Combined reduction of intercellular coupling and membrane excitability differentially affects transverse and longitudinal cardiac conduction

Cardiovascular Research

Volumn 83, Issue 1, 2009, Pages 52-60

  Stein, Mra ^a   Van Veen, Toon A B ^a   Remme, Carol Ann ^c   Boulaksil, Mohamed ^a,b   Noorman, Maartje ^a   Van Stuijvenberg, Leonie ^a   Van Der Nagel, Roel ^a   Bezzina, Connie R ^c   Hauer, Richard N W ^a   De Bakker, Jacques M T ^a,b,c   Van Rijen, Harold V M ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

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

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Electrical coupling; Excitability; Gap junction; Impulse conduction

Indexed keywords

COLLAGEN; CONNEXIN 43; SODIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARRHYTHMOGENESIS; ARTICLE; CONTROLLED STUDY; EPICARDIUM MAPPING; FEMALE; HEART ARRHYTHMIA; HEART CONDUCTION; HEART LEFT VENTRICLE; HEART MUSCLE FIBER MEMBRANE; HEART RIGHT VENTRICLE; HETEROZYGOTE; IMMUNOHISTOLOGY; ISOLATED HEART; MALE; MEMBRANE DEPOLARIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; QRS COMPLEX; QT INTERVAL;

ANIMALS; ARRHYTHMIAS, CARDIAC; CELL MEMBRANE; CONNEXIN 43; DISEASE MODELS, ANIMAL; ELECTROCARDIOGRAPHY; ELECTROPHYSIOLOGIC TECHNIQUES, CARDIAC; FEMALE; HEART CONDUCTION SYSTEM; HEART VENTRICLES; INTERCELLULAR JUNCTIONS; MALE; MICE; MICE, TRANSGENIC; SODIUM CHANNELS;

EID: 67649331915     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp124     Document Type: Article

References (48)

