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Published in: Heart and Vessels 1/2011

01-01-2011 | Original Article

Diverse cell morphology and intracellular calcium dynamics in pulmonary vein cardiomyocytes

Authors: Ming-Chih Yu, Chun-Feng Huang, Che-Ming Chang, Yao-Chang Chen, Cheng-I Lin, Shih-Ann Chen

Published in: Heart and Vessels | Issue 1/2011

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Abstract

Pulmonary veins (PVs) contain cardiomyocytes with a complex cellular morphology and high arrhythmogenesis. Ca2+ regulation and Ca2+ sparks play a pivotal role in the electrical activity of cardiomyocytes. The purpose of this study was to investigate whether the cell morphology can determine the PV electrical activity and Ca2+ homeostasis. Through confocal microscopy with fluo-3 Ca2+ fluorescence, Ca2+ sparks and Ca2+ transients were evaluated in isolated single rabbit left atria (LA) and PV cardiomyocytes according to the cell morphology (rod, rod-spindle and spindle/bifurcated). Twenty-two (20%) rod, 49 (43%) rod-spindle and 41 (37%) spindle/bifurcated cardiomyocytes were identified in the LA (n = 29) and PV (n = 83) cardiomyocytes. The PV cardiomyocytes with pacemaker activity had a higher incidence of spindle/bifurcated morphology than LA and PV cardiomyocytes without pacemaker activity. As compared to those in the rod or rod-spindle cardiomyocytes, spindle/bifurcated cardiomyocytes had a larger Ca2+ transient amplitude and higher frequency of the Ca2+ sparks with larger amplitude and longer duration. In contrast, rod-spindle and rod cardiomyocytes had similar Ca2+ transients and Ca2+ sparks. The cell length correlated well with the amplitude of the Ca2+ transient and Ca2+ spark duration with a linear regression. In conclusion, cell morphology and cell length play a potential role in the Ca2+ homeostasis and Ca2+ spark. The large Ca2+ transients and high frequency of Ca2+ sparks in spindle/bifurcated cardiomyocytes may cause a high arrhythmogenesis in the PV cardiomyocytes with pacemaker activity.
Literature
1.
go back to reference Pappone C, Rosanio S, Oreto G, Tocchi M, Gugliotta F, Vicedomini G, Salvati A, Dicandia C, Mazzone P, Santinelli V, Gulletta S, Chierchia S (2000) Circumferential radiofrequency ablation of pulmonary vein ostia: a new anatomic approach for curing atrial fibrillation. Circulation 102:2619–2628PubMed Pappone C, Rosanio S, Oreto G, Tocchi M, Gugliotta F, Vicedomini G, Salvati A, Dicandia C, Mazzone P, Santinelli V, Gulletta S, Chierchia S (2000) Circumferential radiofrequency ablation of pulmonary vein ostia: a new anatomic approach for curing atrial fibrillation. Circulation 102:2619–2628PubMed
2.
go back to reference Chen SA, Chen YJ, Yeh HI, Tai CT, Chen YC, Lin CI (2003) Pathophysiology of the pulmonary vein as an atrial fibrillation initiator. Pacing Clin Electrophysiol 26:1576–1582CrossRefPubMed Chen SA, Chen YJ, Yeh HI, Tai CT, Chen YC, Lin CI (2003) Pathophysiology of the pulmonary vein as an atrial fibrillation initiator. Pacing Clin Electrophysiol 26:1576–1582CrossRefPubMed
3.
go back to reference Chen YJ, Chen SA, Chang MS, Lin CI (2000) Arrhythmogenic activity of cardiac muscle in pulmonary veins of the dog: implication for the genesis of atrial fibrillation. Cardiovasc Res 48:265–273CrossRefPubMed Chen YJ, Chen SA, Chang MS, Lin CI (2000) Arrhythmogenic activity of cardiac muscle in pulmonary veins of the dog: implication for the genesis of atrial fibrillation. Cardiovasc Res 48:265–273CrossRefPubMed
