Spatial and temporal heterogeneities are localized to the right ventricular outflow tract in a heterozygotic Scn5a mouse model

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 2, 2011, Pages

  Martin, Claire A ^a   Grace, Andrew A ^a   Huang, Christopher L H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Arrhythmia; Sodium channel; Transgenic mouse

Indexed keywords

FLECAINIDE; QUINIDINE; SODIUM CHANNEL NAV1.5;

ACTION POTENTIAL; ANIMAL TISSUE; ARRHYTHMOGENESIS; ARTICLE; HEART ELECTROPHYSIOLOGY; HEART RIGHT VENTRICLE OUTFLOW TRACT; HEART VENTRICLE TACHYCARDIA; ISOLATED HEART; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; ANTI-ARRHYTHMIA AGENTS; ARRHYTHMIAS, CARDIAC; BLOOD PRESSURE; ELECTROCARDIOGRAPHY; ELECTROPHYSIOLOGICAL PHENOMENA; FLECAINIDE; HETEROZYGOTE; MICE; MICE, KNOCKOUT; PERICARDIUM; QUINIDINE; REFRACTORY PERIOD, ELECTROPHYSIOLOGICAL; SODIUM CHANNELS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR FUNCTION, RIGHT;

EID: 79551475074     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00824.2010     Document Type: Article

References (63)

