T-type calcium current contributes to escape automaticity and governs the occurrence of lethal arrhythmias after atrioventricular block in mice

Circulation: Arrhythmia and Electrophysiology

Volumn 6, Issue 4, 2013, Pages 799-808

  Le Quang, Khai ^a,b   Benito, Begoña ^a,c   Naud, Patrice ^a   Qi, Xiao Yan ^a   Shi, Yan Fen ^a   Tardif, Jean Claude ^a   Gillis, Marc Antoine ^a   Dobrev, Dobromir ^d,e   Charpentier, Flavien ^f   Nattel, Stanley ^a  

^a MONTREAL HEART INSTITUTE   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c HOSPITAL DEL MAR   (Spain)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f L INSTITUT DU THORAX   (France)

Author keywords

Atrioventricular block; Cardiac remodeling, ventricular; Cav3.1 protein, mouse; T type calcium channel; Tachycardia, ventricular

Indexed keywords

CALCIUM CHANNEL T TYPE; ISOPRENALINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRADYCARDIA; CALCIUM CURRENT; CARDIOVASCULAR MORTALITY; COMPLETE HEART BLOCK; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAM; GENE EXPRESSION; HEART ARRHYTHMIA; HEART ATRIOVENTRICULAR NODE; HEART RATE; HEART RHYTHM; HEART VENTRICLE FUNCTION; HEART VENTRICLE TACHYCARDIA; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RADIOFREQUENCY; SINUS BRADYCARDIA; TELEMETRY; TORSADE DES POINTES;

ATRIOVENTRICULAR BLOCK; CARDIAC REMODELING, VENTRICULAR; CAV3.1 PROTEIN, MOUSE; T-TYPE CALCIUM CHANNEL; TACHYCARDIA, VENTRICULAR;

ACTION POTENTIALS; ANIMALS; ATRIOVENTRICULAR BLOCK; BRADYCARDIA; CALCIUM CHANNELS, T-TYPE; CALCIUM SIGNALING; DISEASE MODELS, ANIMAL; ELECTROCARDIOGRAPHY, AMBULATORY; ELECTROPHYSIOLOGIC TECHNIQUES, CARDIAC; GENE EXPRESSION REGULATION; HEART CONDUCTION SYSTEM; HEART RATE; MALE; MICE; MICE, KNOCKOUT; PERIODICITY; RNA, MESSENGER; TELEMETRY; TIME FACTORS; TORSADES DE POINTES; VENTRICULAR REMODELING;

EID: 84884520282     PISSN: 19413149     EISSN: 19413084     Source Type: Journal    
DOI: 10.1161/CIRCEP.113.000407     Document Type: Article

References (33)