4.
go back to reference Suzuki S, Yamashita T, Otsuka T, Sagara K, Uejima T, Oikawa Y, Yajima J, Koike A, Nagashima K, Kirigaya H, Ogasawara K, Sawada H, Yamazaki T, Aizawa T (2009) Treatment strategy and clinical outcome in Japanese patients with atrial fibrillation. Heart Vessels 24:287–293CrossRefPubMed Suzuki S, Yamashita T, Otsuka T, Sagara K, Uejima T, Oikawa Y, Yajima J, Koike A, Nagashima K, Kirigaya H, Ogasawara K, Sawada H, Yamazaki T, Aizawa T (2009) Treatment strategy and clinical outcome in Japanese patients with atrial fibrillation. Heart Vessels 24:287–293CrossRefPubMed
5.
go back to reference Ejima K, Shoda M, Futagawa K, Kimura R, Manaka T, Hagiwara N, Kasanuki H (2009) Transverse shifting of the esophagus according to the patient’s position helped achieve a safe and successful pulmonary vein isolation procedure. Heart Vessels 24:317–319CrossRefPubMed Ejima K, Shoda M, Futagawa K, Kimura R, Manaka T, Hagiwara N, Kasanuki H (2009) Transverse shifting of the esophagus according to the patient’s position helped achieve a safe and successful pulmonary vein isolation procedure. Heart Vessels 24:317–319CrossRefPubMed
6.
go back to reference Wu J, Schuessler RB, Rodefeld MD, Saffitz JE, Boineau JP (2001) Morphological and membrane characteristics of spider and spindle cells isolated from rabbit sinus node. Am J Physiol Heart Circ Physiol 280:1232–1240 Wu J, Schuessler RB, Rodefeld MD, Saffitz JE, Boineau JP (2001) Morphological and membrane characteristics of spider and spindle cells isolated from rabbit sinus node. Am J Physiol Heart Circ Physiol 280:1232–1240
7.
go back to reference Munk AA, Adjemian RA, Zhao J, Ogbaghebriel A, Shrier A (1996) Electrophysiological properties of morphologically distinct cells isolated from the rabbit atrioventricular node. J Physiol 493:801–818PubMed Munk AA, Adjemian RA, Zhao J, Ogbaghebriel A, Shrier A (1996) Electrophysiological properties of morphologically distinct cells isolated from the rabbit atrioventricular node. J Physiol 493:801–818PubMed
8.
go back to reference Ren FX, Niu XL, Ou Y, Han ZH, Ling FD, Zhou SS, Li YJ (2006) Morphological and electrophysiological properties of single myocardial cells from Koch triangle of rabbit heart. Chin Med J 119:2075–2084PubMed Ren FX, Niu XL, Ou Y, Han ZH, Ling FD, Zhou SS, Li YJ (2006) Morphological and electrophysiological properties of single myocardial cells from Koch triangle of rabbit heart. Chin Med J 119:2075–2084PubMed
9.
go back to reference Chen YC, Chen SA, Chen YJ, Tai CT, Chan P, Lin CI (2004) T-type calcium current in electrical activity of cardiomyocytes isolated from rabbit pulmonary vein. J Cardiovasc Electrophysiol 15:567–571CrossRefPubMed Chen YC, Chen SA, Chen YJ, Tai CT, Chan P, Lin CI (2004) T-type calcium current in electrical activity of cardiomyocytes isolated from rabbit pulmonary vein. J Cardiovasc Electrophysiol 15:567–571CrossRefPubMed
10.
go back to reference Chou CC, Nihei M, Zhou S, Tan A, Kawase A, Macias ES, Fishbein MC, Lin SF, Chen PS (2005) Intracellular calcium dynamics and anisotropic reentry in isolated canine pulmonary veins and left atrium. Circulation 111:2889–2897CrossRefPubMed Chou CC, Nihei M, Zhou S, Tan A, Kawase A, Macias ES, Fishbein MC, Lin SF, Chen PS (2005) Intracellular calcium dynamics and anisotropic reentry in isolated canine pulmonary veins and left atrium. Circulation 111:2889–2897CrossRefPubMed
