The cardiac sodium channel displays differential distribution in the conduction system and transmural heterogeneity in the murine ventricular myocardium

Basic Research in Cardiology

Volumn 104, Issue 5, 2009, Pages 511-522

  Remme, C A ^a,d   Verkerk, A O ^a   Hoogaars, W M H ^a   Aanhaanen, W T J ^a   Scicluna, B P ^a   Annink, C ^a   van den Hoff, M J B ^a   Wilde, A A M ^a   van Veen, T A B ^b   Veldkamp, M W ^a   de Bakker, J M T ^a,b,c   Christoffels, V M ^a   Bezzina, C R ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Cardiac conduction system; Cardiac sodium channel; Conduction; Immunohistochemistry; Patch clamp

Indexed keywords

MESSENGER RNA; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL NAV1.5; VOLTAGE GATED SODIUM CHANNEL TYPE 5 ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYONAL TISSUE; GENE EXPRESSION; GENETIC TRANSFECTION; HEART ATRIOVENTRICULAR NODE; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION SYSTEM; HEART MUSCLE POTENTIAL; HEART VENTRICLE WALL; HIS BUNDLE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; PATCH CLAMP; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; PURKINJE FIBER; SINUS NODE;

ACTION POTENTIALS; ANIMALS; ATRIOVENTRICULAR NODE; BUNDLE OF HIS; CELL LINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART CONDUCTION SYSTEM; HEART VENTRICLES; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE; MUSCLE PROTEINS; MYOCARDIUM; PATCH-CLAMP TECHNIQUES; PURKINJE FIBERS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SODIUM CHANNELS; TRANSFECTION;

EID: 70349667322     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-009-0012-8     Document Type: Article

References (48)

