Calcium-activated potassium current modulates ventricular repolarization in chronic heart failure

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Bonilla, Ingrid M ^a,b   Long, Victor P ^a,b   Vargas Pinto, Pedro ^c,e   Wright, Patrick ^b   Belevych, Andriy ^b   Lou, Qing ^b   Mowrey, Kent ^d   Yoo, Jae ^a   Binkley, Philip F ^b   Fedorov, Vadim V ^b   Györke, Sandor ^b   Janssen, Paulus M L ^b   Kilic, Ahmet ^b   Mohler, Peter J ^b   Carnes, Cynthia A ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d ST JUDE MEDICAL   (United States)

^e UNIVERSIDAD DE LA SALLE   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL 1; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL 3; UNCLASSIFIED DRUG; CALCIUM; POTASSIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOG; FEMALE; HEART ARRHYTHMIA; HEART ATRIUM FIBRILLATION; HEART DEPOLARIZATION; HEART DILATATION; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE POTENTIAL; HEART REPOLARIZATION; HUMAN; HUMAN TISSUE; MALE; NONHUMAN; POTASSIUM CURRENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; ACTION POTENTIAL; ANIMAL; ATRIAL FIBRILLATION; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; DISEASE MODEL; HEART; HEART VENTRICLE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; ATRIAL FIBRILLATION; CALCIUM; DISEASE MODELS, ANIMAL; DOGS; HEART; HEART FAILURE; HEART VENTRICLES; HUMANS; MYOCARDIUM; MYOCYTES, CARDIAC; POTASSIUM;

EID: 84907542577     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108824     Document Type: Article

References (47)

