Altered Repolarization Reserve in Failing Rabbit Ventricular Myocytes: Calcium and β-Adrenergic Effects on Delayed- and Inward-Rectifier Potassium Currents

Circulation: Arrhythmia and Electrophysiology

Volumn 11, Issue 2, 2018, Pages

  Hegyi, Bence ^a   Bossuyt, Julie ^a   Ginsburg, Kenneth S ^a   Mendoza, Lynette M ^c   Talken, Linda ^a   Ferrier, William T ^b   Pogwizd, Steven M ^d   Izu, Leighton T ^b   Chen Izu, Ye ^a,b   Bers, Donald M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b School of Medicine   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

action potential; calcium calmodulin dependent protein kinase II; electrophysiology; heart failure; potassium channels

Indexed keywords

BETA ADRENERGIC RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOPRENALINE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CALCIUM; POTASSIUM;

ACTION POTENTIAL DURATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTIC STENOSIS; ARRHYTHMOGENESIS; ARTICLE; CARDIAC MUSCLE CELL; CONTROLLED STUDY; CURRENT CLAMP TECHNIQUE; ECHOCARDIOGRAPHY; ELECTROPHYSIOLOGY; HEART ARRHYTHMIA; HEART FAILURE; HEART RATE; HEART REPOLARIZATION; LUNG EDEMA; MALE; MEMBRANE STEADY POTENTIAL; NEW ZEALAND WHITE (RABBIT); NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; TEMPERATURE; UPREGULATION; ACTION POTENTIAL; ANIMAL; DISEASE MODEL; DRUG EFFECT; HEART VENTRICLE; LEPORIDAE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ADRENERGIC BETA-AGONISTS; ANIMALS; CALCIUM; DISEASE MODELS, ANIMAL; HEART FAILURE; HEART VENTRICLES; MALE; MYOCYTES, CARDIAC; POTASSIUM; RABBITS;

EID: 85044534177     PISSN: 19413149     EISSN: 19413084     Source Type: Journal    
DOI: 10.1161/CIRCEP.117.005852     Document Type: Article

References (60)