1. Antzelevitch C, Fish J (2001) Electrical heterogeneity within the ventricular wall. Basic Res Cardiol 96:517-527
2. Antzelevitch C, Yan GX, Shimizu W (1999) Transmural dispersion of repolarization and arrhythmogenicity: The Brugada syndrome versus the long QT syndrome. J Electrocardiol 32(Suppl):158-165
3. Ashamalla SM, Navarro D, Ward CA (2001) Gradient of sodium current across the left ventricular wall of adult rat hearts. J Physiol 536:439-443
4. Bébarová M, O'Hara T, Geelen JL, Jongbloed RJ, Timmermans C, Arens YH, Rodriguez LM, Rudy Y, Volders PG (2008) Subepicardial phase 0 block and discontinuous transmural conduction underlie right precordial ST-segment elevation by a SCN5A loss-of-function mutation. Am J Physiol Heart Circ Physiol 295:H48-H58
5. Benson DW, Wang DW, Dyment M, Knilans TK, Fish FA, Strieper MJ, Rhodes TH, George AL Jr (2003) Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). J Clin Invest 112:1019-1028
6. Berecki G, Wilders R, van Ginneken ACG, Verkerk AO (2006) Non-physiological holding potential affects sodium channel repriming kinetics. Biophs J 90:sUppl.1:392-Pos (abstract)
7. + channel mutation causing both long-QT and Brugada syndromes. Circ Res 85:1206-1213
8. Bruneau BG, Nemer G, Schmitt JP, Charron F, Robitaille L, Caron S, Conner DA, Gessler M, Nemer M, Seidman CE, Seidman JG (2001) A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106:709-721
9. Cascio WE (2001) Myocardial ischemia: What factors determine arrhythmogenesis? J Cardiovasc Electrophysiol 12:726-729
10. Christoffels VM, Keijser AG, Houweling AC, Clout DE, Moorman AF (2000) Patterning the embryonic heart: Identification of five mouse Iroquois homeobox genes in the developing heart. Dev Biol 224:263-274
11. Coppen SR, Kaba RA, Halliday D, Dupont E, Skepper JN, Elneil S, Severs NJ (2003) Comparison of connexin expression patterns in the developing mouse heart and human foetal heart. Mol Cell Biochem 242:121-127
12. Cordeiro JM, Mazza M, Goodrow R, Ulahannan N, Antzelevitch C, Di Diego JM (2008) Functionally distinct sodium channels in ventricular epicardial and endocardial cells contribute to a greater sensitivity of the epicardium to electrical depression. Am J Physiol Heart Circ Physiol 295:H154-H162
13. 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 (2005) 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
14. Costantini DL, Arruda EP, Agarwal P, Kim KH, Zhu Y, Zhu W, Lebel M, Cheng CW, Park CY, Pierce SA, Guerchicoff A, Pollevick GD, Chan TY, Kabir MG, Cheng SH, Husain M, Antzelevitch C, Srivastava D, Gross GJ, Hui CC, Backx PH, Bruneau BG (2005) The homeodomain transcription factor Irx5 establishes the mouse cardiac ventricular repolarization gradient. Cell 123:347-358
15. Di Diego JM, Sun Z-Q, Antzelevitch C (1996) I to and action potential notch are smaller in left vs right canine ventricular epicardium. Am J Physiol 271:H548-H561
16. Dobrzynski H, Boyett MR, Anderson RH (2007) New insights into pacemaker activity: Promoting understanding of sick sinus syndrome. Circulation 115:1921-1932
17. Domínguez JN, de la Rosa A, Navarro F, Franco D, Aránega AE (2008) Tissue distribution and subcellular localization of the cardiac sodium channel during mouse heart development. Cardiovasc Res 78:45-52
18. Gaborit N, Le Bouter S, Szuts V, Varro A, Escande D, Nattel S, Demolombe S (2007) Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J Physiol 582:675-693
19. Gros D, Jarry-Guichard T, Ten Velde I, de Maziere A, van Kempen MJ, Davoust J, Briand JP, Moorman AF, Jongsma HJ (1994) Restricted distribution of connexin40, a gap junctional protein, in mammalian heart. Circ Res 74:839-851
20. Harrell MD, Harbi S, Hoffman JF, Zavadil J, Coetzee WA (2007) Large-scale analysis of ion channel gene expression in the mouse heart during perinatal development. Physiol Genomics 28:273-283
21. Honen BN, Saint DA (2002) Heterogeneity of the properties of I Na in epicardial and endocardial cells of rat ventricle. Clin Exp Pharmacol Physiol 29:161-166
22. Hoogaars WM, Engel A, Brons JF, Verkerk AO, de Lange FJ, Wong LY, Bakker ML, Clout DE, Wakker V, Barnett P, Ravesloot JH, Moorman AF, Verheijck EE, Christoffels VM (2007) Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria. Genes Dev 21:1098-1112
23. Kleber AG, Fast V (1997) Molecular and cellular aspects of re-entrant arrhythmias. Basic Res Cardiol 92(Suppl 1):111-119
24. Koopmann TT, Bezzina CR, Wilde AAM (2006) Voltage-gated sodium channels: action players with many faces. Ann Med 38:472-482
25. Lei M, Jones SA, Liu J, Lancaster MK, Fung SS, Dobrzynski H, Camelliti P, Maier SK, Noble D, Boyett MR (2004) Requirement of neuronal- and cardiac-type sodium channels for murine sinoatrial node pacemaking. J Physiol 559(Pt 3):835-848
26. Liu DW, Antzelevitch C (1995) Characteristics of the delayed rectifier current (IKr and IKs) in canine ventricular epicardial, midmyocardial, and endocardial myocytes: A weaker IKs contributes to the longer action potential of the M cell. Circ Res 76:351-365
