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Published in: Journal of Interventional Cardiac Electrophysiology 2/2021

01-03-2021 | Atrial Fibrillation

Role of intermediate-conductance calcium-activated potassium channels in atrial fibrillation in canines with rapid atrial pacing

Authors: Mei Yang, Youcheng Wang, Hongyi Zhao, Junkui Yin, Liuliu Zi, Xi Wang, Yanhong Tang, Congxin Huang, Qingyan Zhao

Published in: Journal of Interventional Cardiac Electrophysiology | Issue 2/2021

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Abstract

Purpose

The aim of the present study was to explore the role of intermediate-conductance Ca2+-activated K+ (SK4) in atrial fibrillation (AF) inducibility in canines with rapid atrial pacing.

Methods

Eighteen dogs were divided into the control group, the pacing group and the stellate ganglion ablation (SGA) + pacing group. In the pacing group, dogs were subjected to rapid atrial pacing, and the atrial effective refractory period (AERP) and AF inducibility were measured. After cessation of 7-h pacing, SK4 inhibitor (TRAM-34) was administered. After SGA, the SGA + pacing group received the same procedure of pacing and electrophysiological measurement as the pacing group. The expression of SK4 was measured in the left atrium (LA) and the right atrium (RA) in the three groups.

Results

The duration of the AERP decreased, while the number of AF episodes, the duration of induced AF, and the amplitude of stellate ganglion neural activity all increased after rapid atrial pacing. TRAM-34 completely inhibited AF induction in the pacing group. There was no significant difference in AERP shortening or AF vulnerability between the SGA + pacing group and the control group. The expression of SK4 in the LA and RA was higher in the pacing group than in the control and SGA + pacing groups. However, there was no significant difference in the expression of SK4 in the LA or the RA between the SGA + pacing group and the control group.