1. Aiba T, Shimizu W, Hidaka I, Uemura K, Noda T, Zheng C, Kamiya A, Inagaki M, Sugimachi M, Sunagawa K. Cellular basis for trigger and maintenance of ventricular fibrillation in the Brugada syndrome model: high-resolution optical mapping study. J Am Coll Cardiol 47: 2074-2085, 2006.
2. Alings M, Dekker L, Sadee A, Wilde A. Quinidine induced electrocardiographic normalization in two patients with Brugada syndrome. Pacing Clin Electrophysiol 24: 1420-1422, 2001.
3. Antzelevitch C. Role of spatial dispersion of repolarization in inherited and acquired sudden cardiac death syndromes. Am J Physiol Heart Circ Physiol 293: H2024-H2038, 2007.
4. Antzelevitch C, Brugada P, Brugada J, Brugada R. Brugada syndrome: from cell to bedside. Curr Probl Cardiol 30: 9-54, 2005.
5. Balasubramaniam R, Grace AA, Saumarez RC, Vandenberg JI, Huang CL. Electrogram prolongation and nifedipine-suppressible ventricular arrhythmias in mice following targeted disruption of KCNE1. J Physiol 552: 535-546, 2003.
6. Banville I, Gray RA. Effect of action potential duration and conduction velocity restitution and their spatial dispersion on alternans and the stability of arrhythmias. J Cardiovasc Electrophysiol 13: 1141-1149, 2002.
7. Birkett D. Therapeutic drug monitoring. Aust Prescr 20: 9-11, 1997.
8. + current in the ferret heart. Circ Res 81: 128-135, 1997.
9. Burton FL, Cobbe SM. Dispersion of ventricular repolarization and refractory period. Cardiovasc Res 50: 10-23, 2001.
10. Burton FL, Cobbe SM. Effect of sustained stretch on dispersion of ventricular fibrillation intervals in normal rabbit hearts. Cardiovasc Res 39: 351-359, 1998.
11. Chauhan VS, Downar E, Nanthakumar K, Parker JD, Ross HJ, Chan W, Picton P. Increased ventricular repolarization heterogeneity in patients with ventricular arrhythmia vulnerability and cardiomyopathy: a human in vivo study. Am J Physiol Heart Circ Physiol 290: H79-H86, 2006.
12. + current: a potential mechanism of the proarrhythmic effects of methanesulfonanilideclass III agents. Cardiovasc Res 43: 135-147, 1999.
13. Cherry EM, Fenton FH. Suppression of alternans and conduction blocks despite steep APD restitution: electrotonic, memory, and conduction velocity restitution effects. Am J Physiol Heart Circ Physiol 286: H2332-H2341, 2004.
14. Coronel R, Casini S, Koopmann TT, Wilms-Schopman FJ, Verkerk AO, de Groot JR, Bhuiyan Z, Bezzina CR, Veldkamp MW, Linnenbank AC, van der Wal AC, Tan HL, Brugada P, Wilde AA, de Bakker JM. Right ventricular fibrosis and conduction delay in a patient with clinical signs of Brugada syndrome: a combined electrophysiological, genetic, histopathologic, and computational study. Circulation 112: 2769-2777, 2005.
15. Dean JW, Lab MJ. Regional changes in ventricular excitability during load manipulation of the in situ pig heart. J Physiol 429: 387-400, 1990.
16. Eckardt L, Probst V, Smits JP, Bahr ES, Wolpert C, Schimpf R, Wichter T, Boisseau P, Heinecke A, Breithardt G, Borggrefe M, LeMarec H, Bocker D, Wilde AA. Long-term prognosis of individuals with right precordial ST-segment-elevation Brugada syndrome. Circulation 111: 257-263, 2005.
17. Franz MR, Bargheer K, Rafflenbeul W, Haverich A, Lichtlen PR. Monophasic action potential mapping in human subjects with normal electrocardiograms: direct evidence for the genesis of the T wave. Circulation 75: 379-386, 1987.
18. Frustaci A, Priori SG, Pieroni M, Chimenti C, Napolitano C, Rivolta I, Sanna T, Bellocci F, Russo MA. Cardiac histological substrate in patients with clinical phenotype of Brugada syndrome. Circulation 112: 3680-3687, 2005. (Pubitemid 43739507)
19. Hayashi M, Takatsuki S, Maison-Blanche P, Messali A, Haggui A, Milliez P, Leenhardt A, Extramiana F. Ventricular repolarization restitution properties in patients exhibiting type 1 Brugada electrocardiogram with and without inducible ventricular fibrillation. J Am Coll Cardiol 51: 1162-1168, 2008.
20. Head CE, Balasubramaniam R, Thomas G, Goddard CA, Lei M, Colledge WH, Grace AA, Huang CL. Paced electrogram fractionation analysis of arrhythmogenic tendency in DeltaKPQ Scn5a mice. J Cardiovasc Electrophysiol 16: 1329-1340, 2005.
21. Hisamatsu K, Kusano KF, Morita H, Takenaka S, Nagase S, Nakamura K, Emori T, Matsubara H, Mikouchi H, Nishizaki Y, Ohe T. Relationships between depolarization abnormality and repolarization abnormality in patients with Brugada syndrome: using body surface signalaveraged electrocardiography and body surface maps. J Cardiovasc Electrophysiol 15: 870-876, 2004.
22. Izumida N, Asano Y, Doi S, Wakimoto H, Fukamizu S, Kimura T, Ueyama T, Sakurada H, Kawano S, Sawanobori T, Hiraoka M. Changes in body surface potential distributions induced by isoproterenol and Na channel blockers in patients with the Brugada syndrome. Int J Cardiol 95: 261-268, 2004.
