|
|
||||||||
Experimental and Molecular Cardiology Group, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Moorman, Antoon F. M., and Vincent M. Christoffels. Cardiac Chamber Formation: Development, Genes, and Evolution. Physiol Rev 83: 1223-1267, 2003; 10.1152/physrev.00006.2003.Concepts of cardiac development have greatly influenced the description of the formation of the four-chambered vertebrate heart. Traditionally, the embryonic tubular heart is considered to be a composite of serially arranged segments representing adult cardiac compartments. Conversion of such a serial arrangement into the parallel arrangement of the mammalian heart is difficult to understand. Logical integration of the development of the cardiac conduction system into the serial concept has remained puzzling as well. Therefore, the current description needed reconsideration, and we decided to evaluate the essentialities of cardiac design, its evolutionary and embryonic development, and the molecular pathways recruited to make the four-chambered mammalian heart. The three principal notions taken into consideration are as follows. 1) Both the ancestor chordate heart and the embryonic tubular heart of higher vertebrates consist of poorly developed and poorly coupled "pacemaker-like" cardiac muscle cells with the highest pacemaker activity at the venous pole, causing unidirectional peristaltic contraction waves. 2) From this heart tube, ventricular chambers differentiate ventrally and atrial chambers dorsally. The developing chambers display high proliferative activity and consist of structurally well-developed and well-coupled muscle cells with low pacemaker activity, which permits fast conduction of the impulse and efficacious contraction. The forming chambers remain flanked by slowly proliferating pacemaker-like myocardium that is temporally prevented from differentiating into chamber myocardium. 3) The trabecular myocardium proliferates slowly, consists of structurally poorly developed, but well-coupled, cells and contributes to the ventricular conduction system. The atrial and ventricular chambers of the formed heart are activated and interconnected by derivatives of embryonic myocardium. The topographical arrangement of the distinct cardiac muscle cells in the forming heart explains the embryonic electrocardiogram (ECG), does not require the invention of nodes, and allows a logical transition from a peristaltic tubular heart to a synchronously contracting four-chambered heart. This view on the development of cardiac design unfolds fascinating possibilities for future research.
2 Reynolds number (Re) is a unitless number representative of the tendency of a liquid (or gas) to become turbulent. It is proportional to the velocity of flow and to the density, and inversely proportional to the viscosity.
Address for reprint requests and other correspondence: A. F. M. Moorman, Dept. of Anatomy & Embryology, Academic Medical Center, Meibergdreef 15, 1105 AZ Amsterdam, The Netherlands (E-mails: a.f.moorman{at}amc.uva.nl; v.m.christoffels{at}amc.uva.nl).
This article has been cited by other articles:
![]() |
R. Singh, T. Horsthuis, H. F. Farin, T. Grieskamp, J. Norden, M. Petry, V. Wakker, A. F.M. Moorman, V. M. Christoffels, and A. Kispert Tbx20 Interacts With Smads to Confine Tbx2 Expression to the Atrioventricular Canal Circ. Res., August 28, 2009; 105(5): 442 - 452. [Abstract] [Full Text] [PDF] |
||||
![]() |
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] |
||||
![]() |
W. T.J. Aanhaanen, J. F. Brons, J. N. Dominguez, M. S. Rana, J. Norden, R. Airik, V. Wakker, C. de Gier-de Vries, N. A. Brown, A. Kispert, et al. The Tbx2+ Primary Myocardium of the Atrioventricular Canal Forms the Atrioventricular Node and the Base of the Left Ventricle Circ. Res., June 5, 2009; 104(11): 1267 - 1274. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. A. DiMichele, Z. S. Hakim, R. L. Sayers, M. Rojas, R. J. Schwartz, C. P. Mack, and J. M. Taylor Transient Expression of FRNK Reveals Stage-Specific Requirement for Focal Adhesion Kinase Activity in Cardiac Growth Circ. Res., May 22, 2009; 104(10): 1201 - 1208. [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] |
||||
![]() |
G. van den Berg, R. Abu-Issa, B. A. de Boer, M. R. Hutson, P. A.J. de Boer, A. T. Soufan, J. M. Ruijter, M. L. Kirby, M. J.B. van den Hoff, and A. F.M. Moorman A Caudal Proliferating Growth Center Contributes to Both Poles of the Forming Heart Tube Circ. Res., January 30, 2009; 104(2): 179 - 188. [Abstract] [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] |
||||
![]() |