Conclusion

The higher expression of SK4 plays an important role in AF induction and the increased expression of SK4 in the atrium is related to SG activity during rapid atrial pacing.
Literature
1.
go back to reference Go AS, Hylek EM, Phillips KA, Chang Y, Henault LE, Selby JV, et al. Prevalence of diagnosed atrial fibrillation in adults: national implications for rhythm management and stroke prevention: the AnTicoagulation and Risk Factors in Atrial Fibrillation (ATRIA) study. JAMA. 2001;285:2370–5.CrossRef Go AS, Hylek EM, Phillips KA, Chang Y, Henault LE, Selby JV, et al. Prevalence of diagnosed atrial fibrillation in adults: national implications for rhythm management and stroke prevention: the AnTicoagulation and Risk Factors in Atrial Fibrillation (ATRIA) study. JAMA. 2001;285:2370–5.CrossRef
2.
go back to reference Chen PS, Chen LS, Fishbein MC, Lin SF, Nattel S. Role of the autonomic nervous system in atrial fibrillation: pathophysiology and therapy. Circ Res. 2014;114:1500–15.CrossRef Chen PS, Chen LS, Fishbein MC, Lin SF, Nattel S. Role of the autonomic nervous system in atrial fibrillation: pathophysiology and therapy. Circ Res. 2014;114:1500–15.CrossRef
3.
go back to reference Wang X, Zhao Q, Huang H, Tang Y, Xiao J, Dai Z, et al. Effect of renal sympathetic denervation on atrial substrate remodeling in ambulatory canines with prolonged atrial pacing. PLoS One. 2013;8:e64611.CrossRef Wang X, Zhao Q, Huang H, Tang Y, Xiao J, Dai Z, et al. Effect of renal sympathetic denervation on atrial substrate remodeling in ambulatory canines with prolonged atrial pacing. PLoS One. 2013;8:e64611.CrossRef
4.
go back to reference Schauerte P, Scherlag BJ, Pitha J, Scherlag MA, Reynolds D, Lazzara R, et al. Catheter ablation of cardiac autonomic nerves for prevention of vagal atrial fibrillation. Circulation. 2000;102:2774–80.CrossRef Schauerte P, Scherlag BJ, Pitha J, Scherlag MA, Reynolds D, Lazzara R, et al. Catheter ablation of cardiac autonomic nerves for prevention of vagal atrial fibrillation. Circulation. 2000;102:2774–80.CrossRef
5.
go back to reference Yu L, Scherlag BJ, Sha Y, Li S, Sharma T, Nakagawa H, et al. Interactions between atrial electrical remodeling and autonomic remodeling: how to break the vicious cycle. Heart Rhythm. 2012;9:804–9.CrossRef Yu L, Scherlag BJ, Sha Y, Li S, Sharma T, Nakagawa H, et al. Interactions between atrial electrical remodeling and autonomic remodeling: how to break the vicious cycle. Heart Rhythm. 2012;9:804–9.CrossRef
6.
go back to reference Baron R, Jänig W, With H. Sympathetic and afferent neurones projecting into forelimb and trunk nerves and the anatomical organization of the thoracic sympathetic outflow of the rat. J Auton Nerv Syst. 1995;53:205–14.CrossRef Baron R, Jänig W, With H. Sympathetic and afferent neurones projecting into forelimb and trunk nerves and the anatomical organization of the thoracic sympathetic outflow of the rat. J Auton Nerv Syst. 1995;53:205–14.CrossRef
7.
go back to reference Taniguchi T, Morimoto M, Taniguchi Y, Takasaka M, Totoki T. Cutaneous distribution of sympathetic postganglionic fibers from stellate ganglion: a retrograde axonal tracing study using wheat germ agglutinin conjugated with horseradish peroxidase. J Anesth. 1994;8:441–9.CrossRef Taniguchi T, Morimoto M, Taniguchi Y, Takasaka M, Totoki T. Cutaneous distribution of sympathetic postganglionic fibers from stellate ganglion: a retrograde axonal tracing study using wheat germ agglutinin conjugated with horseradish peroxidase. J Anesth. 1994;8:441–9.CrossRef
8.