11.
go back to reference Patterson E, Lazzara R, Szabo B, Liu H, Tang D, Li YH, Scherlag BJ, Po SS (2006) Sodium-calcium exchange initiated by the Ca2+ transient: a arrhythmia trigger within pulmonary veins. J Am Coll Cardiol 47:1196–1206CrossRefPubMed Patterson E, Lazzara R, Szabo B, Liu H, Tang D, Li YH, Scherlag BJ, Po SS (2006) Sodium-calcium exchange initiated by the Ca2+ transient: a arrhythmia trigger within pulmonary veins. J Am Coll Cardiol 47:1196–1206CrossRefPubMed
12.
go back to reference Wongcharoen W, Chen YC, Chen YJ, Chen SY, Yeh HI, Lin CI, Chen SA (2007) Aging increases pulmonary veins arrhythmogenesis and susceptibility to calcium regulation agents. Heart Rhythm 4:1338–1349CrossRefPubMed Wongcharoen W, Chen YC, Chen YJ, Chen SY, Yeh HI, Lin CI, Chen SA (2007) Aging increases pulmonary veins arrhythmogenesis and susceptibility to calcium regulation agents. Heart Rhythm 4:1338–1349CrossRefPubMed
13.
go back to reference Chen YJ, Chen SA, Chen YC, Yeh HI, Chang MS, Lin CI (2002) Electrophysiology of single cardiomyocytes isolated from rabbit pulmonary veins: implication in initiation of focal atrial fibrillation. Basic Res Cardiol 97:26–34CrossRefPubMed Chen YJ, Chen SA, Chen YC, Yeh HI, Chang MS, Lin CI (2002) Electrophysiology of single cardiomyocytes isolated from rabbit pulmonary veins: implication in initiation of focal atrial fibrillation. Basic Res Cardiol 97:26–34CrossRefPubMed
14.
go back to reference Chen YJ, Chen YC, Tai CT, Yeh HI, Lin CI, Chen SA (2006) Angiotensin II and angiotensin II receptor blocker modulate the arrhythmogenic activity of pulmonary veins. Br J Pharmacol 147:12–22CrossRefPubMed Chen YJ, Chen YC, Tai CT, Yeh HI, Lin CI, Chen SA (2006) Angiotensin II and angiotensin II receptor blocker modulate the arrhythmogenic activity of pulmonary veins. Br J Pharmacol 147:12–22CrossRefPubMed
15.
go back to reference Wongcharoen W, Chen YC, Chen YJ, Chang CM, Yeh HI, Lin CI, Chen SA (2006) Effects of a Na+/Ca2+ exchanger inhibitor on pulmonary vein electrical activity and ouabain-induced arrhythmogenicity. Cardiovasc Res 70:497–508CrossRefPubMed Wongcharoen W, Chen YC, Chen YJ, Chang CM, Yeh HI, Lin CI, Chen SA (2006) Effects of a Na+/Ca2+ exchanger inhibitor on pulmonary vein electrical activity and ouabain-induced arrhythmogenicity. Cardiovasc Res 70:497–508CrossRefPubMed
16.
go back to reference Chang SH, Chen YC, Chiang SJ, Higa S, Cheng CC, Chen YJ, Chen SA (2008) Increased Ca(2+) sparks and sarcoplasmic reticulum Ca(2+) stores potentially determine the spontaneous activity of pulmonary vein cardiomyocytes. Life Sci 83:284–292CrossRefPubMed Chang SH, Chen YC, Chiang SJ, Higa S, Cheng CC, Chen YJ, Chen SA (2008) Increased Ca(2+) sparks and sarcoplasmic reticulum Ca(2+) stores potentially determine the spontaneous activity of pulmonary vein cardiomyocytes. Life Sci 83:284–292CrossRefPubMed
17.
go back to reference López-López JR, Shacklock PS, Balke CW, Wier WG (1994) Local Stochastic release of Ca2+ in voltage-clamped rat heart cells: visualization with confocal microscopy. J Physiol 480:21–29PubMed López-López JR, Shacklock PS, Balke CW, Wier WG (1994) Local Stochastic release of Ca2+ in voltage-clamped rat heart cells: visualization with confocal microscopy. J Physiol 480:21–29PubMed
18.