J. Krishnan, P. Ahuja, S. Bodenmann, D. Knapik, E. Perriard, W. Krek, and J.-C. Perriard Essential Role of Developmentally Activated Hypoxia-Inducible Factor 1{alpha} for Cardiac Morphogenesis and Function Circ. Res., November 7, 2008; 103(10): 1139 - 1146. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Rojas, S. W. Kong, P. Agarwal, B. Gilliss, W. T. Pu, and B. L. Black GATA4 Is a Direct Transcriptional Activator of Cyclin D2 and Cdk4 and Is Required for Cardiomyocyte Proliferation in Anterior Heart Field-Derived Myocardium Mol. Cell. Biol., September 1, 2008; 28(17): 5420 - 5431. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. T. MacDonald, S. D. Bamforth, C.-M. Chen, C. R. Farthing, A. Franklyn, C. Broadbent, J. E. Schneider, Y. Saga, M. Lewandoski, and S. Bhattacharya Epiblastic Cited2 deficiency results in cardiac phenotypic heterogeneity and provides a mechanism for haploinsufficiency Cardiovasc Res, August 1, 2008; 79(3): 448 - 457. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. E. Mangoni and J. Nargeot Genesis and Regulation of the Heart Automaticity Physiol Rev, July 1, 2008; 88(3): 919 - 982. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. L. Bakker, B. J. Boukens, M. T.M. Mommersteeg, J. F. Brons, V. Wakker, A. F.M. Moorman, and V. M. Christoffels Transcription Factor Tbx3 Is Required for the Specification of the Atrioventricular Conduction System Circ. Res., June 6, 2008; 102(11): 1340 - 1349. [Abstract] [Full Text] [PDF] |
||||
![]() |
K.-J. Boogerd, L.Y. E. Wong, V. M. Christoffels, M. Klarenbeek, J. M. Ruijter, A. F.M. Moorman, and P. Barnett Msx1 and Msx2 are functional interacting partners of T-box factors in the regulation of Connexin43 Cardiovasc Res, June 1, 2008; 78(3): 485 - 493. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Niessen and A. Karsan Notch Signaling in Cardiac Development Circ. Res., May 23, 2008; 102(10): 1169 - 1181. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Burstein, E. Libby, A. Calderone, and S. Nattel Differential Behaviors of Atrial Versus Ventricular Fibroblasts: A Potential Role for Platelet-Derived Growth Factor in Atrial-Ventricular Remodeling Differences Circulation, April 1, 2008; 117(13): 1630 - 1641. [Abstract] [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] |
||||
![]() |
A. F.M Moorman, V. M Christoffels, R. H Anderson, and M. J.B van den Hoff The heart-forming fields: one or multiple? Phil Trans R Soc B, August 29, 2007; 362(1484): 1257 - 1265. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. T Butcher and R. R Markwald Valvulogenesis: the moving target Phil Trans R Soc B, August 29, 2007; 362(1484): 1489 - 1503. [Abstract] [Full Text] [PDF] |
||||
![]() |
Z. S. Hakim, L. A. DiMichele, J. T. Doherty, J. W. Homeister, H. E. Beggs, L. F. Reichardt, R. J. Schwartz, J. Brackhan, O. Smithies, C. P. Mack, et al. Conditional Deletion of Focal Adhesion Kinase Leads to Defects in Ventricular Septation and Outflow Tract Alignment Mol. Cell. Biol., August 1, 2007; 27(15): 5352 - 5364. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. G. Holtzman, J. J. Schoenebeck, H.-J. Tsai, and D. Yelon Endocardium is necessary for cardiomyocyte movement during heart tube assembly Development, June 15, 2007; 134(12): 2379 - 2386. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. M.H. Hoogaars, A. Engel, J. F. Brons, A. O. Verkerk, F. J. de Lange, L.Y. E. Wong, M. L. Bakker, D. E. Clout, V. Wakker, P. Barnett, et al. Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria Genes & Dev., May 1, 2007; 21(9): 1098 - 1112. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. van Wijk, A. F.M. Moorman, and M. J.B. van den Hoff Role of bone morphogenetic proteins in cardiac differentiation Cardiovasc Res, May 1, 2007; 74(2): 244 - 255. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. S. Rana, N. C.A. Horsten, S. Tesink-Taekema, W. H. Lamers, A. F.M. Moorman, and M. J.B. van den Hoff Trabeculated Right Ventricular Free Wall in the Chicken Heart Forms by Ventricularization of the Myocardium Initially Forming the Outflow Tract Circ. Res., April 13, 2007; 100(7): 1000 - 1007. [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] |
||||
![]() |
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] |
||||
![]() |
K. Mesbah, A. Camus, C. Babinet, and J. Barra Mutation in the Trap{alpha}/Ssr1 Gene, Encoding Translocon-Associated Protein {alpha}, Results in Outflow Tract Morphogenetic Defects. Mol. Cell. Biol., October 1, 2006; 26(20): 7760 - 7771. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Satou and N. Satoh Gene regulatory networks for the development and evolution of the chordate heart Genes & Dev., October 1, 2006; 20(19): 2634 - 2638. [Full Text] [PDF] |