go back to reference Li Z, Wang M, Zhang Y, Zheng S, Wang X, Hou Y. The effect of the left stellate ganglion on sympathetic neural remodeling of the left atrium in rats following myocardial infarction. Pacing Clin Electrophysiol. 2015;38:107–14.CrossRef Li Z, Wang M, Zhang Y, Zheng S, Wang X, Hou Y. The effect of the left stellate ganglion on sympathetic neural remodeling of the left atrium in rats following myocardial infarction. Pacing Clin Electrophysiol. 2015;38:107–14.CrossRef
9.
go back to reference Köhler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, et al. Small conductance, calcium-activated potassium channels from mammalian brain. Science. 1996;273:1709–14.CrossRef Köhler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, et al. Small conductance, calcium-activated potassium channels from mammalian brain. Science. 1996;273:1709–14.CrossRef
10.
go back to reference Tuteja D, Rafizadeh S, Timofeyev V, Wang S, Zhang Z, Li N, et al. Differential expression of small-conductance Ca 2+-activated K+ channels SK1, SK2, and SK3 in mouse atrial and ventricular myocytes. Am J Physiol Heart Circ Physiol. 2005;289:H2714–23.CrossRef Tuteja D, Rafizadeh S, Timofeyev V, Wang S, Zhang Z, Li N, et al. Differential expression of small-conductance Ca 2+-activated K+ channels SK1, SK2, and SK3 in mouse atrial and ventricular myocytes. Am J Physiol Heart Circ Physiol. 2005;289:H2714–23.CrossRef
11.
go back to reference Zhang XD, Lieu DK, Chiamvimonvat N. Small-conductance Ca2+-activated K+ channels and cardiac arrhythmias. Heart Rhythm. 2015;12:1845–51.CrossRef Zhang XD, Lieu DK, Chiamvimonvat N. Small-conductance Ca2+-activated K+ channels and cardiac arrhythmias. Heart Rhythm. 2015;12:1845–51.CrossRef
12.
go back to reference Nouchi H, Takahara A, Nakamura H, Namekata I, Sugimoto T, Tsuneoka Y, et al. Chronic left atrial volume overload abbreviates the action potential duration of the caninepulmonary vein myocardium via activation of IK channel. Eur J Pharmacol. 2008;597:81–5.CrossRef Nouchi H, Takahara A, Nakamura H, Namekata I, Sugimoto T, Tsuneoka Y, et al. Chronic left atrial volume overload abbreviates the action potential duration of the caninepulmonary vein myocardium via activation of IK channel. Eur J Pharmacol. 2008;597:81–5.CrossRef
13.
go back to reference Qi XY, Diness JG, Brundel BJ, Zhou XB, Naud P, Wu CT, et al. Role of small-conductance calcium-activated potassium channels in atrial electrophysiologyand fibrillation in the dog. Circulation. 2014;129:430–40.CrossRef Qi XY, Diness JG, Brundel BJ, Zhou XB, Naud P, Wu CT, et al. Role of small-conductance calcium-activated potassium channels in atrial electrophysiologyand fibrillation in the dog. Circulation. 2014;129:430–40.CrossRef
14.
go back to reference Weisbrod D, Khun SH, Bueno H, Peretz A, Attali B. Mechanisms underlying the cardiac pacemaker: the role of SK4 calcium-activated potassium channels. Acta Pharmacol Sin. 2016;37:82–97.CrossRef Weisbrod D, Khun SH, Bueno H, Peretz A, Attali B. Mechanisms underlying the cardiac pacemaker: the role of SK4 calcium-activated potassium channels. Acta Pharmacol Sin. 2016;37:82–97.CrossRef
15.
go back to reference Diness JG, Bentzen BH, Sørensen US. Morten Grunnet Role of calcium-activated potassium channels in atrial fibrillation pathophysiology and therapy. J Cardiovasc Pharmacol. 2015;66:441–8.CrossRef Diness JG, Bentzen BH, Sørensen US. Morten Grunnet Role of calcium-activated potassium channels in atrial fibrillation pathophysiology and therapy. J Cardiovasc Pharmacol. 2015;66:441–8.CrossRef
16.