go back to reference Yin L, Bien H, Entcheva E (2004) Scaffold topography alters intracellular calcium dynamics in cultured cardiomyocyte networks. Am J Physiol Heart Circ Physiol 287:1276–1285CrossRef Yin L, Bien H, Entcheva E (2004) Scaffold topography alters intracellular calcium dynamics in cultured cardiomyocyte networks. Am J Physiol Heart Circ Physiol 287:1276–1285CrossRef
19.
go back to reference DiFrancesco D, Ferroni A, Mazzanti M, Tromba C (1986) Properties of the hyperpolarizing-activated current in cells isolated from the rabbit sino-atrial node. J Physiol 377:61–88PubMed DiFrancesco D, Ferroni A, Mazzanti M, Tromba C (1986) Properties of the hyperpolarizing-activated current in cells isolated from the rabbit sino-atrial node. J Physiol 377:61–88PubMed
20.
go back to reference Van Ginneken A, Giles W (1991) Voltage clamp measurements of the hyperpolarization-activated inward current If in single cells from rabbit sino-atrial node. J Physiol 434:57–83PubMed Van Ginneken A, Giles W (1991) Voltage clamp measurements of the hyperpolarization-activated inward current If in single cells from rabbit sino-atrial node. J Physiol 434:57–83PubMed
21.
go back to reference Baartscheer A, Schumacher CA, Belterman CN, Coronel R, Fiolet JW (2003) SR calcium handling and calcium after-transients in a rabbit model of heart failure. Cardiovasc Res 58:99–108CrossRefPubMed Baartscheer A, Schumacher CA, Belterman CN, Coronel R, Fiolet JW (2003) SR calcium handling and calcium after-transients in a rabbit model of heart failure. Cardiovasc Res 58:99–108CrossRefPubMed
22.
go back to reference Lipsius SL, Bers DM (2003) Cardiac pacemaking: If vs. Ca2+, is it really that simple? J Mol Cell Cardiol 35:891–893CrossRefPubMed Lipsius SL, Bers DM (2003) Cardiac pacemaking: If vs. Ca2+, is it really that simple? J Mol Cell Cardiol 35:891–893CrossRefPubMed
23.
go back to reference Kwong KF, Schuessler RB, Green KG, Laing JG, Beyer EC, Boineau JP, Saffitz JE (1998) Differential expression of gap junction proteins in the canine sinus node. Circ Res 82:604–612PubMed Kwong KF, Schuessler RB, Green KG, Laing JG, Beyer EC, Boineau JP, Saffitz JE (1998) Differential expression of gap junction proteins in the canine sinus node. Circ Res 82:604–612PubMed
24.
go back to reference Honjo H, Boyett MR, Kodama I, Toyama J (1996) Correlation between electrical activity and the size of rabbit sino-atrial node cells. J Physiol 496:795–808PubMed Honjo H, Boyett MR, Kodama I, Toyama J (1996) Correlation between electrical activity and the size of rabbit sino-atrial node cells. J Physiol 496:795–808PubMed
25.
go back to reference Sobie EA, Dilly KW, dos Santos CJ, Lederer WJ, Jafri MS (2002) Termination of cardiac Ca2+ sparks: an investigative mathematical model of calcium-induced calcium release. Biophys J 83:59–78CrossRefPubMed Sobie EA, Dilly KW, dos Santos CJ, Lederer WJ, Jafri MS (2002) Termination of cardiac Ca2+ sparks: an investigative mathematical model of calcium-induced calcium release. Biophys J 83:59–78CrossRefPubMed
Metadata
Title
Diverse cell morphology and intracellular calcium dynamics in pulmonary vein cardiomyocytes
Authors
Ming-Chih Yu
Chun-Feng Huang
Che-Ming Chang
Yao-Chang Chen
Cheng-I Lin
Shih-Ann Chen
Publication date
01-01-2011
Publisher
Springer Japan
Published in
Heart and Vessels / Issue 1/2011
Print ISSN: 0910-8327
Electronic ISSN: 1615-2573
DOI
https://doi.org/10.1007/s00380-010-0035-y

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