CD, Adelman JP, Yue DT (1999) Calmodulin is the Ca2+ sensor for Ca2 + -dependent inactivation of L-type calcium channels. Neuron 22(3):549–558
25. Rigg L, Mattick PA, Heath BM, Terrar DA (2003) Modulation of the hyperpolarization-activated current (I(f)) by calcium and calmodulin in the guinea-pig sino-atrial node. Cardiovasc Res 57(2):497–504
26. Sanguinetti MC, Curran ME, Zou A, Shen J, Spector PS, Atkinson DL, Keating MT (1996) Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature 384(6604):80–83
27. Sanguinetti MC, Jiang C, Curran ME, Keating MT (1995) A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell 81(2):299–307
28. Schonherr R, Lober K, Heinemann SH (2000) Inhibition of human ether a go-go potassium channels by Ca(2+)/calmodulin. EMBO J 19(13):3263–3271
29. Shamgar L, Ma L, Schmitt N, Haitin Y, Peretz A, Wiener R, Hirsch J, Pongs O, Attali B (2006) Calmodulin is essential for cardiac IKS channel gating and assembly: impaired function in long-QT mutations. Circ Res 98(8):1055–1063
30. Tohse N (1990) Calcium-sensitive delayed rectifier potassium current in guinea pig ventricular cells. Am J Physiol 258(4 Pt 2):H1200–H1207
31. Trudeau MC, Warmke JW, Ganetzky B, Robertson GA (1995) HERG, a human inward rectifier in the voltage-gated potassium channel family. Science 269(5220):92–95
32. Vinogradova TM, Zhou YY, Bogdanov KY, Yang D, Kuschel M, Cheng H, Xiao RP (2000) Sinoatrial node pacemaker activity requires Ca(2+)/calmodulin-dependent protein kinase II activation. Circ Res 87(9):760–767
33. Wagner S, Dybkova N, Rasenack EC, Jacobshagen C, Fabritz L, Kirchhof P, Maier SK, Zhang T, Hasenfuss G, Brown JH, Bers DM, Maier LS (2006) Ca2+/calmodulin-dependent protein kinase II regulates cardiac Na+ channels. J Clin Invest 116(12):3127–3138
34. Wang Z, Wilson GF, Griffith LC (2002) Calcium/calmodulin-dependent protein kinase II phosphorylates and regulates the Drosophila eag potassium channel. J Biol Chem 277(27):24022–24029
35. Wehrens XH, Lehnart SE, Reiken SR, Marks AR (2004) Ca2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94(6):e61–e70
36. Wen H, Levitan IB (2002) Calmodulin is an auxiliary subunit of KCNQ2/3 potassium channels. J Neurosci 22(18):7991–8001
37. Yaniv Y, Spurgeon HA, Ziman BD, Lakatta EG (2013) Ca(2)+/calmodulin-dependent protein kinase II (CaMKII) activity and sinoatrial nodal pacemaker cell energetics. PLoS One 8(2):e57079
38. Yue DT, Marban E, Wier WG (1986) Relationship between force and intracellular [Ca2+] in tetanized mammalian heart muscle. J Gen Physiol 87(2):223–242
39. Yus-Najera E, Santana-Castro I, Villarroel A (2002) The identification and characterization of a noncontinuous calmodulin-binding site in noninactivating voltage-dependent KCNQ potassium channels. J Biol Chem 277(32):28545–28553