Combinatorial signaling in the heart orchestrates cardiac induction, lineage specification and chamber formation

Seminars in Cell and Developmental Biology

Volumn 18, Issue 1, 2007, Pages 54-66

  Dunwoodie, Sally L ^a,b  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Cardiac chamber; Cardiac induction; Heart; Progenitor

Indexed keywords

TRANSCRIPTION FACTOR;

HEART DEVELOPMENT; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; NONHUMAN; REVIEW; VERTEBRATE;

MAMMALIA;

EID: 33847297490     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2006.12.003     Document Type: Review

References (162)

1. Buckingham M., Meilhac S., and Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 6 11 (2005) 826-835
2. Christoffels V.M., Habets P.E., Franco D., Campione M., de Jong F., Lamers W.H., et al. Chamber formation and morphogenesis in the developing mammalian heart. Dev Biol 223 2 (2000) 266-278
3. Christoffels V.M., Burch J.B., and Moorman A.F. Architectural plan for the heart: early patterning and delineation of the chambers and the nodes. Trends Cardiovasc Med 14 8 (2004) 301-307
4. Franco D., Meilhac S.M., Christoffels V.M., Kispert A., Buckingham M., and Kelly R.G. Left and right ventricular contributions to the formation of the interventricular septum of the mouse heart. Dev Biol 294 2 (2006) 366-375
5. Moorman A.F., de Jong F., Denyn M.M., and Lamers W.H. Development of the cardiac conduction system. Circ Res 82 6 (1998) 629-644
6. Moorman A.F., and Christoffels V.M. Cardiac chamber formation: development, genes, and evolution. Physiol Rev 83 4 (2003) 1223-1267
7. Tomanek R.J. Formation of the coronary vasculature during development. Angiogenesis 8 (2005) 273-284
8. Stottmann R.W., Choi M., Mishina Y., Meyers E.N., and Klingensmith J. BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium. Development 131 (2004) 2205-2218
9. Stoller J.Z., and Epstein J.A. Cardiac neural crest. Semin Cell Dev Biol 16 (2005) 704-715
10. de la Cruz M.V., Sanchez Gomez C., Arteaga M.M., and Arguello C. Experimental study of the development of the truncus and the conus in the chick embryo. J Anat 123 (1977) 661-686
11. De Vries PA. Evolution of precardiac and splanchnic mesoderm in relationship to the infundibulum and truncus. New York; 1981, p. 31-84.
12. Viragh S., and Challice C.E. Origin and differentiation of cardiac muscle cells in the mouse. J Ultrastruct Res 42 (1973) 1-24
13. Stalsberg H., and DeHaan R.L. The precardiac areas and formation of the tubular heart in the chick embryo. Dev Biol 19 (1969) 128-159
14. Mjaatvedt C.H., Nakaoka T., Moreno-Rodriguez R., Norris R.A., Kern M.J., Eisenberg C.A., et al. The outflow tract of the heart is recruited from a novel heart-forming field. Dev Biol 238 1 (2001) 97-109
15. Waldo K.L., Kumiski D.H., Wallis K.T., Stadt H.A., Hutson M.R., Platt D.H., et al. Conotruncal myocardium arises from a secondary heart field. Development 128 16 (2001) 3179-3188
16. Kelly R.G., Brown N.A., and Buckingham M.E. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1 3 (2001) 435-440
17. Zaffran S., Kelly R.G., Meilhac S.M., Buckingham M.E., and Brown N.A. Right ventricular myocardium derives from the anterior heart field. Circ Res 95 3 (2004) 261-268
18. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5 6 (2003) 877-889
19. Verzi M.P., McCulley D.J., De Val S., Dodou E., and Black B.L. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev Biol 287 1 (2005) 134-145
20. Abu-Issa R., Waldo K.L., and Kirby M.L. Heart fields: one, two or more?. Dev Biol 272 (2004) 281-285
21. Meilhac S.M., Esner M., Kelly R.G., Nicolas J.F., and Buckingham M.E. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev Cell 6 5 (2004) 685-698