1. Kleber AG, Rudy Y. Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 2004;84:431-488.
2. Wiegerinck RF, Verkerk AO, Belterman CN, van Veen TA, Baartscheer A, Opthof Tet al. Larger cell size in rabbits with heart failure increases myocardial conduction velocity and QRS duration. Circulation 2006;113:806-813.
3. Vetter FJ, Simons SB, Mironov S, Hyatt CJ, Pertsov AM. Epicardial fiber organization in swine right ventricle and its impact on propagation. Circ Res 2005;96:244-251.
4. van Veen TA, Stein M, Royer A, Le Quang K, Charpentier F, Colledge WH et al. Impaired impulse propagation in Scn5a-knockout mice. Combined contribution of excitability, connexin expression, and tissue architecture in relation to aging. Circulation 2005;112:1927-1935.
5. Stein M, Noorman M, van Veen TA, Herold E, Engelen MA, Boulaksil M et al. Dominant arrhythmia vulnerability of the right ventricle in senescent mice. Heart Rhythm 2008;5:438-448.
6. Ufret-Vincenty CA, Baro DJ, Lederer WJ, Rockman HA, Quinones LE, Santana LF. Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J Biol Chem 2001;21:21.
7. Borlak J, Thum T. Hallmarks of ion channel gene expression in end-stage heart failure. FASEB J 2003;17:1592-1608.
8. Valdivia CR, Chu WW, Pu J, Foell JD, Haworth RA, Wolff MR et al. Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. J Mol Cell Cardiol 2005;38:475-483.
9. Peters NS. New insights into myocardial arrhythmogenesis: distribution of gap junctional coupling in normal ischemic and hypertrophied human hearts. Clin Sci 1996;90:447-452.
10. Kaprielian RR, Gunning M, Dupont E, Sheppard MN, Rothery SM, Underwood R et al. Downregulation of immunodetectable connexin43 and decreased gap junction size in the pathogenesis of chronic hibernation in the human left ventricle. Circulation 1998;97:651-660.
11. Peters NS, Coromilas J, Severs NJ, Wit AL. Disturbed Connexin43 gap junction distribution correlates with the location of reentrant circuits in the epicardial border zone of healing canine infarcts that cause ventricular tachycardia. Circulation 1997;95:988-996.
12. Yamada KA, Rogers JG, Sundset R, Steinberg TH, Saffitz JE. Up-regulation of connexin45 in heart failure. J Cardiovasc Electrophysiol 2003;14:1205-1212.
13. Kostin S, Rieger M, Dammer S, Hein S, Richter M, Klovekorn WP et al. Gap junction remodeling and altered connexin43 expression in the failing human heart. Mol Cell Biochem 2003;242:135-144.
14. Kostin S, Dammer S, Hein S, Klovekorn WP, Bauer EP, Schaper J. Connexin 43 expression and distribution in compensated and decompensated cardiac hypertrophy in patients with aortic stenosis. Cardiovasc Res 2004;62:426-436.
15. La Vecchia L, Ometto R, Bedogni F, Finocchi G, Mosele GM, Bozzola L et al. Ventricular late potentials, interstitial fibrosis, and right ventricular function in patients with ventricular tachycardia and normal left ventricular function. Am J Cardiol 1998;81:790-792.
16. Swynghedauw B. Molecular mechanisms of myocardial remodeling. Physiol Rev 1999;79:215-262.
17. Kawara T, Derksen R, de Groot JR, Coronel R, Tasseron S, Linnenbank AC et al. Activation delay after premature stimulation in chronically diseased human myocardium relates to the architecture of interstitial fibrosis. Circulation 2001;104:3069-3075.
18. Spach MS, Miller WT III, Geselowitz DB, Barr RC, Kootsey JM, Johnson EA. The discontinuous nature of propagation in normal canine cardiac muscle: evidence for recurrent discontinuities of intracellular resistance that affect the membrane currents. Circ Res 1981;48:39-54.
19. Delmar M, Michaels DC, Johnson T, Jalife J. Effects of increasing intercellular resistance on transverse and longitudinal propagation in sheep epicardial muscle. Circ Res 1987;60:780-785.
20. Spach MS, Dolber PC, Heidlage JF, Kootsey JM, Johnson EA. Propagating depolarization in anisotropic human and canine cardiac muscle: apparent directional differences in membrane capacitance. A simplified model for selective directional effects of modifying the sodium conductance on Vmax, tau foot, and the propagation safety factor. Circ Res 1987;60:206-219.
21. Spach MS, Heidlage JF, Dolber PC, Barr RC. Electrophysiological effects of remodeling cardiac gap junctions and cell size. Experimental and model studies of normal cardiac growth. Circ Res 2000;86:302-311.
22. Shaw RM, Rudy Y. Electrophysiologic effects of acute myocardial ischemia: a mechanistic investigation of action potential conduction and conduction failure. Circ Res 1997;80:124-138.
23. Bastiaanse EM, Jongsma HJ, van der Laarse A, Takens-Kwak BR. Heptanol-induced decrease in cardiac gap junctional conductance is mediated by a decrease in the fluidity of membranous cholesterol-rich domains. J Membr Biol 1993;136:135-145.