1. Tomaselli GF, Beuckelmann DJ, Calkins HG, Berger RD, Kessler PD, Lawrence JH, Kass D, Feldman AM, Marban E, Sudden cardiac death in heart failure. The role of abnormal repolarization. Circulation 1994 90 2534 2539
2. Watanabe E, Arakawa T, Uchiyama T, Tong M, Yasui K, Takeuchi H, Terasawa T, Kodama I, Hishida H, Prognostic significance of circadian variability of RR and QT intervals and QT dynamicity in patients with chronic heart failure. Heart Rhythm 2007 4 999 1005. doi: 10.1016/j.hrthm.2007.04.019.
3. Arsenos P, Gatzoulis KA, Dilaveris P, Gialernios T, Sideris S, Lazaros G, Archontakis S, Tsiachris D, Kartsagoulis E, Stefanadis C, The rate-corrected QT interval calculated from 24-hour Holter recordings may serve as a significant arrhythmia risk stratifier in heart failure patients. Int J Cardiol 2011 147 321 323. doi: 10.1016/j.ijcard.2010.12.076.
4. Algra A, Tijssen JG, Roelandt JR, Pool J, Lubsen J, QTc prolongation measured by standard 12-lead electrocardiography is an independent risk factor for sudden death due to cardiac arrest. Circulation 1991 83 1888 1894
5. Piccirillo G, Magrì D, Matera S, Magnanti M, Torrini A, Pasquazzi E, Schifano E, Velitti S, Marigliano V, Quaglione R, Barillà F, QT variability strongly predicts sudden cardiac death in asymptomatic subjects with mild or moderate left ventricular systolic dysfunction: a prospective study. Eur Heart J 2007 28 1344 1350. doi: 10.1093/eurheartj/ehl367.
6. Vrtovec B, Knezevic I, Poglajen G, Sebestjen M, Okrajsek R, Haddad F, Relation of B-type natriuretic peptide level in heart failure to sudden cardiac death in patients with and without QT interval prolongation. Am J Cardiol 2013 111 886 890. doi: 10.1016/j.amjcard.2012.11.041.
7. Beuckelmann DJ, Näbauer M, Erdmann E, Alterations of K+ currents in isolated human ventricular myocytes from patients with terminal heart failure. Circ Res 1993 73 379 385
8. Li GR, Lau CP, Leung TK, Nattel S, Ionic current abnormalities associated with prolonged action potentials in cardiomyocytes from diseased human right ventricles. Heart Rhythm 2004 1 460 468. doi: 10.1016/j.hrthm.2004.06.003.
9. Kääb S, Nuss HB, Chiamvimonvat N, O'Rourke B, Pak PH, Kass DA, Marban E, Tomaselli GF, Ionic mechanism of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circ Res 1996 78 262 273
10. Tsuji Y, Zicha S, Qi XY, Kodama I, Nattel S, Potassium channel subunit remodeling in rabbits exposed to long-term bradycardia or tachycardia: discrete arrhythmogenic consequences related to differential delayed-rectifier changes. Circulation 2006 113 345 355. doi: 10.1161/CIRCULATIONAHA.105.552968.
11. Pogwizd SM, Schlotthauer K, Li L, Yuan W, Bers DM, Arrhythmogenesis and contractile dysfunction in heart failure: roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circ Res 2001 88 1159 1167
12. Rose J, Armoundas AA, Tian Y, DiSilvestre D, Burysek M, Halperin V, O'Rourke B, Kass DA, Marbán E, Tomaselli GF, Molecular correlates of altered expression of potassium currents in failing rabbit myocardium. Am J Physiol Heart Circ Physiol 2005 288 H2077 H2087. doi: 10.1152/ajpheart.00526.2003.
13. Li GR, Lau CP, Ducharme A, Tardif JC, Nattel S, Transmural action potential and ionic current remodeling in ventricles of failing canine hearts. Am J Physiol Heart Circ Physiol 2002 283 H1031 H1041. doi: 10.1152/ajpheart.00105.2002.
14. Rozanski GJ, Xu Z, Whitney RT, Murakami H, Zucker IH, Electrophysiology of rabbit ventricular myocytes following sustained rapid ventricular pacing. J Mol Cell Cardiol 1997 29 721 732. doi: 10.1006/jmcc.1996.0314.