go back to reference Diness JG, Skibsbye L, Simó-Vicens R, Santos JL, Lundegaard P, Citerni C, Sauter DRP, Bomholtz SH, Svendsen JH, Olesen SP, Sørensen US, Jespersen T, Grunnet M, Bentzen BH. Termination of vernakalant-resistant atrial fibrillation by inhibition of small-conductance Ca2+-activated K+ channels in pigs. Circ Arrhythm Electrophysiol. 2017;10. Diness JG, Skibsbye L, Simó-Vicens R, Santos JL, Lundegaard P, Citerni C, Sauter DRP, Bomholtz SH, Svendsen JH, Olesen SP, Sørensen US, Jespersen T, Grunnet M, Bentzen BH. Termination of vernakalant-resistant atrial fibrillation by inhibition of small-conductance Ca2+-activated K+ channels in pigs. Circ Arrhythm Electrophysiol. 2017;10.
17.
go back to reference Faber ES, Delaney AJ, Power JM, Sedlak PL, Crane JW, Sah P. Modulation of SK channel trafficking by beta adrenoceptors enhances excitatory synaptic transmission and plasticity in the amygdala. J Neurosci. 2008;28:10803–13.CrossRef Faber ES, Delaney AJ, Power JM, Sedlak PL, Crane JW, Sah P. Modulation of SK channel trafficking by beta adrenoceptors enhances excitatory synaptic transmission and plasticity in the amygdala. J Neurosci. 2008;28:10803–13.CrossRef
18.
go back to reference Haron-Khun S, Weisbrod D, Bueno H, Yadin D, Behar J, Peretz A, et al. SK4 K+ channels are therapeutic targets for the treatment of cardiac arrhythmias. EMBO Mol Med. 2017;9:415–29.CrossRef Haron-Khun S, Weisbrod D, Bueno H, Yadin D, Behar J, Peretz A, et al. SK4 K+ channels are therapeutic targets for the treatment of cardiac arrhythmias. EMBO Mol Med. 2017;9:415–29.CrossRef
19.
go back to reference Vergara C, Latorre R, Marrion NV, Adelman JP. Calcium-activated potassium channels. Curr Opin Neurobiol. 1998;8:321–9.CrossRef Vergara C, Latorre R, Marrion NV, Adelman JP. Calcium-activated potassium channels. Curr Opin Neurobiol. 1998;8:321–9.CrossRef
20.
go back to reference Chen WT, Chen YC, Lu YY, Kao YH, Huang JH, Lin YK, et al. Apamin modulates electrophysiological characteristics of the pulmonary vein and the sinoatrial node. Eur J Clin Investig. 2013;43:957–63.CrossRef Chen WT, Chen YC, Lu YY, Kao YH, Huang JH, Lin YK, et al. Apamin modulates electrophysiological characteristics of the pulmonary vein and the sinoatrial node. Eur J Clin Investig. 2013;43:957–63.CrossRef
21.
go back to reference Nouchi H, Takahara A, Nakamura H, Namekata I, Sugimoto T, Tsuneoka Y, et al. Chronic left atrial volume overload abbreviates the action potential duration of the canine pulmonary vein myocardium via activation of IK channel. Eur J Pharmacol. 2008;597:81–5.CrossRef Nouchi H, Takahara A, Nakamura H, Namekata I, Sugimoto T, Tsuneoka Y, et al. Chronic left atrial volume overload abbreviates the action potential duration of the canine pulmonary vein myocardium via activation of IK channel. Eur J Pharmacol. 2008;597:81–5.CrossRef
22.
go back to reference Liebau S, Tischendorf M, Ansorge D, Linta L, Stockmann M, Weidgang C, et al. An inducible expression system of the calcium-activated potassium channel 4 to study the differential impact on embryonic stem cells. Stem Cells Int. 2011;2011:1–12.CrossRef Liebau S, Tischendorf M, Ansorge D, Linta L, Stockmann M, Weidgang C, et al. An inducible expression system of the calcium-activated potassium channel 4 to study the differential impact on embryonic stem cells. Stem Cells Int. 2011;2011:1–12.CrossRef
23.
go back to reference Weisbrod D, Peretz A, Ziskind A, Menaker N, Oz S, Barad L, et al. SK4 Ca2+ activated K+ channel is a critical player in cardiac pacemaker derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2013;110:E1685–94.CrossRef Weisbrod D, Peretz A, Ziskind A, Menaker N, Oz S, Barad L, et al. SK4 Ca2+ activated K+ channel is a critical player in cardiac pacemaker derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2013;110:E1685–94.CrossRef
24.
go back to reference Ter Keurs HE, Boyden PA. Calcium and arrhythmogenesis. Physiol Rev. 2007;87:457–506.CrossRef Ter Keurs HE, Boyden PA. Calcium and arrhythmogenesis. Physiol Rev. 2007;87:457–506.CrossRef