23. Kanda M, Shimizu W, Matsuo K, Nagaya N, Taguchi A, Suyama K, Kurita T, Aihara N, Kamakura S. Electrophysiologic characteristics and implications of induced ventricular fibrillation in symptomatic patients with Brugada syndrome. J Am Coll Cardiol 39: 1799-1805, 2002.
24. Kurita T, Shimizu W, Inagaki M, Suyama K, Taguchi A, Satomi K, Aihara N, Kamakura S, Kobayashi J, Kosakai Y. The electrophysiologic mechanism of ST-segment elevation in Brugada syndrome. J Am Coll Cardiol 40: 330-334, 2002.
25. Lambiase PD, Ahmed AK, Ciaccio EJ, Brugada R, Lizotte E, Chaubey S, Ben-Simon R, Chow AW, Lowe MD, McKenna WJ. High-density substrate mapping in Brugada syndrome: combined role of conduction and repolarization heterogeneities in arrhythmogenesis. Circulation 120: 106-117, 2009.
26. Laurita KR, Girouard SD, Rosenbaum DS. Modulation of ventricular repolarization by a premature stimulus. Role of epicardial dispersion of repolarization kinetics demonstrated by optical mapping of the intact guinea pig heart. Circ Res 79: 493-503, 1996.
27. + current in human ventricular myocytes. Circ Res 78: 689-696, 1996.
28. Martin CA, Zhang Y, Grace AA, Huang CL. In vivo studies of Scn5a+/- mice modeling Brugada syndrome demonstrate both conduction and repolarization abnormalities. J Electrocardiol 43: 433-439, 2010.
29. Martin CA, Zhang Y, Grace AA, Huang CL. Increased right ventricular repolarization gradients promote arrhythmogenesis in a murine model of Brugada Syndrome. J Cardiovasc Electrophysiol 21: 1153-1159, 2010.
30. Matthews GD, Martin CA, Grace AA, Zhang Y, Huang CL. Regional variations in action potential alternans in isolated murine Scn5a(+/-) hearts during dynamic pacing. Acta Physiol (Oxf) 200: 129-146, 2010.
31. Meregalli PG, Wilde AA, Tan HL. Pathophysiological mechanisms of Brugada syndrome: depolarization disorder, repolarization disorder, or more? Cardiovasc Res 67: 367-378, 2005.
32. Moorman AF, Schumacher CA, de Boer PA, Hagoort J, Bezstarosti K, van den Hoff MJ, Wagenaar GT, Lamers JM, Wuytack F, Christoffels VM, Fiolet JW. Presence of functional sarcoplasmic reticulum in the developing heart and its confinement to chamber myocardium. Dev Biol 223: 279-290, 2000.
33. Morita H, Fukushima-Kusano K, Nagase S, Takenaka-Morita S, Nishii N, Kakishita M, Nakamura K, Emori T, Matsubara H, Ohe T. Site-specific arrhythmogenesis in patients with Brugada syndrome. J Cardiovasc Electrophysiol 14: 373-379, 2003.
34. Morita H, Zipes DP, Fukushima-Kusano K, Nagase S, Nakamura K, Morita ST, Ohe T, Wu J. Repolarization heterogeneity in the right ventricular outflow tract: correlation with ventricular arrhythmias in Brugada patients and in an in vitro canine Brugada model. Heart Rhythm 5: 725-733, 2008.
35. Moss AJ, Kass RS. Long QT syndrome: from channels to cardiac arrhythmias. J Clin Invest 115: 2018-2024, 2005.
36. Nagase S, Kusano KF, Morita H, Fujimoto Y, Kakishita M, Nakamura K, Emori T, Matsubara H, Ohe T. Epicardial electrogram of the right ventricular outflow tract in patients with the Brugada syndrome: using the epicardial lead. J Am Coll Cardiol 39: 1992-1995, 2002.
37. Nishida K, Fujiki A, Mizumaki K, Sakabe M, Sugao M, Tsuneda T, Inoue H. Canine model of Brugada syndrome using regional epicardial cooling of the right ventricular outflow tract. J Cardiovasc Electrophysiol 15: 936-941, 2004.
38. Nolasco JB, Dahlen RW. A graphic method for the study of alternation in cardiac action potentials. J Appl Physiol 25: 191-196, 1968.
39. Osaka T, Kodama I, Tsuboi N, Toyama J, Yamada K. Effects of activation sequence and anisotropic cellular geometry on the repolarization phase of action potential of dog ventricular muscles. Circulation 76: 226-236, 1987.
40. Papadatos GA, Wallerstein PM, Head CE, Ratcliff R, Brady PA, Benndorf K, Saumarez RC, Trezise AE, Huang CL, Vandenberg JI, Colledge WH, Grace AA. Slowed conduction and ventricular tachycardia after targeted disruption of the cardiac sodium channel gene Scn5a. Proc Natl Acad Sci U S A 99: 6210-6215, 2002.
41. Pastore JM, Girouard SD, Laurita KR, Akar FG, Rosenbaum DS. Mechanism linking T-wave alternans to the genesis of cardiac fibrillation. Circulation 99: 1385-1394, 1999.
42. Pham TV, Robinson RB, Danilo P Jr, Rosen MR. Effects of gonadal steroids on gender-related differences in transmural dispersion of L-type calcium current. Cardiovasc Res 53: 752-762, 2002.