15. Davey PP, Barlow C, Hart G, Prolongation of the QT interval in heart failure occurs at low but not at high heart rates. Clin Sci (Lond) 2000 98 603 610
16. 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. doi: 10.1016/j.yjmcc.2004.12.012.
17. Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM, Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 2005 97 1314 1322. doi: 10.1161/01.RES.0000194329.41863.89.
18. 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. doi: 10.1172/JCI26620.
19. 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. doi: 10.1161/CIRCEP.108.842799.
20. Anderson ME, Brown JH, Bers DM, CaMKII in myocardial hypertrophy and heart failure. J Mol Cell Cardiol 2011 51 468 473. doi: 10.1016/j.yjmcc.2011.01.012.
21. Hoeker GS, Hanafy MA, Oster RA, Bers DM, Pogwizd SM, Reduced arrhythmia inducibility with calcium/calmodulin-dependent protein kinase II inhibition in heart failure rabbits. J Cardiovasc Pharmacol 2016 67 260 265. doi: 10.1097/FJC.0000000000000343.
22. Pogwizd SM, Qi M, Yuan W, Samarel AM, Bers DM, Upregulation of Na(+)/Ca(2+) exchanger expression and function in an arrhythmogenic rabbit model of heart failure. Circ Res 1999 85 1009 1019
23. Despa S, Islam MA, Weber CR, Pogwizd SM, Bers DM, Intracellular Na(+) concentration is elevated in heart failure but Na/K pump function is unchanged. Circulation 2002 105 2543 2548
24. 2+ leak in normal and failing rabbit ventricular myocytes. J Physiol 2010 588 p t 23 4743 4757. doi: 10.1113/jphysiol.2010.197913.
25. Uchinoumi H, Yang Y, Oda T, Li N, Alsina KM, Puglisi JL, Chen-Izu Y, Cornea RL, Wehrens XHT, Bers DM, CaMKII-dependent phosphorylation of RyR2 promotes targetable pathological RyR2 conformational shift. J Mol Cell Cardiol 2016 98 62 72. doi: 10.1016/j.yjmcc.2016.06.007.
26. Banyasz T, Horvath B, Jian Z, Izu LT, Chen-Izu Y, Sequential dissection of multiple ionic currents in single cardiac myocytes under action potential-clamp. J Mol Cell Cardiol 2011 50 578 581. doi: 10.1016/j.yjmcc.2010.12.020.
27. Banyasz T, Jian Z, Horvath B, Khabbaz S, Izu LT, Chen-Izu Y, Beta-adrenergic stimulation reverses the I Kr-I Ks dominant pattern during cardiac action potential. Pflugers Arch 2014 466 2067 2076. doi: 10.1007/s00424-014-1465-7.
28. Nichols CB, Chang CW, Ferrero M, Wood BM, Stein ML, Ferguson AJ, Ha D, Rigor RR, Bossuyt S, Bossuyt J, β-adrenergic signaling inhibits Gq-dependent protein kinase D activation by preventing protein kinase D translocation. Circ Res 2014 114 1398 1409. doi: 10.1161/CIRCRESAHA.114.303870.
29. Banyasz T, Horvath B, Jian Z, Izu LT, Chen-Izu Y, Profile of L-type Ca(2+) current and Na(+)/Ca(2+) exchange current during cardiac action potential in ventricular myocytes. Heart Rhythm 2012 9 134 142. doi: 10.1016/j.hrthm.2011.08.029.
30. Johnson DM, Heijman J, Bode EF, Greensmith DJ, van der Linde H, Abi-Gerges N, Eisner DA, Trafford AW, Volders PG, Diastolic spontaneous calcium release from the sarcoplasmic reticulum increases beat-to-beat variability of repolarization in canine ventricular myocytes after β-adrenergic stimulation. Circ Res 2013 112 246 256. doi: 10.1161/CIRCRESAHA.112.275735.
31. Szentandrássy N, Kistamás K, Hegyi B, Horváth B, Ruzsnavszky F, Váczi K, Magyar J, Bányász T, Varró A, Nánási PP, Contribution of ion currents to beat-to-beat variability of action potential duration in canine ventricular myocytes. Pflugers Arch 2015 467 1431 1443. doi: 10.1007/s00424-014-1581-4.
32. Bassani RA, Altamirano J, Puglisi JL, Bers DM, Action potential duration determines sarcoplasmic reticulum Ca2+ reloading in mammalian ventricular myocytes. J Physiol 2004 559 p t 2 593 609. doi: 10.1113/jphysiol.2004.067959.