||||
![]() |
B. Davidson, W. Shi, J. Beh, L. Christiaen, and M. Levine FGF signaling delineates the cardiac progenitor field in the simple chordate, Ciona intestinalis Genes & Dev., October 1, 2006; 20(19): 2728 - 2738. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Sedmera, A. Wessels, T. C. Trusk, R. P. Thompson, K. W. Hewett, and R. G. Gourdie Changes in activation sequence of embryonic chick atria correlate with developing myocardial architecture Am J Physiol Heart Circ Physiol, October 1, 2006; 291(4): H1646 - H1652. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. N. Olson Gene regulatory networks in the evolution and development of the heart. Science, September 29, 2006; 313(5795): 1922 - 1927. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. T. Soufan, G. van den Berg, J. M. Ruijter, P. A.J. de Boer, M. J.B. van den Hoff, and A. F.M. Moorman Regionalized Sequence of Myocardial Cell Growth and Proliferation Characterizes Early Chamber Formation Circ. Res., September 1, 2006; 99(5): 545 - 552. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Somi, A. T. J. Klein, A. C. Houweling, J. M. Ruijter, A. A.M. Buffing, A. F.M. Moorman, and M. J.B. van den Hoff Atrial and Ventricular Myosin Heavy-chain Expression in the Developing Chicken Heart: Strengths and Limitations of Non-radioactive In Situ Hybridization J. Histochem. Cytochem., June 1, 2006; 54(6): 649 - 664. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. J. Kocica, A. F. Corno, F. Carreras-Costa, M. Ballester-Rodes, M. C. Moghbel, C. N.C. Cueva, V. Lackovic, V. I. Kanjuh, and F. Torrent-Guasp The helical ventricular myocardial band: global, three-dimensional, functional architecture of the ventricular myocardium Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S21 - S40. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. F. Corno, M. J. Kocica, and F. Torrent-Guasp The helical ventricular myocardial band of Torrent-Guasp: potential implications in congenital heart defects Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S61 - S68. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. C. Houweling, M. M. van Borren, A. F.M. Moorman, and V. M. Christoffels Expression and regulation of the atrial natriuretic factor encoding gene Nppa during development and disease Cardiovasc Res, September 1, 2005; 67(4): 583 - 593. [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] |
||||
![]() |
R. Fiore, B. Rahim, V. M. Christoffels, A. F. M. Moorman, and A. W. Puschel Inactivation of the Sema5a Gene Results in Embryonic Lethality and Defective Remodeling of the Cranial Vascular System Mol. Cell. Biol., March 15, 2005; 25(6): 2310 - 2319. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. J.B. van den Hoff and A. F.M. Moorman Wnt, a Driver of Myocardialization? Circ. Res., February 18, 2005; 96(3): 274 - 276. [Full Text] [PDF] |
||||
![]() |
A. T. Soufan, M. J.B. van den Hoff, J. M. Ruijter, P. A.J. de Boer, J. Hagoort, S. Webb, R. H. Anderson, and A. F.M. Moorman Reconstruction of the Patterns of Gene Expression in the Developing Mouse Heart Reveals an Architectural Arrangement That Facilitates the Understanding of Atrial Malformations and Arrhythmias Circ. Res., December 10, 2004; 95(12): 1207 - 1215. [Abstract] [Full Text] [PDF] |
||||
![]() |
Z. Harrelson, R. G. Kelly, S. N. Goldin, J. J. Gibson-Brown, R. J. Bollag, L. M. Silver, and V. E. Papaioannou Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development Development, October 15, 2004; 131(20): 5041 - 5052. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. S. Henshel Control of Glutathione Synthesis in Early Embryo Development Toxicol. Sci., October 1, 2004; 81(2): 257 - 259. [Full Text] [PDF] |
||||
![]() |
B. Wang, J. Weidenfeld, M. M. Lu, S. Maika, W. A. Kuziel, E. E. Morrisey, and P. W. Tucker Foxp1 regulates cardiac outflow tract, endocardial cushion morphogenesis and myocyte proliferation and maturation Development, September 15, 2004; 131(18): 4477 - 4487. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. R. Keegan, D. Meyer, and D. Yelon Organization of cardiac chamber progenitors in the zebrafish blastula Development, July 1, 2004; 131(13): 3081 - 3091. [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. Timmermans, L.-M. Rodriguez, H. J.G.M. Crijns, A. F.M. Moorman, and H. J.J. Wellens Idiopathic Left Bundle-Branch Block-Shaped Ventricular Tachycardia May Originate Above the Pulmonary Valve Circulation, October 21, 2003; 108(16): 1960 - 1967. [Abstract] [Full Text] [PDF] |
||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |