Subepicardial phase 0 block and discontinuous transmural conduction underlie right precordial ST-segment elevation by a SCN5A loss-of-function mutation

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 295, Issue 1, 2008, Pages

  Bébarová, Markéta ^a   O'Hara, Tom ^b   Geelen, Jan L M C ^a   Jongbloed, Roselie J ^a   Timmermans, Carl ^a   Arens, Yvonne H ^a   Rodriguez, Luz Maria ^a   Rudy, Yoram ^b   Volders, Paul G A ^a,c  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b WASHINGTON UNIVERSITY   (United States)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Arrhythmia (mechanisms); Computer modeling; Conduction (block); Electrocardiogram; Sodium channel

Indexed keywords

PROTEIN SCN5A; SODIUM CHANNEL; UNCLASSIFIED DRUG; CALCIUM; CALCIUM CHANNEL L TYPE; MUSCLE PROTEIN; SCN5A PROTEIN, HUMAN; SODIUM;

ADULT; ANAMNESIS; ANIMAL CELL; ARTICLE; BRUGADA SYNDROME; CLINICAL FEATURE; COMPUTER PROGRAM; CONTROLLED STUDY; ELECTROCARDIOGRAPHY; ELECTROPHYSIOLOGY; EPICARDIUM; HEART MUSCLE; HUMAN; MALE; MISSENSE MUTATION; MUSCLE EXCITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIMULATION; ST SEGMENT ELEVATION; SYNCOPE; T WAVE INVERSION; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; CASE REPORT; CHO CELL; COMPUTER SIMULATION; CRICETULUS; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; HAMSTER; HEART VENTRICLE; METABOLISM; PATCH CLAMP; PATHOPHYSIOLOGY; PERICARDIUM; SITE DIRECTED MUTAGENESIS; TIME;

ACTION POTENTIALS; ADULT; ANIMALS; BRUGADA SYNDROME; CALCIUM; CALCIUM CHANNELS, L-TYPE; CHO CELLS; COMPUTER SIMULATION; CRICETINAE; CRICETULUS; ELECTROCARDIOGRAPHY; GENETIC PREDISPOSITION TO DISEASE; HEART VENTRICLES; HUMANS; MALE; MODELS, CARDIOVASCULAR; MUSCLE PROTEINS; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; MYOCARDIUM; PATCH-CLAMP TECHNIQUES; PERICARDIUM; SODIUM; SODIUM CHANNELS; TIME FACTORS; TRANSFECTION;

EID: 49849100915     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.91495.2007     Document Type: Article

References (48)