33. Shannon TR, Pogwizd SM, Bers DM, Elevated sarcoplasmic reticulum Ca2+ leak in intact ventricular myocytes from rabbits in heart failure. Circ Res 2003 93 592 594. doi: 10.1161/01.RES.0000093399.11734.B3.
34. Curran J, Brown KH, Santiago DJ, Pogwizd S, Bers DM, Shannon TR, Spontaneous Ca waves in ventricular myocytes from failing hearts depend on Ca(2+)-calmodulin-dependent protein kinase II. J Mol Cell Cardiol 2010 49 25 32. doi: 10.1016/j.yjmcc.2010.03.013.
35. Lengyel C, Iost N, Virág L, Varró A, Lathrop DA, Papp JG, Pharmacological block of the slow component of the outward delayed rectifier current (I(Ks)) fails to lengthen rabbit ventricular muscle QT© and action potential duration. Br J Pharmacol 2001 132 101 110. doi: 10.1038/sj.bjp.0703777.
36. Zaza A, Rocchetti M, Brioschi A, Cantadori A, Ferroni A, Dynamic Ca2+-induced inward rectification of K+ current during the ventricular action potential. Circ Res 1998 82 947 956
37. Straus SM, Kors JA, De Bruin ML, van der Hooft CS, Hofman A, Heeringa J, Deckers JW, Kingma JH, Sturkenboom MC, Stricker BH, Witteman JC, Prolonged QTc interval and risk of sudden cardiac death in a population of older adults. J Am Coll Cardiol 2006 47 362 367. doi: 10.1016/j.jacc.2005.08.067.
38. Barr CS, Naas A, Freeman M, Lang CC, Struthers AD, QT dispersion and sudden unexpected death in chronic heart failure. Lancet 1994 343 327 329
39. Grimm M, Ling H, Willeford A, Pereira L, Gray CB, Erickson JR, Sarma S, Respress JL, Wehrens XH, Bers DM, Brown JH, CaMKIIδ mediates β-adrenergic effects on RyR2 phosphorylation and SR Ca(2+) leak and the pathophysiological response to chronic β-adrenergic stimulation. J Mol Cell Cardiol 2015 85 282 291. doi: 10.1016/j.yjmcc.2015.06.007.
40. Kääb S, Dixon J, Duc J, Ashen D, Näbauer M, Beuckelmann DJ, Steinbeck G, McKinnon D, Tomaselli GF, Molecular basis of transient outward potassium current downregulation in human heart failure: a decrease in Kv4.3 mRNA correlates with a reduction in current density. Circulation 1998 98 1383 1393
41. +] i-induced augmentation of the inward rectifier potassium current (IK1) in canine and human ventricular myocardium. Pflugers Arch 2013 465 1621 1635. doi: 10.1007/s00424-013-1309-x.
42. Tohse N, Calcium-sensitive delayed rectifier potassium current in guinea pig ventricular cells. Am J Physiol 1990 258 4 p t 2 H1200 H1207. doi: 10.1152/ajpheart.1990.258.4.H1200.
43. Xie Y, Ding WG, Matsuura H, Ca2+/calmodulin potentiates I Ks in sinoatrial node cells by activating Ca2+/calmodulin-dependent protein kinase II. Pflugers Arch 2015 467 241 251. doi: 10.1007/s00424-014-1507-1.
44. Bartos DC, Morotti S, Ginsburg KS, Grandi E, Bers DM, Quantitative analysis of the Ca2+ -dependent regulation of delayed rectifier K+ current IKs in rabbit ventricular myocytes. J Physiol 2017 595 2253 2268. doi: 10.1113/JP273676.
45. Nitta J, Furukawa T, Marumo F, Sawanobori T, Hiraoka M, Subcellular mechanism for Ca(2+)-dependent enhancement of delayed rectifier K+ current in isolated membrane patches of guinea pig ventricular myocytes. Circ Res 1994 74 96 104
46. Ghosh S, Nunziato DA, Pitt GS, KCNQ1 assembly and function is blocked by long-QT syndrome mutations that disrupt interaction with calmodulin. Circ Res 2006 98 1048 1054. doi: 10.1161/01.RES.0000218863.44140.f2.
47. Heath BM, Terrar DA, Protein kinase C enhances the rapidly activating delayed rectifier potassium current, IKr, through a reduction in C-type inactivation in guinea-pig ventricular myocytes. J Physiol 2000 522 pt 3 391 402