24. Takens-Kwak BR, Jongsma HJ, Rook MB, Van Ginneken AC. Mechanism of heptanol-induced uncoupling of cardiac gap junctions: a perforated patch-clamp study. Am J Physiol 1992;262:C1531-C1538.
25. Remme CA, Verkerk AO, Nuyens D, van Ginneken AC, van Brunschot S, Belterman CN et al. Overlap syndrome of cardiac sodium channel disease in mice carrying the equivalent mutation of human SCN5A-1795insD. Circulation 2006;114:2584-2594.
26. van Rijen HVM, Eckardt D, Degen J, Theis M, Ott T, Willecke K et al. Slow conduction and enhanced anisotropy increase the propensity for ventricular tachyarrhythmias in adult mice with induced deletion of connexin43. Circulation 2004;109:1048-1055.
27. Morley GE, Vaidya D, Samie FH, Lo C, Delmar M, Jalife J. Characterization of conduction in the ventricles of normal and heterozygous Cx43 knockout mice using optical mapping. J Cardiovasc Electrophysiol 1999;10:1361- 1375.
28. Danik SB, Liu F, Zhang J, Suk HJ, Morley GE, Fishman GI et al. Modulation of cardiac gap junction expression and arrhythmic susceptibility. Circ Res 2004;95:1035-1041.
29. Spach MS. Discontinuous cardiac conduction: its origin in cellular connectivity with long-term adaptive changes that cause arrhythmias. In: Spooner PM, Joyner RW, Jalife J eds. Discontinuous Conduction in the Heart. Armonk, NY: Futura Publishing Company Inc.; 1997.
30. van Rijen HV, de Bakker JM. Penetrance of monogenetic cardiac conduction diseases. A matter of conduction reserve? Cardiovasc Res 2007;76:379-380.
31. van Rijen HV, van Veen TA, Gros D, Wilders R, de Bakker JM. Connexins and cardiac arrhythmias. Adv Cardiol 2006;42:150-160.
32. Stein M, Boulaksil M, Engelen MA, van Veen TA, Hauer RNW, de Bakker JM et al. Conduction reserve and arrhythmias. Neth Heart J 2006;14:113-116.
33. Eckardt D, Theis M, Degen J, Ott T, van Rijen HV, Kirchhoff S et al. Functional role of connexin43 gap junction channels in adult mouse heart assessed by inducible gene deletion. J Mol Cell Cardiol 2004;36:101-110.
34. Royer A, van Veen TA, Le Bouter S, Marionneau C, Griol-Charhbili V, Leoni AL et al. Mouse model of SCN5A-linked hereditary Lenegre's disease: age-related conduction slowing and myocardial fibrosis. Circulation 2005;111:1738-1746.
35. Wiechert S, El-Armouche A, Rau T, Zimmermann WH, Eschenhagen T. 24-h Langendorff-perfused neonatal rat heart used to study the impact of adenoviral gene transfer. Am J Physiol Heart Circ Physiol 2003;285:H907-H914.
36. Potse M, Linnenbank A, Grimbergen C. Software design for analysis of multichannel intracardial and body surface electrocardiograms. Comput Methods Programs Biomed 2002;69:225.
37. Lammers WJ, Schalij MJ, Kirchhof CJ, Allessie MA. Quantification of spatial inhomogeneity in conduction and initiation of reentrant atrial arrhythmias. Am J Physiol 1990;259:H1254-H1263.
38. van Veen AAB, Van Rijen HVM, Wiegerinck RF, Opthof T, Colbert MC, Clement S et al. Remodeling of gap junctions in mouse hearts hypertrophied by forced retinoic acid signaling. J Mol Cell Cardiol 2002;34:1411- 1423.
39. Baba S, Dun W, Cabo C, Boyden PA. Remodeling in cells from different regions of the reentrant circuit during ventricular tachycardia. Circulation 2005;112:2386-2396.
40. Maier SK, Westenbroek RE, McCormick KA, Curtis R, Scheuer T, Catterall WA. Distinct subcellular localization of different sodium channel alpha and beta subunits in single ventricular myocytes from mouse heart. Circulation 2004;109:1421-1427.
41. Maier SK, Westenbroek RE, Schenkman KA, Feigl EO, Scheuer T, Catterall WA. An unexpected role for brain-type sodium channels in coupling of cell surface depolarization to contraction in the heart. Proc Natl Acad Sci USA 2002;99:4073-4078.
42. Malhotra JD, Thyagarajan V, Chen C, Isom LL. Tyrosine-phosphorylated and nonphosphorylated sodium channel beta1 subunits are differentially localized in cardiac myocytes. J Biol Chem 2004;279:40748-40754.
43. Johnson CM, Green KG, Kanter EM, Bou-Abboud E, Saffitz JE, Yamada KA. Voltage-gated Na+ channel activity and connexin expression in Cx43-deficient cardiac myocytes (in process citation). J Cardiovasc Electrophysiol 1999;10:1390-1401.
44. van Rijen HV, de Bakker JM, van Veen TA. Hypoxia, electrical uncoupling, and conduction slowing: role of conduction reserve. Cardiovasc Res 2005;66:9-11.
45. Veeraraghavan R, Poelzing S. Mechanisms underlying increased right ventricular conduction sensitivity to flecainide challenge. Cardiovasc Res 2008;77:749-756.
46. 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 1997;81:727-741.
47. Boengler K, Heusch G, Schulz R. Connexin 43 and ischemic preconditioning: effects of age and disease. Exp Gerontol 2006;41:485-488.
48. Rohr S, Kucera JP, Fast VG, Kleber AG. Paradoxical improvement of impulse conduction in cardiac tissue by partial cellular uncoupling. Science 1997;275:841-844.