The Tbx2+ primary myocardium of the atrioventricular canal forms the atrioventricular node and the base of the left ventricle

Circulation Research

Volumn 104, Issue 11, 2009, Pages 1267-1274

  Aanhaanen, Wim T J ^a   Brons, Janynke F ^a   Domínguez, Jorge N ^b,d   Rana, M Sameer ^a   Norden, Julia ^c   Airik, Rannar ^c   Wakker, Vincent ^a   De Gier De Vries, Corrie ^a   Brown, Nigel A ^b   Kispert, Andreas ^c   Moorman, Antoon F M ^a   Christoffels, Vincent M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF JAÉN   (Spain)

Author keywords

Atrioventricular canal; Cre; Fate; Lineage; Patterning; Transgenic

Indexed keywords

T BOX TRANSCRIPTION FACTOR; T BOX TRANSCRIPTION FACTOR TBX2; UNCLASSIFIED DRUG; T BOX DOMAIN PROTEIN 2; T-BOX DOMAIN PROTEIN 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATRIOVENTRICULAR CANAL; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO DEVELOPMENT; GENETIC LINE; HEART ATRIOVENTRICULAR NODE; HEART DEVELOPMENT; HEART LEFT VENTRICLE; HEART MUSCLE; HEART VALVE; HEART VENTRICLE SEPTUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; ANIMAL; CELL DIVISION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART; HEART VENTRICLE; HEMISPHERIC DOMINANCE; HETEROZYGOTE DETECTION; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PRENATAL DEVELOPMENT; TRANSGENIC MOUSE;

ANIMALS; ATRIOVENTRICULAR NODE; CELL DIFFERENTIATION; CELL DIVISION; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART SEPTUM; HEART VENTRICLES; HETEROZYGOTE DETECTION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCARDIUM; T-BOX DOMAIN PROTEINS;

EID: 67649870457     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.192450     Document Type: Article

References (48)

1. Moorman AFM, Christoffels VM. Cardiac chamber formation: development, genes and evolution. Physiol Rev. 2003;83:1223-1267.
2. Armstrong EJ, Bischoff J. Heart valve development: endothelial cell signaling and differentiation. Circ Res. 2004;95:459-470.
3. Ma L, Lu MF, Schwartz RJ, Martin JF. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development. 2005;132:5601-5611.
4. Wessels A, Markman MWM, Vermeulen JLM, Anderson RH, Moorman AFM, Lamers WH. The development of the atrioventricular junction in the human heart. Circ Res. 1996;78:110-117.
5. Hoffman JI, Kaplan S. The incidence of congenital heart disease. J Am Coll Cardiol. 2002;39:1890-1900.
6. Pierpont ME, Markwald RR, Lin AE. Genetic aspects of atrioventricular septal defects. Am J Med Genet. 2000;97:289-296.
7. Walsh EP. Arrhythmias in patients with congenital heart disease. Card Electrophysiol Rev. 2002;6:422-430.
8. Virágh Sz, Challice CE. The development of the conduction system in the mouse embryo heart. II. Histogenesis of the atrioventricular node and bundle. Dev Biol. 1977;56:397-411.
9. Chan-Thomas PS, Thompson RP, Robert B, Yacoub MH, Barton PJR. Expression of homeobox genes Msx-1 (Hox-7) and Msx-2 (Hox-8) during cardiac development in the chick. Dev Dyn. 1993;197:203-216.
10. Davis DL, Edwards AV, Juraszek AL, Phelps A, Wessels A, Burch JB. A GATA-6 gene heart-region-specific enhancer provides a novel means to mark and probe a discrete component of the mouse cardiac conduction system. Mech Dev. 2001;108:105-119.
11. de Lange FJ, Moorman AFM, Anderson RH, Manner J, Soufan AT, de Gier-de Vries C, Schneider MD, Webb S, van den Hoff MJB, Christoffels VM. Lineage and morphogenetic analysis of the cardiac valves. Circ Res. 2004;95:645-654.
12. Gaussin V, Morley GE, Cox L, Zwijsen A, Vance KM, Emile L, Tian Y, Liu J, Hong C, Myers D, Conway SJ, Depre C, Mishina Y, Behringer RR, Hanks MC, Schneider MD, Huylebroeck D, Fishman GI, Burch JB, Vatner SF. Alk3/Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res. 2005; 97:219-226.
13. Di Lisi R, Sandri C, Franco D, Ausoni S, Moorman AFM, Schiaffino S. An atrioventricular canal domain defined by cardiac troponin I transgene expression in the embryonic myocardium. Anat Embryol (Berl). 2000; 202:95-101.
14. Hoogaars WMH, Tessari A, Moorman AFM, de Boer PAJ, Hagoort J, Soufan AT, Campione M, Christoffels VM. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc Res. 2004;62:489-499.
15. Yamada M, Revelli JP, Eichele G, Barron M, Schwartz RJ. Expression of chick Tbx-2, Tbx-3, and Tbx-5 genes during early heart development: evidence for BMP2 induction of Tbx2. Dev Biol. 2000;228:95-105.
16. Habets PEMH, Moorman AFM, Clout DEW, van Roon MA, Lingbeek M, Lohuizen M, Campione M, Christoffels VM. Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev. 2002;16: 1234-1246.
17. Christoffels VM, Hoogaars WMH, Tessari A, Clout DEW, Moorman AFM, Campione M. T-box transcription factor Tbx2 represses differentiation and formation of the cardiac chambers. Dev Dyn. 2004;229: 763-770.
18. Harrelson Z, Kelly RG, Goldin SN, Gibson-Brown JJ, Bollag RJ, Silver LM, Papaioannou VE. Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development. Development. 2004;131:5041-5052.
19. Nagy A. Cre recombinase: the universal reagent for genome tailoring. Genesis. 2000;26:99-109.
20. Abu-Issa R, Waldo K, Kirby ML. Heart fields: one, two or more? Dev Biol. 2004;272:281-285.
21. Buckingham M, Meilhac S, Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet. 2005;6:826-837.
22. Horsthuis T, Houweling AC, Habets PEMH, de Lange FJ, el Azzouzi H, Clout DEW, Moorman AFM, Christoffels VM. Distinct regulation of developmental and heart disease induced atrial natriuretic factor expression by two separate distal sequence. Circ Res. 2008;102:849-859.
23. Arguëllo C, Alanis J, Valenzuela B. The early development of the atrio-ventricular node and bundle of His in the embryonic chick heart. An electrophysiological and morphological study. Development. 1988;102: 623-637.
24. Mommersteeg MTM, Soufan AT, de Lange FJ, van den Hoff MJB, Anderson RH, Christoffels VM, Moorman AFM. Two distinct pools of mesenchyme contribute to the development of the atrial septum. Circ Res. 2006;99:351-353.
25. Snarr BS, Wirrig EE, Phelps AL, Trusk TC, Wessels A. A spatiotemporal evaluation of the contribution of the dorsal mesenchymal protrusion to cardiac development. Dev Dyn. 2007;236:1287-1294.
26. Kelly RG, Brown NA, Buckingham ME. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell. 2001;1:435-440.