22. Laugwitz K.L., Moretti A., Lam J., Gruber P., Chen Y., Woodard S., et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433 (2005) 585-587
23. Christoffels V.M., Mommersteeg M.T.M., Trow M.-O., Prall O.W., de Gier-de Vries C., Soufan A.T., et al. Formation of the venous pole of the heart from and Nkx2-5-negative precursor population requires Tbx18. Circ Res 98 (2006) 1555-1563
24. Harvey R.P. NK-2 homeobox genes and heart development. Dev Biol 178 (1996) 203-216
25. Zaffran S., Reim I., Qian L., Lo P.C., Bodmer R., and Frasch M. Cardioblast-intrinsic Tinman activity controls proper diversification and differentiation of myocardial cells in Drosophila. Development 133 20 (2006) 4073-4083
26. Raffin M., Leong L.M., Rones M.S., Sparrow D.B., Mohun T., and Mercola M. Subdivision of the cardiac Nkx2-5 expression domain into myogenic and non-myogenic compartments. Dev Biol 218 (2000) 326-340
27. Stainier D.Y., Lee R.W., and Fishman M.C. Cardiovascular development in the zebrafish. I. Myocardial fate map and heart formation. Development 119 (1993) 31-40
28. Tam P.P.L., and Schoenwolf G.C. Cardiac fate maps: lineage allocation, morphogenetic movements and cell commitment. In: Harvey R.P., and Rosenthal N. (Eds). Heart development (1999), Academic Press, London
29. Fullilove S.L. Heart induction: distribution of active factors in newt endoderm. J Exp Zool 175 3 (1970) 323-326
30. Nascone N., and Mercola M. An inductive role for the endoderm in Xenopus cardiogenesis. Development 121 (1995) 515-523
31. Yatskievych T.A., Ladd A.N., and Antin P.B. Induction of cardiac myogenesis in avian pregastrula epiblast: the role of the hypoblast and activin. Development 124 13 (1997) 2561-2570
32. Foley A.C., and Mercola M. Heart induction by Wnt antagonists depends on the homeodomain transcription factor Hex. Genes Dev 19 3 (2005) 387-396
33. Arai A., Yamamoto K., and Toyama J. Murine cardiac progenitor cells require visceral embryonic endoderm and primitive streak for terminal differentiation. Dev Dyn 210 3 (1997) 344-353
34. Schultheiss T.M., Burch J.B., and Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev 11 4 (1997) 451-462
35. Andree B., Duprez D., Vorbusch B., Arnold H.H., and Brand T. BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech Dev 70 1-2 (1998) 119-131
36. Alsan B.H., and Schultheiss T.M. Regulation of avian cardiogenesis by Fgf8 signaling. Development 129 8 (2002) 1935-1943
37. Pandur P., Lasche M., Eisenberg L.M., and Kuhl M. Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418 6898 (2002) 636-641
38. Marvin M.J., Di Rocco G., Gardiner A., Bush S.M., and Lassar A.B. Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev 15 3 (2001) 316-327
39. Schneider V.A., and Mercola M. Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev 15 3 (2001) 304-315
40. Zang X.M., Ramalho-Santos M., and McMahon A.P. Smoothened mutants reveal redundant roles for Shh and Ihh signalling including regulation of L/R symmetry by the mouse node. Cell 106 (2001) 781-792
41. Tzahor E., and Lassar A.B. Wnt signals from the neural tube block ectopic cardiogenesis. Genes Dev 15 3 (2001) 255-260
42. Lickert H., Kutsch S., Kanzler B., Tamai Y., Taketo M.M., and Kemler R. Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev Cell 3 2 (2002) 171-181
43. Brickman J.M., Jones C.M., Clements M., Smith J.C., and Beddington R.S. Hex is a transcriptional repressor that contributes to anterior identity and suppresses Spemann organiser function. Development 127 11 (2000) 2303-2315
44. Guiral M., Bess K., Goodwin G., and Jayaraman P.S. PRH represses transcription in hematopoietic cells by at least two independent mechanisms. J Biol Chem 276 4 (2001) 2961-2970