25.
go back to reference Jayachandran JV, Sih HJ, Winkle W, Zipes DP, Hutchins GD, Olgin JE. Atrial fibrillation produced by prolonged rapid atrial pacing is associated with heterogeneous changes in atrial sympathetic innervation. Circulation. 2000;101:1185–91.CrossRef Jayachandran JV, Sih HJ, Winkle W, Zipes DP, Hutchins GD, Olgin JE. Atrial fibrillation produced by prolonged rapid atrial pacing is associated with heterogeneous changes in atrial sympathetic innervation. Circulation. 2000;101:1185–91.CrossRef
26.
go back to reference Swissa M, Zhou S, Tan AY, Fishbein MC, Chen PS, Chen LS. Atrial sympathetic and parasympathetic nerve sprouting and hyperinnervation induced by subthreshold electrical stimulation of the left stellate ganglion in normal dogs. Cardiovasc Pathol. 2008;17:303–8.CrossRef Swissa M, Zhou S, Tan AY, Fishbein MC, Chen PS, Chen LS. Atrial sympathetic and parasympathetic nerve sprouting and hyperinnervation induced by subthreshold electrical stimulation of the left stellate ganglion in normal dogs. Cardiovasc Pathol. 2008;17:303–8.CrossRef
27.
go back to reference Rahman F, Kwan GF, Benjamin EJ. Global epidemiology of atrial fibrillation. Nat Rev Cardiol. 2014;11:639–54.CrossRef Rahman F, Kwan GF, Benjamin EJ. Global epidemiology of atrial fibrillation. Nat Rev Cardiol. 2014;11:639–54.CrossRef
28.
go back to reference Healey JS, Oldgren J, Ezekowitz M, Zhu J, Pais P, Wang J, et al. Occurrence of death and stroke in patients in 47 countries 1 year after presenting with atrial fibrillation: a cohort study. Lancet. 2016;388:1161–9.CrossRef Healey JS, Oldgren J, Ezekowitz M, Zhu J, Pais P, Wang J, et al. Occurrence of death and stroke in patients in 47 countries 1 year after presenting with atrial fibrillation: a cohort study. Lancet. 2016;388:1161–9.CrossRef
29.
go back to reference Cotté FE, Chaize G, Gaudin AF, Samson A, Vainchtock A, Fauchier L. Burden of stroke and other cardiovascular complications in patients with atrial fibrillation hospitalized in France. Europace. 2016;18:501–7.CrossRef Cotté FE, Chaize G, Gaudin AF, Samson A, Vainchtock A, Fauchier L. Burden of stroke and other cardiovascular complications in patients with atrial fibrillation hospitalized in France. Europace. 2016;18:501–7.CrossRef
30.
go back to reference Sorgente A, Tung P, Wylie J, Josephson ME. Six year follow-up after catheter ablation of atrial fibrillation: a palliation more than a true cure. Am J Cardiol. 2012;109:1179–86.CrossRef Sorgente A, Tung P, Wylie J, Josephson ME. Six year follow-up after catheter ablation of atrial fibrillation: a palliation more than a true cure. Am J Cardiol. 2012;109:1179–86.CrossRef
31.
go back to reference Tilz RR, Rillig A, Thum AM, Arya A, Wohlmuth P, Metzner A, et al. Catheter ablation of long-standing persistent atrial fibrillation: 5-year outcomes of the Hamburg Sequential Ablation Strategy. J Am Coll Cardiol. 2012;60:1921–9.CrossRef Tilz RR, Rillig A, Thum AM, Arya A, Wohlmuth P, Metzner A, et al. Catheter ablation of long-standing persistent atrial fibrillation: 5-year outcomes of the Hamburg Sequential Ablation Strategy. J Am Coll Cardiol. 2012;60:1921–9.CrossRef
Metadata
Title
Role of intermediate-conductance calcium-activated potassium channels in atrial fibrillation in canines with rapid atrial pacing
Authors
Mei Yang
Youcheng Wang
Hongyi Zhao
Junkui Yin
Liuliu Zi
Xi Wang
Yanhong Tang
Congxin Huang
Qingyan Zhao
Publication date
01-03-2021
Publisher
Springer US
Published in
Journal of Interventional Cardiac Electrophysiology / Issue 2/2021
Print ISSN: 1383-875X
Electronic ISSN: 1572-8595
DOI
https://doi.org/10.1007/s10840-020-00736-8

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