1. Ackerman MJ, Splawski I, Makielski JC, Tester DJ, Will ML, Timothy KW, Keating MT, Jones G, Chadha M, Burrow CR, Stephens JC, Xu C, Judson R, Curran ME. Spectrum and prevalence of cardiac sodium channel variants among black, white, Asian, and Hispanic individuals: implications for arrhythmogenic susceptibility and Brugada/long QT syndrome genetic testing. Heart Rhythm 1: 600-607, 2004.
2. Albert CM, Nam EG, Rimm EB, Jin HW, Hajjar RJ, Hunter DJ, MacRae CA, Ellinor PT. Cardiac sodium channel gene variants and sudden cardiac death in women. Circulation 117: 16-23, 2008.
3. Antzelevitch C. Late potentials and the Brugada syndrome. J Am Coll Cardiol 39: 1996-1999, 2002.
4. Antzelevitch C, Brugada P, Borggrefe M, Brugada J, Brugada R, Corrado D, Gussak I, LeMarec H, Nademanee K, Perez Riera AR, Shimizu W, Schulze-Bahr E, Tan H, Wilde A. Brugada syndrome: report of the second consensus conference. Endorsed by the Heart Rhythm Society and the European Heart Rhythm Association. Circulation 111: 659-670, 2005.
5. Antzelevitch C, Sicouri S, Litovsky SH, Lukas A, Krishnan SC, Di Diego JM, Gintant GA, Liu DW. Heterogeneity within the ventricular wall: electrophysiology and pharmacology of epicardial, endocardial, and M cells. Circ Res 69: 1427-1449, 1991.
6. Baroudi G, Chahine M. Biophysical phenotypes of SCN5A mutations causing long QT and Brugada syndromes. FEBS Lett 487: 224-228, 2000.
7. + channel mutation causing both long-QT and Brugada syndromes. Circ Res 85: 1206-1213, 1999.
8. Bezzina CR, Rook MB, Groenewegen WA, Herfst LJ, van der Wal AC, Lam J, Jongsma HJ, Wilde AAM, Mannens MMAM. Compound heterozygosity for mutations (W156X and R225W) in SCN5A associated with severe cardiac conduction disturbances and degenerative changes in the conduction system. Circ Res 92: 159-168, 2003.
9. Bezzina CR, Shimizu W, Yang P, Koopmann TT, Tanck MWT, Miyamoto Y, Kamakura S, Roden DM, Wilde AAM. Common sodium channel promoter haplotype in Asian subjects underlies variability in cardiac conduction. Circulation 113: 338-344, 2006.
10. Brugada P, Brugada J. Right bundle branch block, persistent ST segment elevation and sudden cardiac death: a distinct clinical and electrocardiographic syndrome. A multicenter report. J Am Coll Cardiol 20: 1391-1396, 1992.
11. Chen Q, Kirsch GE, Zhang D, Brugada R, Brugada J, Brugada P, Potenza D, Moya A, Borggrefe M, Breithardt G, Ortiz-Lopez R, Wang Z, Antzelevitch C, O'Brien RE, Schulze-Bahr E, Keating MT, Towbin JA, Wang Q. Genetic basis and molecular mechanism for idiopathic ventricular fibrillation. Nature 392: 293-296, 1998.
12. Clancy CE, Rudy Y. Linking a genetic defect to its cellular phenotype in a cardiac arrhythmia. Nature 400: 566-569, 1999.
13. + channel mutation that causes both Brugada and long-QT syndrome phenotypes: a simulation study of mechanism. Circulation 105: 1208-1213, 2002.
14. + channel C terminus: evidence for a role of helical structures in modulation of channel inactivation. J Biol Chem 277: 9233-9241, 2002.
15. Coronel R, Casini S, Koopmann TT, Wilms-Schopman FJG, Verkerk AO, de Groot JR, Bhuiyan Z, Bezzina CR, Veldkamp MW, Linnenbank AC, van der Wal AC, Tan HL, Brugada P, Wilde AAM, de Bakker JMT. 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.
16. Dumaine R, Towbin JA, Brugada P, Vatta M, Nesterenko DV, Nesterenko VV, Brugada J, Brugada R, Antzelevitch C. Ionic mechanisms responsible for the electrocardiographic phenotype of the Brugada syndrome are temperature dependent. Circ Res 85: 803-809, 1999.
17. i overloaded cardiac myocytes: a simulation study. Biophys J 78: 2392-2404, 2000.
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.
19. Gima K, Rudy Y. Ionic current basis of electrocardiographic waveforms: a model study. Circ Res 90: 889-896, 2002.
20. Hong K, Guerchicoff A, Pollevick GD, Oliva A, Dumaine R, de Zutter M, Burashnikov E, Wu YS, Brugada J, Brugada P, Brugada R. Cryptic 5́ splice site activation in SCN5A associated with Brugada syndrome. J Mol Cell Cardiol 38: 555-560, 2005.
21. Hough PD, Kolda TG, Torczon VJ. Asynchronous parallel pattern search for nonlinear optimization. SIAM J Sci Comput 23: 134-156, 2001.
22. Joyner RW, Kumar R, Wilders R, Jongsma HJ, Verheijck EE, Golod DA, van Ginneken ACG, Wagner MB, Goolsby WN. Modulating L-type calcium current affects discontinuous cardiac action potential conduction. Biophys J 71: 237-245, 1996.
23. Kasanuki H, Ohnishi S, Ohtuka M, Matsuda N, Nirei T, Isogai R, Shoda M, Toyoshima Y, Hosoda S. Idiopathic ventricular fibrillation induced with vagal activity in patients without obvious heart disease. Circulation 95: 2277-2285, 1997.
24. Kleber AG, Fast VG, Kucera J, Rohr S. [Physiology and pathophysiology of cardiac impulse conduction]. Z Kardiol 85, Suppl 6: 25-33, 1996.