27. Liu DW, Gintant GA, Antzelevitch C (1993) 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
28. Maier SKG, Westenbroek RE, Yamanushi TT, Dobrzynski H, Boyett MR, Catterall WA, Scheuer T (2003) An unexpected requirement for brain-type sodium channels for control of heart rate in the mouse sinoatrial node. Proc Natl Acad Sci USA 100:3507-3512
29. Maier SKG, Westenbroek RE, McCormick KA, Curtis R, Scheuer T, Catterall WA (2004) Distinct subcellular localization of different sodium channel α and β subunits in single ventricular myocytes from mouse heart. Circulation 109:1421-1427
30. Marionneau C, Couette B, Liu J, Li H, Mangoni ME, Nargeot J, Lei M, Escande D, Demolombe S (2005) Specific pattern of ionic channel gene expression associated with pacemaker activity in the mouse heart. J Physiol 562:223-234
31. Mohler PJ, Rivolta I, Napolitano C, LeMaillet G, Lambert S, Priori SG, Bennett V (2004) Nav1.5 E1053 K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc Natl Acad Sci USA 101:17533-17538
32. Nguemo F, Sasse P, Fleischmann BK, Kamanyi A, Schunkert H, Hescheler J, Reppel M (2008) Modulation of L-type Ca(2+) channel current density and inactivation by beta-adrenergic stimulation during murine cardiac embryogenesis. Basic Res Cardiol (in press). doi: 10.1007/ s00395-008-0755-7
33. Petrecca K, Amellal F, Laird DW, Cohen SA, Shrier A (1997) Sodium channel distribution within the rabbit atrioventricular node as analysed by confocal microscopy. J Physiol 501:263-274
34. Remme CA, Verkerk AO, Nuyens D, van Ginneken AC, van Brunschot S, Belterman CN, Wilders R, van Roon MA, Tan HL, Wilde AA, Carmeliet P, de Bakker JM, Veldkamp MW, Bezzina CR (2006) Overlap syndrome of cardiac sodium channel disease in mice carrying the equivalent mutation of human SCN5A-1795insD. Circulation 114:2584-2594
35. Remme CA, Wilde AAM, Bezzina CR (2008) Cardiac sodium channel overlap syndromes: Different faces of SCN5A mutations. Trends Cardiovasc Med 18:78-87
36. Schulze-Bahr E, Eckardt L, Breithardt G, Seidl K, Wichter T, Wolpert C, Borggrefe M, Haverkamp W (2003) Sodium channel gene (SCN5A) mutations in 44 index patients with Brugada syndrome: Different incidences in familial and sporadic disease. Hum Mutat 21:651-652
37. Sheets MF, Hanck DA, Fozzard HA (1988) Nonlinear relation between V max and I Na in canine cardiac Purkinje cells. Circ Res 63:386-398
38. Smits JPP, Eckardt L, Probst V, Bezzina CR, Schott JJ, Remme CA, Haverkamp W, Breithardt G, Escande D, Schulze-Bahr E, LeMarec H, Wilde AA (2002) Genotype-phenotype relationship in Brugada syndrome: electrocardiographic features differentiate SCN5A-related patients from non-SCN5A-related patients. J Am Coll Cardiol 40:350-356
39. Smits JP, Koopmann TT, Wilders R, Veldkamp MW, Opthof T, Bhuiyan ZA, Mannens MM, Balser JR, Tan HL, Bezzina CR, Wilde AA (2005) A mutation in the human cardiac sodium channel (E161 K) contributes to sick sinus syndrome, conduction disease and Brugada syndrome in two families. J Mol Cell Cardiol 38:969-981
40. Szabó G, Szentandrássy N, Biró T, Tóth BI, Czifra G, Magyar J, Bányász T, Varró A, Kovács L, Nánási PP (2005) Asymmetrical distribution of ion channels in canine and human left-ventricular wall: epicardium versus midmyocardium. Eur J Physiol 450:307-316
41. Tomaselli GF, Zipes DP (2004) What causes sudden death in heart failure? Circ Res 95:754-763
42. Veldkamp MW, Wilders R, Baartscheer A, Zegers JG, Bezzina CR, Wilde AA (2003) Contribution of sodium channel mutations to bradycardia and sinus node dysfunction in LQT3 families. Circ Res 92:976-983
43. Wang DW, Viswanathan PC, Balser JR, George AL Jr, Benson DW (2002) Clinical, genetic, and biophysical characterization of SCN5A mutations associated with atrioventricular conduction block. Circulation 105:341-346
44. Wiegerinck RF, van Veen TAB, Belterman CN, Schumacher CA, Noorman M, de Bakker JMT, Coronel R (2008) Transmural dispersion of refractoriness and conduction velocity is associated with heterogeneously reduced connexin43 in a rabbit model of heart failure. Heart Rhythm 5:1178-1185
45. Wiegerinck RF, de Bakker JMT, Opthof T, de Jonge N, Kirkels H, Wilms-Schopman FJG, Coronel R (2009) The effect of enhanced gap junctional conductance on ventricular conduction in explanted hearts from patients with heart failure. Basic Res Cardiol (in press). doi: 10.1007/s00395-008-0771-7
46. Wolk R, Cobbe SM, Hicks MN, Kane KA (1999) Functional, structural, and dynamic basis of electrical heterogeneity in healthy and diseased cardiac muscle: Implications for arrhythmogenesis and anti-arrhythmic drug therapy. Pharmacol Ther 84:207-231
47. + channel isoforms at the atrioventricular junction and atrioventricular node in the rat. Circulation 114:1360-1371
48. Zygmunt AC, Eddlestone GT, Thomas GP, Nesterenko VV, Antzelevitch C (2001) Larger late sodium conductance in M cells contributes to electrical heterogeneity in canine ventricle. Am J Physiol Heart Circ Physiol 281:H689-H697