48. Bowling N, Walsh RA, Song G, Estridge T, Sandusky GE, Fouts RL, Mintze K, Pickard T, Roden R, Bristow MR, Sabbah HN, Mizrahi JL, Gromo G, King GL, Vlahos CJ, Increased protein kinase C activity and expression of Ca2+-sensitive isoforms in the failing human heart. Circulation 1999 99 384 391
49. Braz JC, Gregory K, Pathak A, Zhao W, Sahin B, Klevitsky R, Kimball TF, Lorenz JN, Nairn AC, Liggett SB, Bodi I, Wang S, Schwartz A, Lakatta EG, DePaoli-Roach AA, Robbins J, Hewett TE, Bibb JA, Westfall MV, Kranias EG, Molkentin JD, PKC-alpha regulates cardiac contractility and propensity toward heart failure. Nat Med 2004 10 248 254. doi: 10.1038/nm1000.
50. Cockerill SL, Tobin AB, Torrecilla I, Willars GB, Standen NB, Mitcheson JS, Modulation of hERG potassium currents in HEK-293 cells by protein kinase C. Evidence for direct phosphorylation of pore forming subunits. J Physiol 2007 581 p t 2 479 493. doi: 10.1113/jphysiol.2006.123414.
51. Holzem KM, Gomez JF, Glukhov AV, Madden EJ, Koppel AC, Ewald GA, Trenor B, Efimov IR, Reduced response to IKr blockade and altered hERG1a/1b stoichiometry in human heart failure. J Mol Cell Cardiol 2016 96 82 92. doi: 10.1016/j.yjmcc.2015.06.008.
52. Shu L, Zhang W, Su G, Zhang J, Liu C, Xu J, Modulation of HERG K+ channels by chronic exposure to activators and inhibitors of PKA and PKC: actions independent of PKA and PKC phosphorylation. Cell Physiol Biochem 2013 32 1830 1844. doi: 10.1159/000356616.
53. + currents to isoprenaline-induced changes in canine ventricular cells. Br J Pharmacol 2012 167 599 611. doi: 10.1111/j.1476-5381.2012.02015.x.
54. Desantiago J, Ai X, Islam M, Acuna G, Ziolo MT, Bers DM, Pogwizd SM, Arrhythmogenic effects of beta2-adrenergic stimulation in the failing heart are attributable to enhanced sarcoplasmic reticulum Ca load. Circ Res 2008 102 1389 1397. doi: 10.1161/CIRCRESAHA.107.169011.
55. Barbagallo F, Xu B, Reddy GR, West T, Wang Q, Fu Q, Li M, Shi Q, Ginsburg KS, Ferrier W, Isidori AM, Naro F, Patel HH, Bossuyt J, Bers D, Xiang YK, Genetically encoded biosensors reveal PKA hyperphosphorylation on the myofilaments in rabbit heart failure. Circ Res 2016 119 931 943. doi: 10.1161/CIRCRESAHA.116.308964.
56. Bányász T, Magyar J, Szentandrássy N, Horváth B, Birinyi P, Szentmiklósi J, Nánási PP, Action potential clamp fingerprints of K+ currents in canine cardiomyocytes: their role in ventricular repolarization. Acta Physiol (Oxf) 2007 190 189 198. doi: 10.1111/j.1748-1716.2007.01674.x.
57. Jost N, Virág L, Bitay M, Takács J, Lengyel C, Biliczki P, Nagy Z, Bogáts G, Lathrop DA, Papp JG, Varró A, Restricting excessive cardiac action potential and QT prolongation: a vital role for IKs in human ventricular muscle. Circulation 2005 112 1392 1399. doi: 10.1161/CIRCULATIONAHA.105.550111.
58. Jurkiewicz NK, Sanguinetti MC, Rate-dependent prolongation of cardiac action potentials by a methanesulfonanilide class III antiarrhythmic agent. Specific block of rapidly activating delayed rectifier K+ current by dofetilide. Circ Res 1993 72 75 83
59. Fox K, Ford I, Steg PG, Tendera M, Ferrari R, BEAUTIFUL Investigators Ivabradine for patients with stable coronary artery disease and left-ventricular systolic dysfunction (BEAUTIFUL): a randomised, double-blind, placebo-controlled trial. Lancet 2008 372 807 816. doi: 10.1016/S0140-6736(08)61170-8.
60. Swedberg K, Komajda M, Böhm M, Borer JS, Ford I, Dubost-Brama A, Lerebours G, Tavazzi L, SHIFT Investigators Ivabradine and outcomes in chronic heart failure (SHIFT): a randomised placebo-controlled study. Lancet 2010 376 875 885. doi: 10.1016/S0140-6736(10)61198-1.