25. Kucera JP, Kleber AG, Rohr S. Slow conduction in cardiac tissue. II. Effects of branching tissue geometry. Circ Res 83: 795-805, 1998.
26. Kyndt F, Probst V, Potet F, Demolombe S, Chevallier JC, Baro I, Moisan JP, Boisseau P, Schott JJ, Escande D, Le Marec H. Novel SCN5A mutation leading either to isolated cardiac conduction defect or Brugada syndrome in a large French family. Circulation 104: 3081-3086, 2001.
27. to1 in myocytes isolated from the human right ventricle. Am J Physiol Heart Circ Physiol 275: H369-H377, 1998.
28. Li GR, Lau CP, Ducharme A, Tardif JC, Nattel S. Transmural action potential and ionic current remodeling in ventricles of failing canine hearts. Am J Physiol Heart Circ Physiol 283: H1031-H1041, 2002.
29. Litovsky SH, Antzelevitch C. Transient outward current prominent in canine ventricular epicardium but not endocardium. Circ Res 62: 116-126, 1988.
30. Liu DW, Gintant GA, Antzelevitch C. Ionic bases for electrophysiological distinctions among epicardial, midmyocardial, and endocardial myocytes from the free wall of the canine left ventricle. Circ Res 72: 671-687, 1993.
31. Mantegazza M, Yu FH, Catterall WA, Scheuer T. Role of the C-terminal domain in inactivation of brain and cardiac sodium channels. Proc Natl Acad Sci USA 98: 15348-15353, 2001.
32. Maron BJ, Towbin JA, Thiene G, Antzelevitch C, Corrado D, Arnett D, Moss AJ, Seidman CE, Young JB. Contemporary definitions and classification of the cardiomyopathies: an American Heart Association Scientific Statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention. Circulation 113: 1807-1816, 2006.
33. Matsuo K, Kurita T, Inagaki M, Kakishita M, Aihara N, Shimizu W, Taguchi A, Suyama K, Kamakura S, Shimomura K. The circadian pattern of the development of ventricular fibrillation in patients with Brugada syndrome. Eur Heart J 20: 465-470, 1999.
34. Meregalli PG, Wilde AA, Tan HL. Pathophysiological mechanisms of Brugada syndrome: depolarization disorder, repolarization disorder, or more? Cardiovasc Res 67: 367-378, 2005.
35. Mizumaki K, Fujiki A, Tsuneda T, Sakabe M, Nishida K, Sugao M, Inoue H. Vagal activity modulates spontaneous augmentation of ST elevation in the daily life of patients with Brugada syndrome. J Cardiovasc Electrophysiol 15: 667-673, 2004.
36. + channels. Am J Physiol Heart Circ Physiol 275: H2016-H2024, 1998.
37. Nelder JA, Meade R. A simplex method for function minimization. Computer Journal 7: 313, 1965.
38. Proclemer A, Facchin D, Feruglio GA, Nucifora R. [Recurrent ventricular fibrillation, right bundle-branch block and persistent ST segment elevation in V1-V3: a new arrhythmia syndrome? A clinical case report.] G Ital Cardiol 23: 1211-1218, 1993.
39. Rivolta I, Abriel H, Tateyama M, Liu H, Memmi M, Vardas P, Napolitano C, Priori SG, Kass RS. Inherited Brugada and long QT-3 syndrome mutations of a single residue of the cardiac sodium channel confer distinct channel and clinical phenotypes. J Biol Chem 276: 30623-30630, 2001.
40. Rossenbacker T, Schollen E, Kuipéri C, de Ravel TJL, Devriendt K, Matthijs G, Collen D, Heidbüchel H, Carmeliet P. Unconventional intronic splice site mutation in SCN5A associates with cardiac sodium channelopathy. J Med Genet 42: e29, 2005.
41. Shaw RM, Rudy Y. Ionic mechanisms of propagation in cardiac tissue: roles of the sodium and L-type calcium currents during reduced excitability and decreased gap junction coupling. Circ Res 81: 727-741, 1997.
42. Smits JP, Eckardt L, Probst V, Bezzina CR, Schott JJ, Remme CA, Haverkamp W, Breithardt G, Escande D, Schulze-Bahr E, LeMarec H, Wilde AA. Genotype-phenotype relationship in Brugada syndrome: electrocardiographic features differentiate SCN5A-related patients from non-SCN5A-related patients. J Am Coll Cardiol 40: 350-356, 2002.
43. Vatta M, Dumaine R, Varghese G, Richard TA, Shimizu W, Aihara N, Nademanee K, Brugada R, Brugada J, Veerakul G, Li H, Bowles NE, Brugada P, Antzelevitch C, Towbin JA. Genetic and biophysical basis of sudden unexplained nocturnal death syndrome (SUNDS), a disease allelic to Brugada syndrome. Hum Mol Genet 11: 337-345, 2002.
44. + channel. Circ Res 86: e91-e97, 2000.
45. Ks heterogeneity on action potential duration and its rate dependence: a simulation study. Circulation 99: 2466-2474, 1999.
46. Wang DW, Desai RR, Crotti L, Arnestad M, Insolia R, Pedrazzini M, Ferrandi C, Vege A, Rognum T, Schwartz PJ, George AL Jr. Cardiac sodium channel dysfunction in sudden infant death syndrome. Circulation 115: 368-376, 2007.
47. Wang Y, Rudy Y. Action potential propagation in inhomogeneous cardiac tissue: safety factor considerations and ionic mechanism. Am J Physiol Heart Circ Physiol 278: H1019-H1029, 2000.
48. Yang XC, Zhou P, Li CL. Electrical heterogeneity of canine right ventricular transient outward potassium currents. Chin Med J (Engl) 117: 528-531, 2004.