1. Hagiwara N, Irisawa H, Kameyama M. Contribution of two types of calcium currents to the pacemaker potentials of rabbit sino-atrial node cells. J Physiol. 1988;395: 233-253.
2. Verheijck EE, van Ginneken AC, Wilders R, Bouman LN. Contribution of L-type Ca2+ current to electrical activity in sinoatrial nodal myocytes of rabbits. Am J Physiol. 1999;276(3 Pt 2):H1064-H1077.
3. Stieber J, Herrmann S, Feil S, Löster J, Feil R, Biel M, Hofmann F, Ludwig A. The hyperpolarization-activated channel HCN4 is required for the generation of pacemaker action potentials in the embryonic heart. Proc Natl Acad Sci U S A. 2003;100: 15235-15240.
4. Gao Z, Chen B, Joiner ML, Wu Y, Guan X, Koval OM, Chaudhary AK, Cunha SR, Mohler PJ, Martins JB, Song LS, Anderson ME. I(f) and SR Ca(2+) release both contribute to pacemaker activity in canine sinoatrial node cells. J Mol Cell Cardiol. 2010;49: 33-40.
5. Mangoni ME, Traboulsie A, Leoni AL, Couette B, Marger L, Le Quang K, Kupfer E, Cohen-Solal A, Vilar J, Shin HS, Escande D, Charpentier F, Nargeot J, Lory P. Bradycardia and slowing of the atrioventricular conduction in mice lacking CaV3.1/alpha1G T-type calcium channels. Circ Res. 2006;98: 1422-1430.
6. Hüser J, Blatter LA, Lipsius SL. Intracellular Ca2+ release contributes to automaticity in cat atrial pacemaker cells. J Physiol. 2000;524(Pt 2): 415-422.
7. Vassort G, Talavera K, Alvarez JL. Role of T-type Ca2+ channels in the heart. Cell Calcium. 2006;40: 205-220.
8. Qi X, Yeh YH, Chartier D, Xiao L, Tsuji Y, Brundel BJ, Kodama I, Nattel S. The calcium/calmodulin/kinase system and arrhythmogenic afterdepolarizations in bradycardia-related acquired long-QT syndrome. Circ Arrhythm Electrophysiol. 2009;2: 295-304.
9. Kim D, Song I, Keum S, Lee T, Jeong MJ, Kim SS, McEnery MW, Shin HS. Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels. Neuron. 2001;31: 35-45.
10. Bignolais O, Quang KL, Naud P, El Harchi A, Briec F, Piron J, Bourge A, Leoni AL, Charpentier F, Demolombe S. Early ion-channel remodeling and arrhythmias precede hypertrophy in a mouse model of complete atrioventricular block. J Mol Cell Cardiol. 2011;51: 713-721.
11. Liao Y, Ishikura F, Beppu S, Asakura M, Takashima S, Asanuma H, Sanada S, Kim J, Ogita H, Kuzuya T, Node K, Kitakaze M, Hori M. Echocardiographic assessment of LV hypertrophy and function in aortic- banded mice: necropsy validation. Am J Physiol Heart Circ Physiol. 2002;282:H1703-H1708.
12. Gaborit N, Le Bouter S, Szuts V, Varro A, Escande D, Nattel S, Demolombe S. Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J Physiol. 2007;582(Pt 2): 675-693.
13. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25: 402-408.
14. Ono K, Iijima T. Cardiac T-type Ca(2+) channels in the heart. J Mol Cell Cardiol. 2010;48: 65-70.
15. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev. 2005;57: 411-425.
16. Ferron L, Capuano V, Deroubaix E, Coulombe A, Renaud JF. Functional and molecular characterization of a T-type Ca(2+) channel during fetal and postnatal rat heart development. J Mol Cell Cardiol. 2002;34: 533-546.
17. Bohn G, Moosmang S, Conrad H, Ludwig A, Hofmann F, Klugbauer N. Expression of T- and L-type calcium channel mRNA in murine sinoatrial node. FEBS Lett. 2000;481: 73-76.
18. Schram G, Pourrier M, Melnyk P, Nattel S. Differential distribution of cardiac ion channel expression as a basis for regional specialization in electrical function. Circ Res. 2002;90: 939-950.
19. Nilius B, Hess P, Lansman JB, Tsien RW. A novel type of cardiac calcium channel in ventricular cells. Nature. 1985;316: 443-446.
20. Subbiah RN, Gollob MH, Gula LJ, Davies RW, Leong-Sit P, Skanes AC, Yee R, Klein GJ, Krahn AD. Torsades de pointes during complete atrioventricular block: Genetic factors and electrocardiogram correlates. Can J Cardiol. 2010;26: 208-212.
21. Gang UJ, Jøns C, Jørgensen RM, Abildstrøm SZ, Messier MD, Haarbo J, Huikuri HV, Thomsen PE. Clinical significance of late high-degree atrioventricular block in patients with left ventricular dysfunction after an acute myocardial infarction-a Cardiac Arrhythmias and Risk Stratification After Acute Myocardial Infarction (CARISMA) substudy. Am Heart J. 2011;162: 542-547.
22. Volders PG, Sipido KR, Vos MA, Spätjens RL, Leunissen JD, Carmeliet E, Wellens HJ. Downregulation of delayed rectifier K(+) currents in dogs with chronic complete atrioventricular block and acquired torsades de pointes. Circulation. 1999;100: 2455-2461.
23. Tsuji Y, Opthof T, Yasui K, Inden Y, Takemura H, Niwa N, Lu Z, Lee JK, Honjo H, Kamiya K, Kodama I. Ionic mechanisms of acquired QT prolongation and torsades de pointes in rabbits with chronic complete atrioventricular block. Circulation. 2002;106: 2012-2018.
24. 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 delayedrectifier changes. Circulation. 2006;113: 345-355.
25. Viswanathan PC, Rudy Y. Pause induced early afterdepolarizations in the long QT syndrome: a simulation study. Cardiovasc Res. 1999;42: 530-542.
26. Sipido KR, Volders PG, de Groot SH, Verdonck F, Van de Werf F, Wellens HJ, Vos MA. Enhanced Ca(2+) release and Na/Ca exchange activity in hypertrophied canine ventricular myocytes: potential link between contractile adaptation and arrhythmogenesis. Circulation. 2000;102: 2137-2144.
27. Le Quang K, Naud P, Qi XY, Duval F, Shi YF, Gillis MA, Comtois P, Tardif JC, Li D, Levesque PC, Dobrev D, Charpentier F, Nattel S. Role of T-type calcium channel subunits in post-myocardial infarction remodelling probed with genetically engineered mice. Cardiovasc Res. 2011;91: 420-428.
28. Chien KR, Knowlton KU, Zhu H, Chien S. Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. FASEB J. 1991;5: 3037-3046.
29. McMullen JR, Jennings GL. Differences between pathological and physiological cardiac hypertrophy: novel therapeutic strategies to treat heart failure. Clin Exp Pharmacol Physiol. 2007;34: 255-262.
30. Sandmann S, Min JY, Meissner A, Unger T. Effects of the calcium channel antagonist mibefradil on haemodynamic parameters and myocardial Ca(2+)-handling in infarct-induced heart failure in rats. Cardiovasc Res. 1999;44: 67-80.
31. Fareh S, Bénardeau A, Thibault B, Nattel S. The T-type Ca(2+) channel blocker mibefradil prevents the development of a substrate for atrial fibrillation by tachycardia-induced atrial remodeling in dogs. Circulation. 1999;100: 2191-2197.
32. Nakayama H, Bodi I, Correll RN, Chen X, Lorenz J, Houser SR, Robbins J, Schwartz A, Molkentin JD. alpha1G-dependent T-type Ca2+ current antagonizes cardiac hypertrophy through a NOS3-dependent mechanism in mice. J Clin Invest. 2009;119: 3787-3796.
33. Selvetella G, Hirsch E, Notte A, Tarone G, Lembo G. Adaptive and maladaptive hypertrophic pathways: points of convergence and divergence. Cardiovasc Res. 2004;63: 373-380.