1. Kannel WB, Wolf PA, Benjamin EJ, Levy D (1998) Prevalence, incidence, prognosis, and predisposing conditions for atrial fibrillation: population-based estimates. Am J Cardiol 82:2N-9N.
2. Wang TJ, Larson MG, Levy D, Vasan RS, Leip EP, et al. (2003) Temporal relations of atrial fibrillation and congestive heart failure and their joint influence on mortality: the Framingham Heart Study. Circulation 107:2920-2925. doi: 10.1161/01. CIR.0000072767.89944.6E.
3. Xu Y, Tuteja D, Zhang Z, Xu D, Zhang Y, et al. (2003) Molecular identification and functional roles of a Ca (2+)-activated K+ channel in human and mouse hearts. J Biol Chem 278:49085-49094. doi: 10.1074/jbc. M307508200.
4. Vergara C, Latorre R, Marrion NV, Adelman JP (1998) Calcium-activated potassium channels. Curr Opin Neurobiol 8:321-329. doi: 10.1016/S0959-4388 (98) 80056-1.
5. Ro S, Hatton WJ, Koh SD, Horowitz B (2001) Molecular properties of smallconductance Ca2+-activated K+ channels expressed in murine colonic smooth muscle. Am J Physiol Gastrointest Liver Physiol 281:G964-G973.
6. Tuteja D, Xu D, Timofeyev V, Lu L, Sharma D, et al. (2005) Differential expression of small-conductance Ca2+-activated K+ channels SK1, SK2, and SK3 in mouse atrial and ventricular myocytes. Am J Physiol Heart Circ Physiol 289:H2714-H2723. doi: 10.1152/ajpheart.00534.2005.
7. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, et al. (1998) Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395:503-507. doi: 10.1038/26758.
8. Wei AD, Gutman GA, Aldrich R, Chandy KG, Grissmer S, et al. (2005) International Union of Pharmacology. LII. Nomenclature and molecular relationships of calcium-activated potassium channels. Pharmacol Rev 57:463-472. doi: 10.1124/pr.57.4.9.
9. Grunnet M, Jensen BS, Olesen SP, Klaerke DA (2001) Apamin interacts with all subtypes of cloned small-conductance Ca2+-activated K+ channels. Pflugers Arch 441:544-550.
10. Yu CC, Ai T, Weiss JN, Chen PS (2014) Apamin does not inhibit human cardiac Na+ current, L-type Ca2+ current or other major K+ currents. PLoS One 9:e96691. doi: 10.1371/journal.pone.0096691 [doi];PONE-D-14-01991 [pii].
11. Li N, Timofeyev V, Tuteja D, Xu D, Lu L, et al. (2009) Ablation of a Ca2+-activated K+ channel (SK2 channel) results in action potential prolongation in atrial myocytes and atrial fibrillation. J Physiol 587:1087-1100. doi: 10.1113/jphysiol.2008.167718.
12. Gui L, Bao Z, Jia Y, Qin X, Cheng ZJ, et al. (2013) Ventricular tachyarrhythmias in rats with acute myocardial infarction involves activation of small-conductance Ca2+-activated K+ channels. Am J Physiol Heart Circ Physiol 304:H118-H130. doi: 10.1152/ajpheart.00820.2011.
13. Chua SK, Chang PC, Maruyama M, Turker I, Shinohara T, et al. (2011) Smallconductance calcium-activated potassium channel and recurrent ventricular fibrillation in failing rabbit ventricles. Circ Res 108:971-979. doi: 10.1161/CIRCRESAHA.110.238386.
14. Chang PC, Turker I, Lopshire JC, Masroor S, Nguyen BL, et al. (2013) Heterogeneous upregulation of apamin-sensitive potassium currents in failing human ventricles. J Am Heart Assoc 2:e004713. doi: 10.1161/JAHA.112.004713.
15. Qi XY, Diness JG, Brundel B, Zhou XB, Naud P, et al. (2013) Role of Small Conductance Calcium-Activated Potassium Channels in Atrial Electrophysiology and Fibrillation in the Dog. Circulation 430-440. doi: 10.1161/CIRCULATIONAHA.113.003019.
16. Hsueh CH, Chang PC, Hsieh YC, Reher T, Chen PS, et al. (2013) Proarrhythmic effect of blocking the small conductance calcium activated potassium channel in isolated canine left atrium. Heart Rhythm 10:891-898. doi: 10.1016/j.hrthm.2013.01.033.
17. Nishijima Y, Feldman DS, Bonagura JD, Ozkanlar Y, Jenkins PJ, et al. (2005) Canine nonischemic left ventricular dysfunction: a model of chronic human cardiomyopathy. J Card Fail 11:638-644. doi: 10.1016/j.cardfail.2005.05.006.
18. Terentyev D, Gyorke I, Belevych AE, Terentyeva R, Sridhar A, et al. (2008) Redox modification of ryanodine receptors contributes to sarcoplasmic reticulum Ca2+ leak in chronic heart failure. Circ Res 103:1466-1472. doi: 10.1161/CIRCRESAHA.108.184457.
19. Nishijima Y, Feldman DS, Bonagura JD, Ozkanlar Y, Jenkins PJ, et al. (2005) Canine nonischemic left ventricular dysfunction: a model of chronic human cardiomyopathy. J Card Fail 11:638-644.
20. Sridhar A, Nishijima Y, Terentyev D, Khan M, Terentyeva R, et al. (2009) Chronic heart failure and the substrate for atrial fibrillation. Cardiovasc Res 84:227-236. doi: 10.1093/cvr/cvp216.
21. Nishijima Y, Sridhar A, Viatchenko-Karpinski S, Shaw C, Bonagura JD, et al. (2007) Chronic cardiac resynchronization therapy and reverse ventricular remodeling in a model of nonischemic cardiomyopathy. Life Sci 81:1152-1159. doi: 10.1016/j.lfs.2007.08.022.
22. Bonilla IM, Sridhar A, Nishijima Y, Gyorke S, Cardounel AJ, et al. (2013) Differential effects of the peroxynitrite donor, SIN-1, on atrial and ventricular myocyte electrophysiology. J Cardiovasc Pharmacol 61:401-407. doi: 10.1097/FJC.0b013e31828748ca.
23. Bonilla IM, Sridhar A, Gyorke S, Cardounel AJ, Carnes CA (2012) Nitric oxide synthases and atrial fibrillation. Front Physiol 3:105. doi: 10.3389/fphys.2012.00105.