43. Postema PG, van Dessel PF, Kors JA, Linnenbank AC, van Herpen G, Ritsema van Eck HJ, van Geloven N, de Bakker JM, Wilde AA, Tan HL. Local depolarization abnormalities are the dominant pathophysiologic mechanism for type 1 electrocardiogram in brugada syndrome a study of electrocardiograms, vectorcardiograms, and body surface potential maps during ajmaline provocation. J Am Coll Cardiol 55: 789-797, 2010.
44. Postema PG, van Dessel PFHM, de Bakker JMT, Dekker LRC, Linnenbank AC, Hoogendijk MG, Coronel R, Tijssen JGP, Wilde AAM, Tan HL. Slow and discontinuous conduction conspire in Brugada Syndrome: a right ventricular mapping and stimulation study. Circ Arrhythm Electrophysiol 1: 379-386, 2008.
45. Postema PG, Wolpert C, Amin AS, Probst V, Borggrefe M, Roden DM, Priori SG, Tan HL, Hiraoka M, Brugada J, Wilde AA. Drugs and Brugada syndrome patients: review of the literature, recommendations, and an up-to-date website (www.brugadadrugs org). Heart Rhythm 6: 1335-1341, 2009.
46. Priori SG, Napolitano C, Schwartz PJ, Bloise R, Crotti L, Ronchetti E. The elusive link between LQT3 and Brugada syndrome: the role of flecainide challenge. Circulation 102: 945-947, 2000.
47. Qu Z, Garfinkel A, Chen PS, Weiss JN. Mechanisms of discordant alternans and induction of reentry in simulated cardiac tissue. Circulation 102: 1664-1670, 2000.
48. Rosenbaum DS, Jackson LE, Smith JM, Garan H, Ruskin JN, Cohen RJ. Electrical alternans and vulnerability to ventricular arrhythmias. N Engl J Med 330: 235-241, 1994.
49. Sabir IN, Li LM, Jones VJ, Goddard CA, Grace AA, Huang CL. Criteria for arrhythmogenicity in genetically-modified Langendorff-perfused murine hearts modelling the congenital long QT syndrome type 3 and the Brugada syndrome. Pflügers Arch 455: 637-651, 2008.
50. Sacher F, Probst V, Iesaka Y, Jacon P, Laborderie J, Mizon-Gerard F, Mabo P, Reuter S, Lamaison D, Takahashi Y, O'Neill MD, Garrigue S, Pierre B, Jais P, Pasquie JL, Hocini M, Salvador-Mazenq M, Nogami A, Amiel A, Defaye P, Bordachar P, Boveda S, Maury P, Klug D, Babuty D, Haissaguerre M, Mansourati J, Clementy J, Le Marec H. Outcome after implantation of a cardioverter-defibrillator in patients with Brugada syndrome: a multicenter study. Circulation 114: 2317-2324, 2006.
51. Salata JJ, Jurkiewicz NK, Jow B, Folander K, Guinosso PJ Jr, Raynor B, Swanson R, Fermini B. IK of rabbit ventricle is composed of two currents: evidence for IKs. Am J Physiol Heart Circ Physiol 271: H2477-H2489, 1996.
52. Saumarez RC, Grace AA. Paced ventricular electrogram fractionation and sudden death in hypertrophic cardiomyopathy and other non-coronary heart diseases. Cardiovasc Res 47: 11-22, 2000.
53. Stokoe KS, Balasubramaniam R, Goddard CA, Colledge WH, Grace AA, Huang CL. Effects of flecainide and quinidine on arrhythmogenic properties of Scn5a+/- murine hearts modelling the Brugada syndrome. J Physiol 581: 255-275, 2007.
54. Szentadrassy N, Banyasz T, Biro T, Szabo G, Toth BI, Magyar J, Lazar J, Varro A, Kovacs L, Nanasi PP. Apico-basal inhomogeneity in distribution of ion channels in canine and human ventricular myocardium. Cardiovasc Res 65: 851-860, 2005. (Pubitemid 40249729)
55. Tukkie R, Sogaard P, Vleugels J, de Groot IK, Wilde AA, Tan HL. Delay in right ventricular activation contributes to Brugada syndrome. Circulation 109: 1272-1277, 2004.
56. van Veen TA, Stein M, Royer A, Le Quang K, Charpentier F, Colledge WH, Huang CL, Wilders R, Grace AA, Escande D, de Bakker JM, van Rijen HV. Impaired impulse propagation in Scn5a-knockout mice: combined contribution of excitability, connexin expression, and tissue architecture in relation to aging. Circulation 112: 1927-1935, 2005.
57. Veeraraghavan R, Poelzing S. Mechanisms underlying increased right ventricular conduction sensitivity to flecainide challenge. Cardiovasc Res 77: 749-756, 2008.
58. Watanabe MA, Fenton FH, Evans SJ, Hastings HM, Karma A. Mechanisms for discordant alternans. J Cardiovasc Electrophysiol 12: 196-206, 2001.
59. Wilde AA, Coronel R. The complexity of genotype-phenotype relations associated with loss-of-function sodium channel mutations and the role of in silico studies. Am J Physiol Heart Circ Physiol 295: H8-H9, 2008.
60. Wilson LD, Rosenbaum DS. Mechanisms of arrythmogenic cardiac alternans. Europace 9, Suppl 6: vi77-vi82, 2007.
61. Yan GX, Antzelevitch C. Cellular basis for the Brugada syndrome and other mechanisms of arrhythmogenesis associated with ST-segment elevation. Circulation 100: 1660-1666, 1999.
62. Zaffran S, Kelly RG, Meilhac SM, Buckingham ME, Brown NA. Right ventricular myocardium derives from the anterior heart field. Circ Res 95: 261-268, 2004.
63. Zubair I, Pollard AE, Spitzer KW, Burgess MJ. Effects of activation sequence on the spatial distribution of repolarization properties. J Electrocardiol 27: 115-127, 1994.