45. Ho C.Y., Houart C., Wilson S.W., and Stainier D.Y. A role for the extraembryonic yolk syncytial layer in patterning the zebrafish embryo suggested by properties of the hex gene. Curr Biol 9 19 (1999) 1131-1134
46. Pellizzari L., D'Elia A., Rustighi A., Manfioletti G., Tell G., and Damante G. Expression and function of the homeodomain-containing protein Hex in thyroid cells. Nucleic Acids Res 28 13 (2000) 2503-2511
47. Tanaka T., Inazu T., Yamada K., Myint Z., Keng V.W., Inoue Y., et al. cDNA cloning and expression of rat homeobox gene, Hex, and functional characterization of the protein. Biochem J 339 Pt 1 (1999) 111-117
48. Denson L.A., Karpen S.J., Bogue C.W., and Jacobs H.C. Divergent homeobox gene hex regulates promoter of the Na(+)-dependent bile acid cotransporter. Am J Physiol Gastrointest Liver Physiol 279 2 (2000) G347-G355
49. Brade T., Manner J., and Kuhl M. The role of Wnt signalling in cardiac development and tissue remodelling in the mature heart. Cardiovasc Res 72 2 (2006) 198-209
50. Garriock R.J., D'Agostino S.L., Pilcher K.C., and Krieg P.A. Wnt11-R, a protein closely related to mammalian Wnt11, is required for heart morphogenesis in Xenopus. Dev Biol 279 (2005) 179-192
51. von Both I., Silvestri C., Erdemir T., Lickert H., Walls J.R., Henkelman R.M., et al. Foxh1 is essential for development of the anterior heart field. Dev Cell 7 3 (2004) 331-345
52. Xu C., Liguori G., Adamson E.D., and Persico M.G. Specific arrest of cardiogenesis in cultured embryonic stem cells lacking Cripto-1. Dev Biol 196 (1998) 237-247
53. Kouskoff V., Lacaud G., Schwantz S., Fehling H.J., and Keller G. Sequential development of hematopoietic and cardiac mesoderm during embryonic stem cell differentiation. PNAS 102 (2005) 13170-13175
54. Nakamura T., Sano M., Songyang Z., and Schneider M.D. A Wnt- and β-catenin-dependent pathway for mammalian cardiac myogenesis. PNAS 100 (2003) 5834-5839
55. Yuasa S., Itabashi Y., Koshimizu U., Tanaka T., Sugimura K., Kinoshita M., et al. Transient inhibition of BMP signalling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat Biotechnol 23 (2005) 607-879
56. Nemir M., Croquelois A., Pedrazzini T., and Radtke F. Induction of cardiogenesis in embryonic stem cells via downregulation of Notch1 signaling. Circ Res 98 (2006) 1471-1478
57. Aouadi M., Bost F., Caron L., Laurent K., Le Marchand Brustel Y., and Binetruy B. p38 mitogen-activated protein kinase activity commits embryonic stem cells to either neurogenesis or cardiomyogenesis. Stem Cells 24 (2006) 1399-1406
58. Ventura C., Zinellu E., Maninchedda E., and Maioli M. Dynorphin B is an agonist of nuclear opioid receptors coupling nuclear protein kinase C activation to the transcription of cardiogenic genes in GTR1 embryonic stem cells. Circ Res 92 (2003) 623-629
59. Foshay K., Rodriguez G., Hoel B., Narayan J., and Ian Gallicano G. JAK2/STAT3 directs cardiomyogensis within murine embryonic stem cells in vitro. Stem Cells 23 (2005) 530-543
60. Papadimou E., Menard C., Grey C., and Puceat M. Interplay between the retinoblastoma protein and LEK1 specifies stem cells towards cardiac lineage. EMBO J 24 (2005) 1750-1761
61. Naito A.T., Akazawa H., Takano H., Minamino T., Nagai T., Aburatani H., et al. Phosphatidylinositol 3-kinase-Akt pathway plays a critical role in early cardiomyogenesis by regulating canonical Wnt signaling. Circ Res 97 (2005) 144-151
62. Marguerie A., Bajolle F., Zaffran S., Brown N.A., Dickson C., Buckingham M.E., et al. Congenital heart defects in Fgfr2-IIIb and Fgf10 mutant mice. Cardiovasc Res 71 1 (2006) 50-60
63. Yang L., Cai C.L., Lin L., Qyang Y., Chung C., Monteiro R.M., et al. Isl1Cre reveals a common Bmp pathway in heart and limb development. Development 133 8 (2006) 1575-1585
64. Liu W., Selever J., Wang D., Lu M.F., Moses K.A., Schwartz R.J., et al. Bmp4 signalling is required for outflow-tract septation and branchial-arch artery remodeling. PNAS 101 (2004) 4489-4494
65. Ilagan R., Abu-Issa R., Brown D., Yang Y.P., Jiao K., Schwartz R.J., et al. Fgf8 is required for anterior heart field development. Development 133 12 (2006) 2435-2445
66. Washington Smoak I., Byrd N.A., Abu-Issa R., Goddeeris M.M., Anderson R., Morris J., et al. Sonic hedgehog is required for cardiac outflow tract and neural crest cell development. Dev Biol 283 (2005) 357-372
67. Lin L., Bu L., Cai C., Zhang S., and Evans S. Isl1 is upstream of sonic hedgehog in a pathway required for cardiac morphogenesis. Dev Biol 295 (2006) 756-763
68. Yamagishi H., Maeda J., Hu T., McAnally J., Conway S.J., Kume T., et al. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev 17 2 (2003) 269-281
69. Seo S., and Kume T. Forkhead transcription factors, Foxc1 and Foxc2, are required for the morphogenesis of the cardiac outflow tract. Dev Biol 296 (2006) 421-436
70. Chapman D.L., Garvey N., Hancock S., Alexiou M., Agulnik S.I., Gibson-Brown J.J., et al. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn 206 4 (1996) 379-390
71. Xu H., Morishima M., Wylie J.N., Schwartz R.J., Bruneau B.G., Lindsay E.A., et al. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 131 13 (2004) 3217-3227
72. Merscher S., Funke B., Epstein J.A., Heyer J., Puech A., Lu M.M., et al. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104 4 (2001) 619-629
73. Lindsay E.A., Vitelli F., Su H., Morishima M., Huynh T., Pramparo T., et al. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410 6824 (2001) 97-101
74. Jerome L.A., and Papaioannou V.E. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat Genet 27 3 (2001) 286-291
75. Garg V., Yamagishi C., Hu T., Kathiriya I.S., Yamagishi H., and Srivastava D. Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev Biol 235 1 (2001) 62-73
76. Arnold J.S., Werling U., Braunstein E.M., Liao J., Nowotschin S., Edelmann W., et al. Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133 5 (2006) 977-987
77. Park E.J., Ogden L.A., Talbot A., Evans S., Cai C., Black B.L., et al. Required, tissue-specific roles of Fgf8 in outflow tract formation and remodeling. Development 133 (2006) 2419-2433
78. Brown III C.O., Chi X., Garcia-Gras E., Shirai M., Feng X.H., and Schwartz R.J. The cardiac determination factor, Nkx2-5, is activated by mutual cofactors GATA-4 and Smad1/4 via a novel upstream enhancer. J Biol Chem 279 11 (2004) 10659-10669
79. Lien C.L., Wu C., Mercer B., Webb R., Richardson J.A., and Olson E.N. Control of early cardiac-specific transcription of Nkx2-5 by a GATA-dependent enhancer. Development 126 1 (1999) 75-84
80. Lien C.L., McAnally J., Richardson J.A., and Olson E.N. Cardiac-specific activity of an Nkx2-5 enhancer requires an evolutionarily conserved Smad binding site. Dev Biol 244 2 (2002) 257-266
81. Liberatore C.M., Searcy-Schrick R.D., Vincent E.B., and Yutzey K.E. Nkx-2.5 gene induction in mice is mediated by a Smad consensus regulatory region. Dev Biol 244 2 (2002) 243-256
82. Searcy R.D., Vincent E.B., Liberatore C.M., and Yutzey K.E. A GATA-dependent nkx-2.5 regulatory element activates early cardiac gene expression in transgenic mice. Development 125 22 (1998) 4461-4470
83. Lints T.J., Parsons L.M., Hartley L., Lyons I., and Harvey R.P. Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119 3 (1993) 969
84. Komuro I., and Izumo S. Csx: a murine homeobox-containing gene specifically expressed in the developing heart. Proc Natl Acad Sci USA 90 17 (1993) 8145-8149