24. Thomsen MB, Volders PG, Beekman JD, Matz J, Vos MA (2006) Beat-to-Beat variability of repolarization determines proarrhythmic outcome in dogs susceptible to drug-induced torsades de pointes. J Am Coll Cardiol 48:1268-1276. doi: 10.1016/j.jacc.2006.05.048.
25. Bonilla IM, Vargas-Pinto P, Nishijima Y, Pedraza-Toscano A, Ho HT, et al. (2013) Ibandronate and Ventricular Arrhythmia Risk. J Cardiovasc Electrophysiol. doi: 10.1111/jce.12327.
26. Weatherall KL, Seutin V, Liegeois JF, Marrion NV (2011) Crucial role of a shared extracellular loop in apamin sensitivity and maintenance of pore shape of small-conductance calcium-activated potassium (SK) channels. Proc Natl Acad Sci U S A 108:18494-18499. doi: 10.1073/pnas.1110724108.
27. Weatherall KL, Goodchild SJ, Jane DE, Marrion NV (2010) Small conductance calcium-activated potassium channels: from structure to function. Prog Neurobiol 91:242-255. doi: 10.1016/j.pneurobio.2010.03.002.
28. Grunnet M, Jespersen T, Angelo K, Frokjaer-Jensen C, Klaerke DA, et al. (2001) Pharmacological modulation of SK3 channels. Neuropharmacology 40:879-887. doi: 10.1016/S0028-3908 (01) 00028-4.
29. Thomsen MB, Oros A, Schoenmakers M, van Opstal JM, Maas JN, et al. (2007) Proarrhythmic electrical remodelling is associated with increased beat-to-beat variability of repolarisation. Cardiovasc Res 73:521-530. doi: 10.1016/j.cardiores.2006.11.025.
30. Bildl W, Strassmaier T, Thurm H, Andersen J, Eble S, et al. (2004) Protein kinase CK2 is coassembled with small conductance Ca (2+)-activated K+ channels and regulates channel gating. Neuron 43:847-858. doi: 10.1016/j.neuron. 2004.08.033.
31. Belevych AE, Terentyev D, Terentyeva R, Nishijima Y, Sridhar A, et al. (2011) The relationship between arrhythmogenesis and impaired contractility in heart failure: role of altered ryanodine receptor function. Cardiovasc Res 90:493-502. doi: 10.1093/cvr/cvr025.
32. Terentyev D, Rochira JA, Terentyeva R, Roder K, Koren G, et al. (2013) Sarcoplasmic reticulum Ca2+ release is both necessary and sufficient for SK channel activation in ventricular myocytes. Am J Physiol Heart Circ Physiol In Press. doi: 10.1152/ajpheart.00621.2013.
33. Roden DM (1998) Taking the "idio" out of "idiosyncratic": predicting torsades de pointes. Pacing Clin Electrophysiol 21:1029-1034.
34. Winslow RL, Rice J, Jafri S, Marban E, O'Rourke B (1999) Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, II: model studies. Circ Res 84:571-586. doi: 10.1161/01. RES.84.5.571.
35. Kaab S, Nuss HB, Chiamvimonvat N, O'Rourke B, Pak PH, et al. (1996) Ionic mechanism of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circ Res 78:262-273. doi: 10.1161/01. RES.78.2.262.
36. Nattel S (2009) Calcium-activated potassium current: a novel ion channel candidate in atrial fibrillation. J Physiol 587:1385-1386. doi: 10.1113/jphysiol.2009.170621.
37. Workman AJ, Pau D, Redpath CJ, Marshall GE, Russell JA, et al. (2009) Atrial cellular electrophysiological changes in patients with ventricular dysfunction may predispose to AF. Heart Rhythm 6:445-451. doi: 10.1016/j.hrthm.2008.12.028.
38. Schreieck J, Wang Y, Overbeck M, Schomig A, Schmitt C (2000) Altered transient outward current in human atrial myocytes of patients with reduced left ventricular function. J Cardiovasc Electrophysiol 11:180-192.
39. Glukhov AV, Fedorov VV, Kalish PW, Ravikumar VK, Lou Q, et al. (2012) Conduction remodeling in human end-stage nonischemic left ventricular cardiomyopathy. Circulation 125:1835-1847. doi: 10.1161/CIRCULATIO-NAHA.111.047274.
40. Chang SH, Chang SN, Hwang JJ, Chiang FT, Tseng CD, et al. (2012) Significant association of rs13376333 in KCNN3 on chromosome 1q21 with atrial fibrillation in a Taiwanese population. Circ J 76:184-188. doi: 10.1253/circj. CJ-11-0525.
41. Ellinor PT, Lunetta KL, Glazer NL, Pfeufer A, Alonso A, et al. (2010) Common variants in KCNN3 are associated with lone atrial fibrillation. Nat Genet 42:240-244. doi: 10.1038/ng.537.
42. Yu T, Deng C, Wu R, Guo H, Zheng S, et al. (2012) Decreased expression of small-conductance Ca2+-activated K+ channels SK1 and SK2 in human chronic atrial fibrillation. Life Sci 90:219-227. doi: 10.1016/j.lfs.2011.11.008.
43. Kubalova Z, Terentyev D, Viatchenko-Karpinski S, Nishijima Y, Gyorke I, et al. (2005) Abnormal intrastore calcium signaling in chronic heart failure. Proc Natl Acad Sci U S A 102:14104-14109. doi: 10.1073/pnas.0504298102.
44. Park YB (1994) Ion selectivity and gating of small conductance Ca (2+)-activated K+ channels in cultured rat adrenal chromaffin cells. J Physiol 481(Pt 3):555-570.
45. Van Wagoner DR, Pond AL, Lamorgese M, Rossie SS, McCarthy PM, et al. (1999) Atrial L-type Ca2+ currents and human atrial fibrillation. Circ Res 85:428-436. doi: 10.1161/01. RES.85.5.428.
46. Bkaily G, Sculptoreanu A, Jacques D, Economos D, Menard D (1992) Apamin, a highly potent fetal L-type Ca2+ current blocker in single heart cells. Am J Physiol 262:H463-H471.
47. Brillantes AM, Bezprozvannaya S, Marks AR (1994) Developmental and tissuespecific regulation of rabbit skeletal and cardiac muscle calcium channels involved in excitation-contraction coupling. Circ Res 75:503-510.