27. Rana MS, Horsten NCA, Tesink-Taekema S, Lamers WH, Moorman AFM, van den Hoff MJB. Trabeculated right ventricular free wall in the chicken heart forms by ventricularization of the myocardium initially forming the outflow tract. Circ Res. 2007;100:1000-1007.
28. Verzi MP, McCulley DJ, De VS, Dodou E, Black BL. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev Biol. 2005;287: 134-145.
29. Franco D, Meilhac SM, Christoffels VM, Kispert A, Buckingham M, Kelly RG. Left and right ventricular contributions to the formation of the interventricular septum in the mouse heart. Dev Biol. 2006;294:366-375.
30. Bakker ML, Boukens BJ, Mommersteeg MTM, Brons JF, Wakker V, Moorman AFM, Christoffels VM. Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ Res. 2008;102:1340-1349.
31. Mesbah K, Harrelson Z, Theveniau-Ruissy M, Papaioannou VE, Kelly RG. Tbx3 is required for outflow tract development. Circ Res. 2008;103: 743-750.
32. Ribeiro I, Kawakami Y, Buscher D, Raya A, Rodriguez-Leon J, Morita M, Rodriguez Esteban C, Izpisua Belmonte JC. Tbx2 and Tbx3 regulate the dynamics of cell proliferation during heart remodeling. PLoS ONE. 2007;2:e398.
33. Naiche LA, Harrelson Z, Kelly RG, Papaioannou VE. T-Box Genes in Vertebrate Development. Annu Rev Genet. 2005;39:219-239.
34. Soufan AT, van den Berg G, Moerland PD, Massink MMG, van den Hoff MJB, Moorman AFM, Ruijter JM. Three-dimensional measurement and visualization of morphogenesis applied to cardiac embryology. J Microsc. 2007;225:269-274.
35. Wessels A, Vermeulen JLM, Verbeek FJ, Virágh Sz, Kálmán F, Lamers WH, Moorman AFM. Spatial distribution of "tissue-specific" antigens in the developing human heart and skeletal muscle: III. An immunohisto-chemical analysis of the distribution of the neural tissue antigen G1N2 in the embryonic heart; implications for the development of the atrioven-tricular conduction system. Anat Rec. 1992;232:97-111.
36. Gourdie RG, Harris BS, Bond J, Justus C, Hewett KW, O?Brien TX, Thompson RP, Sedmera D. Development of the cardiac pacemaking and conduction system. Birth Defects Res Part C Embryo Today. 2003;69: 46-57.
37. Pennisi DJ, Rentschler S, Gourdie RG, Fishman GI, Mikawa T. Induction and patterning of the cardiac conduction system. Int J Dev Biol. 2002; 46:765-775. (Pubitemid 35231070)
38. De la Cruz MV, Markwald RR. Living Morphogenesis of the Heart. 1st ed. Cambridge, Mass: Birkhäuser; 1998:1-233.
39. Rentschler S, Vaidya DM, Tamaddon H, Degenhardt K, Sassoon D, Morley GE, Jalife J, Fishman GI. Visualization and functional characterization of the developing murine cardiac conduction system. Development. 2001;128:1785-1792. (Pubitemid 32514858)
40. Kondo RP, Anderson RH, Kupershmidt S, Roden DM, Evans SM. Development of the cardiac conduction system as delineated by minK-lacZ. J Cardiovasc Electrophysiol. 2003;14:383-391.
41. Moskowitz IP, Kim JB, Moore ML, Wolf CM, Peterson MA, Shendure J, Nobrega MA, Yokota Y, Berul C, Izumo S, Seidman JG, Seidman CE. A molecular pathway including id2, tbx5, and nkx2-5 required for cardiac conduction system development. Cell. 2007;129:1365-1376.
42. Soufan AT, van den Berg G, Ruijter JM, de Boer PAJ, van den Hoff MJB, Moorman AFM. Regionalized sequence of myocardial cell growth and proliferation characterizes early chamber formation. Circ Res. 2006;99: 545-552.
43. Christoffels VM, Burch JBE, Moorman AFM. Architectural plan for the heart: early patterning and delineation of the chambers and the nodes. Trends Cardiovasc Med. 2004;14:301-307.
44. Stennard FA, Harvey RP. T-box transcription factors and their roles in regulatory hierarchies in the developing heart. Development. 2005;132: 4897-4910.
45. Chi NC, Shaw RM, De VS, Kang G, Jan LY, Black BL, Stainier DY. Foxn4 directly regulates tbx2b expression and atrioventricular canal formation. Genes Dev. 2008;22:734-739.
46. Christoffels VM, Grieskamp T, Norden J, Mommersteeg MTM, Rudat C, Kispert A. Tbx18 and the fate of epicardial progenitors. Nature. 2009; 458:E8-E9.
47. Cheng G, Litchenberg WH, Cole GJ, Mikawa T, Thompson RP, Gourdie RG. Development of the cardiac conduction system involves recruitment within a multipotent cardiomyogenic lineage. Development. 1999;126: 5041-5049.
48. Erokhina IL, Rumyantsev PP. Proliferation and biosynthetic activities of myocytes from conductive system and working myocardium of the developing mouse heart. Light microscopic autoradiographic study. Acta Histochem. 1988;84:51-66.