Circulation Research, Vol 71, 240-250, Copyright © 1992 by American Heart Association

ARTICLES

Persisting zones of slow impulse conduction in developing chicken hearts

F de Jong, T Opthof, AA Wilde, MJ Janse, R Charles, WH Lamers and AF Moorman
Department of Anatomy and Embryology, University of Amsterdam, The Netherlands.

We performed a correlative electrophysiological and immunohistochemical study of embryonic chicken hearts during the septational period (Hamburger and Hamilton stages 13-31 [2-7 days of incubation]). The analyses yield conclusive evidence for slow conduction, up to 7 days of development, in the outflow tract, in the atrioventricular canal, and in the sinoatrial junction. The conduction velocity remains approximately 1 cm/sec in the outflow tract and increases in the ventricle 20-fold to approximately 20 cm/sec between 2 and 7 days of development. Transmembrane potentials of myocytes in the outflow tract and atrioventricular canal slowly rise (less than 5 V/sec), whereas in the atrium and ventricle, the upstroke velocity is eightfold to 13-fold higher. In the outflow tract, repolarization is completed only after the start of the next cycle. Because of the persistence of slow conduction, the myocardium flanking the developing atria and ventricle is thought to represent segments of persisting "primary" myocardium, whereas the more rapidly conducting "working" myocardium of the ventricle and atria is thought to represent more advanced stages of myocardial differentiation. The persisting primary myocardium was characterized by a continued coexpression of both the atrial and ventricular isoforms of myosin heavy chain. The developing atria and ventricle could be demarcated morphologically from the primary myocardium because the free walls of these segments only express their respective isoforms of myosin heavy chain. The slowly conducting myocardial zones appear to be essential for the function of the embryonic heart because 1) they provide the septating heart with alternating segments of slow and relatively fast conduction necessary for consecutive contraction of the atrial and ventricular segments and 2) their sphincterlike prolonged peristaltic contraction pattern can substitute for the adult type of one-way valves that start to develop at the end of septation.

This article has been cited by other articles:

				T. Horsthuis, H. P.J. Buermans, J. F. Brons, A. O. Verkerk, M. L. Bakker, V. Wakker, D. E.W. Clout, A. F.M. Moorman, P. A.C. 't Hoen, and V. M. Christoffels Gene Expression Profiling of the Forming Atrioventricular Node Using a Novel Tbx3-Based Node-Specific Transgenic Reporter Circ. Res., July 2, 2009; 105(1): 61 - 69. [Abstract] [Full Text] [PDF]

				V. M. Christoffels and A. F.M. Moorman Development of the Cardiac Conduction System: Why Are Some Regions of the Heart More Arrhythmogenic Than Others? Circ Arrhythm Electrophysiol, April 1, 2009; 2(2): 195 - 207. [Full Text] [PDF]

				B. J.D. Boukens, V. M. Christoffels, R. Coronel, and A. F.M. Moorman Developmental Basis for Electrophysiological Heterogeneity in the Ventricular and Outflow Tract Myocardium As a Substrate for Life-Threatening Ventricular Arrhythmias Circ. Res., January 2, 2009; 104(1): 19 - 31. [Abstract] [Full Text] [PDF]

				S. Y. Ho Accessory Atrioventricular Pathways: Getting to the Origins Circulation, March 25, 2008; 117(12): 1502 - 1504. [Full Text] [PDF]

				N. C. Chi, R. M. Shaw, S. De Val, G. Kang, L. Y. Jan, B. L. Black, and D. Y.R. Stainier Foxn4 directly regulates tbx2b expression and atrioventricular canal formation Genes & Dev., March 15, 2008; 22(6): 734 - 739. [Abstract] [Full Text] [PDF]

				B. B. Keller New Insights Into the Developmental Biomechanics of the Atrioventricular Valves Circ. Res., May 25, 2007; 100(10): 1399 - 1401. [Full Text] [PDF]

				J. T. Butcher, T. C. McQuinn, D. Sedmera, D. Turner, and R. R. Markwald Transitions in Early Embryonic Atrioventricular Valvular Function Correspond With Changes in Cushion Biomechanics That Are Predictable by Tissue Composition Circ. Res., May 25, 2007; 100(10): 1503 - 1511. [Abstract] [Full Text] [PDF]

				A. Gurjarpadhye, K. W. Hewett, C. Justus, X. Wen, H. Stadt, M. L. Kirby, D. Sedmera, and R. G. Gourdie Cardiac neural crest ablation inhibits compaction and electrical function of conduction system bundles Am J Physiol Heart Circ Physiol, March 1, 2007; 292(3): H1291 - H1300. [Abstract] [Full Text] [PDF]

				D. P. Kolditz, M. C.E.F. Wijffels, N. A. Blom, A. van der Laarse, R. R. Markwald, M. J. Schalij, and A. C. Gittenberger-de Groot Persistence of Functional Atrioventricular Accessory Pathways in Postseptated Embryonic Avian Hearts: Implications for Morphogenesis and Functional Maturation of the Cardiac Conduction System Circulation, January 2, 2007; 115(1): 17 - 26. [Abstract] [Full Text] [PDF]

				J. B. Rutenberg, A. Fischer, H. Jia, M. Gessler, T. P. Zhong, and M. Mercola Developmental patterning of the cardiac atrioventricular canal by Notch and Hairy-related transcription factors Development, November 1, 2006; 133(21): 4381 - 4390. [Abstract] [Full Text] [PDF]

				Y. N. Tallini, M. Ohkura, B.-R. Choi, G. Ji, K. Imoto, R. Doran, J. Lee, P. Plan, J. Wilson, H.-B. Xin, et al. Imaging cellular signals in the heart in vivo: Cardiac expression of the high-signal Ca2+ indicator GCaMP2 PNAS, March 21, 2006; 103(12): 4753 - 4758. [Abstract] [Full Text] [PDF]

				D. J. Milan, A. C. Giokas, F. C. Serluca, R. T. Peterson, and C. A. MacRae Notch1b and neuregulin are required for specification of central cardiac conduction tissue Development, March 15, 2006; 133(6): 1125 - 1132. [Abstract] [Full Text] [PDF]

				D. Sedmera Form follows function: developmental and physiological view on ventricular myocardial architecture Eur. J. Cardiothorac. Surg., October 1, 2005; 28(4): 526 - 528. [Abstract] [Full Text] [PDF]

				P. G. Meregalli, A. A.M. Wilde, and H. L. Tan Pathophysiological mechanisms of Brugada syndrome: Depolarization disorder, repolarization disorder, or more? Cardiovasc Res, August 15, 2005; 67(3): 367 - 378. [Abstract] [Full Text] [PDF]

				J Boullin and J M Morgan The development of cardiac rhythm Heart, July 1, 2005; 91(7): 874 - 875. [Full Text] [PDF]

				J. L. Lucitti, K. Tobita, and B. B. Keller Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo J. Exp. Biol., May 15, 2005; 208(10): 1877 - 1885. [Abstract] [Full Text] [PDF]

				C.-L. Cai, W. Zhou, L. Yang, L. Bu, Y. Qyang, X. Zhang, X. Li, M. G. Rosenfeld, J. Chen, and S. Evans T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis Development, May 15, 2005; 132(10): 2475 - 2487. [Abstract] [Full Text] [PDF]

				J. N. Dominguez, F. Navarro, D. Franco, R. P. Thompson, and A. E. Aranega Temporal and spatial expression pattern of {beta}1 sodium channel subunit during heart development Cardiovasc Res, March 1, 2005; 65(4): 842 - 850. [Abstract] [Full Text] [PDF]

				F. Rothenberg, V. P. Nikolski, M. Watanabe, and I. R. Efimov Electrophysiology and anatomy of embryonic rabbit hearts before and after septation Am J Physiol Heart Circ Physiol, January 1, 2005; 288(1): H344 - H351. [Abstract] [Full Text] [PDF]

				W. M.H Hoogaars, A. Tessari, A. F.M Moorman, P. A.J de Boer, J. Hagoort, A. T Soufan, M. Campione, and V. M Christoffels The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart Cardiovasc Res, June 1, 2004; 62(3): 489 - 499. [Abstract] [Full Text] [PDF]

				C. E. Hall, R. Hurtado, K. W. Hewett, M. Shulimovich, C. P. Poma, M. Reckova, C. Justus, D. J. Pennisi, K. Tobita, D. Sedmera, et al. Hemodynamic-dependent patterning of endothelin converting enzyme 1 expression and differentiation of impulse-conducting Purkinje fibers in the embryonic heart Development, February 1, 2004; 131(3): 581 - 592. [Abstract] [Full Text] [PDF]

				T. Hochgreb, V. L. Linhares, D. C. Menezes, A. C. Sampaio, C. Y. I. Yan, W. V. Cardoso, N. Rosenthal, and J. Xavier-Neto A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field Development, November 15, 2003; 130(22): 5363 - 5374. [Abstract] [Full Text] [PDF]

				A. F. M. MOORMAN and V. M. CHRISTOFFELS Cardiac Chamber Formation: Development, Genes, and Evolution Physiol Rev, October 1, 2003; 83(4): 1223 - 1267. [Abstract] [Full Text] [PDF]

				M. Reckova, C. Rosengarten, A. deAlmeida, C. P. Stanley, A. Wessels, R. G. Gourdie, R. P. Thompson, and D. Sedmera Hemodynamics Is a Key Epigenetic Factor in Development of the Cardiac Conduction System Circ. Res., July 11, 2003; 93(1): 77 - 85. [Abstract] [Full Text] [PDF]

				A. Rosa, J.-P. Maury, J. Terrand, X. Lyon, P. Kucera, L. Kappenberger, and E. Raddatz Ectopic pacing at physiological rate improves postanoxic recovery of the developing heart Am J Physiol Heart Circ Physiol, June 1, 2003; 284(6): H2384 - H2392. [Abstract] [Full Text] [PDF]

				A. C. Fijnvandraat, R. H. Lekanne Deprez, and A. F.M. Moorman Development of heart muscle-cell diversity: a help or a hindrance for phenotyping embryonic stem cell-derived cardiomyocytes Cardiovasc Res, May 1, 2003; 58(2): 303 - 312. [Abstract] [Full Text] [PDF]

				W. H. Lamers and A. F.M. Moorman Cardiac Septation: A Late Contribution of the Embryonic Primary Myocardium to Heart Morphogenesis Circ. Res., July 26, 2002; 91(2): 93 - 103. [Abstract] [Full Text] [PDF]

				P. E.M.H. Habets, A. F.M. Moorman, D. E.W. Clout, M. A. van Roon, M. Lingbeek, M. van Lohuizen, M. Campione, and V. M. Christoffels Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation Genes & Dev., May 15, 2002; 16(10): 1234 - 1246. [Abstract] [Full Text] [PDF]

				S. RENTSCHLER, G.E. MORLEY, and G.I. FISHMAN Molecular and Functional Maturation of the Murine Cardiac Conduction System Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 353 - 362. [Abstract] [PDF]

				D. Franco, S. Demolombe, S. Kupershmidt, R. Dumaine, J. N Dominguez, D. Roden, C. Antzelevitch, D. Escande, and A. F.M Moorman Divergent expression of delayed rectifier K+ channel subunits during mouse heart development Cardiovasc Res, October 1, 2001; 52(1): 65 - 75. [Abstract] [Full Text] [PDF]

				A. W. Cates, W. M. Smith, R. E. Ideker, and A. E. Pollard Purkinje and ventricular contributions to endocardial activation sequence in perfused rabbit right ventricle Am J Physiol Heart Circ Physiol, August 1, 2001; 281(2): H490 - H505. [Abstract] [Full Text] [PDF]

				K. Yasui, W. Liu, T. Opthof, K. Kada, J.-K. Lee, K. Kamiya, and I. Kodama If Current and Spontaneous Activity in Mouse Embryonic Ventricular Myocytes Circ. Res., March 16, 2001; 88(5): 536 - 542. [Abstract] [Full Text] [PDF]

				J.-S. Kim, S. Viragh, A. F. M. Moorman, R. H. Anderson, and W. H. Lamers Development of the Myocardium of the Atrioventricular Canal and the Vestibular Spine in the Human Heart Circ. Res., March 2, 2001; 88(4): 395 - 402. [Abstract] [Full Text] [PDF]

				D. Franco and J. M. Icardo Molecular characterization of the ventricular conduction system in the developing mouse heart: topographical correlation in normal and congenitally malformed hearts Cardiovasc Res, February 1, 2001; 49(2): 417 - 429. [Abstract] [Full Text] [PDF]

				S Rentschler, D. Vaidya, H Tamaddon, K Degenhardt, D Sassoon, G. Morley, J Jalife, and G. Fishman Visualization and functional characterization of the developing murine cardiac conduction system Development, January 5, 2001; 128(10): 1785 - 1792. [Abstract] [PDF]

				S. Alcolea, M. Theveniau-Ruissy, T. Jarry-Guichard, I. Marics, E. Tzouanacou, J.-P. Chauvin, J.-P. Briand, A. F. M. Moorman, W. H. Lamers, and D. B. Gros Downregulation of Connexin 45 Gene Products During Mouse Heart Development Circ. Res., June 25, 1999; 84(12): 1365 - 1379. [Abstract] [Full Text] [PDF]

				N. A. Blom, A. C. Gittenberger-de Groot, M. C. DeRuiter, R. E. Poelmann, M. M. T. Mentink, and J. Ottenkamp Development of the Cardiac Conduction Tissue in Human Embryos Using HNK-1 Antigen Expression : Possible Relevance for Understanding of Abnormal Atrial Automaticity Circulation, February 16, 1999; 99(6): 800 - 806. [Abstract] [Full Text] [PDF]

				J Xavier-Neto, C. Neville, M. Shapiro, L Houghton, G. Wang, W Nikovits, F. Stockdale, and N Rosenthal A retinoic acid-inducible transgenic marker of sino-atrial development in the mouse heart Development, January 6, 1999; 126(12): 2677 - 2687. [Abstract] [PDF]

				J. Ya, M. W. Schilham, P. A. J. de Boer, A. F. M. Moorman, H. Clevers, and W. H. Lamers Sox4-Deficiency Syndrome in Mice Is an Animal Model for Common Trunk Circ. Res., November 16, 1998; 83(10): 986 - 994. [Abstract] [Full Text] [PDF]

				A. F.M. Moorman, F. de Jong, M. M.F.J. Denyn, and W. H. Lamers Development of the Cardiac Conduction System Circ. Res., April 6, 1998; 82(6): 629 - 644. [Full Text] [PDF]

				D. Franco, W. H Lamers, and A. F.M Moorman Patterns of expression in the developing myocardium: towards a morphologically integrated transcriptional model Cardiovasc Res, April 1, 1998; 38(1): 25 - 53. [Full Text] [PDF]

				J. Ya, M. J. B. van den Hoff, P. A. J. de Boer, S. Tesink-Taekema, D. Franco, A. F. M. Moorman, and W. H. Lamers Normal Development of the Outflow Tract in the Rat Circ. Res., March 9, 1998; 82(4): 464 - 472. [Abstract] [Full Text] [PDF]

				E. T. Chuck, D. M. Freeman, M. Watanabe, and D. S. Rosenbaum Changing Activation Sequence in the Embryonic Chick Heart : Implications for the Development of the His-Purkinje System Circ. Res., October 19, 1997; 81(4): 470 - 476. [Abstract] [Full Text]

				M. Fishman and K. Chien Fashioning the vertebrate heart: earliest embryonic decisions Development, January 6, 1997; 124(11): 2099 - 2117. [Abstract] [PDF]

				A. F. M. Moorman, J. L. M. Vermeulen, M. U. Koban, K. Schwartz, W. H. Lamers, and K. R. Boheler Patterns of Expression of Sarcoplasmic Reticulum Ca2+-ATPase and Phospholamban mRNAs During Rat Heart Development Circ. Res., April 1, 1995; 76(4): 616 - 625. [Abstract] [Full Text]

				R. Gourdie, T Mima, R. Thompson, and T Mikawa Terminal diversification of the myocyte lineage generates Purkinje fibers of the cardiac conduction system Development, January 5, 1995; 121(5): 1423 - 1431. [Abstract] [PDF]