85. Stanley E.G., Biben C., Elefanty A., Barnett L., Koentgen F., Robb L., et al. Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3′UTR-ires-Cre allele of the homeobox gene Nkx2-5. Int J Dev Biol 46 4 (2002) 431-439
86. Moses K.A., DeMayo F., Braun R.M., Reecy J.L., and Schwartz R.J. Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31 4 (2001) 176-180
87. Tanaka M., Chen Z., Bartunkova S., Yamasaki N., and Izumo S. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 126 6 (1999) 1269-1280
88. Lyons I., Parsons L.M., Hartley L., Li R., Andrews J.E., Robb L., et al. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev 9 13 (1995) 1654-1666
89. Yamagishi H., Yamagishi C., Nakagawa O., Harvey R.P., Olson E.N., and Srivastava D. The combinatorial activities of Nkx2.5 and dHAND are essential for cardiac ventricle formation. Dev Biol 239 2 (2001) 190-203
90. Edmondson D.G., Lyons G.E., Martin J.F., and Olson E.N. Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. Development 120 5 (1994) 1251-1263
91. Dodou E., Verzi M.P., Anderson J.P., Xu S.M., and Black B.L. Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development 131 16 (2004) 3931-3942
92. Lin Q., Schwarz J., Bucana C., and Olson E.N. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276 5317 (1997) 1404-1407
93. Bi W., Drake C.J., and Schwarz J.J. The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev Biol 211 2 (1999) 255-267
94. Bruneau B.G., Bao Z.Z., Tanaka M., Schott J.J., Izumo S., Cepko C.L., et al. Cardiac expression of the ventricle-specific homeobox gene Irx4 is modulated by Nkx2-5 and dHand. Dev Biol 217 2 (2000) 266-277
95. Liu Z.P., Nakagawa O., Nakagawa M., Yanagisawa H., Passier R., Richardson J.A., et al. CHAMP, a novel cardiac-specific helicase regulated by MEF2C. Dev Biol 234 2 (2001) 497-509
96. Vong L., Bi W., O'Connor-Halligan K.E., Li C., Cserjesi P., and Schwarz J.J. MEF2C is required for the normal allocation of cells between the ventricular and sinoatrial precursors of the primary heart field. Dev Dyn 235 7 (2006) 1809-1821
97. Weisberg E., Winnier G.E., Chen X., Farnsworth C.L., Hogan B.L., and Whitman M. A mouse homologue of FAST-1 transduces TGF beta superfamily signals and is expressed during early embryogenesis. Mech Dev 79 1-2 (1998) 17-27
98. Bruneau B.G., Logan M., Davis N., Levi T., Tabin C.J., Seidman J.G., et al. Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev Biol 211 1 (1999) 100-108
99. Bruneau B.G., Nemer G., Schmitt J.P., Charron F., Robitaille L., Caron S., et al. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106 6 (2001) 709-721
100. Hiroi Y., Kudoh S., Monzen K., Ikeda Y., Yazaki Y., Nagai R., et al. Tbx5 associates with Nkx2-5 and synergistically promotes cardiomyocyte differentiation. Nat Genet 28 3 (2001) 276-280
101. Habets P.E., Moorman A.F., Clout D.E., van Roon M.A., Lingbeek M., van Lohuizen M., et al. Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev 16 10 (2002) 1234-1246
102. Lickert H., Takeuchi J.K., Von Both I., Walls J.R., McAuliffe F., Adamson S.L., et al. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432 7013 (2004) 107-112
103. Mitsiadis T.A., Angeli I., James C., Lendahl U., and Sharpe P.T. Role of Islet1 in the patterning of murine dentition. Development 130 18 (2003) 4451-4460
104. Kirby M.L. Molecular embryogenesis of the heart. Pediatr Dev Pathol 5 6 (2002) 516-543
105. Yutzey K.E., and Kirby M.L. Wherefore heart thou? Embryonic origins of cardiogenic mesoderm. Dev Dyn 223 3 (2002) 307-320
106. Cserjesi P., Brown D., Lyons G.E., and Olson E.N. Expression of the novel basic helix-loop-helix gene eHAND in neural crest derivatives and extraembryonic membranes during mouse development. Dev Biol 170 2 (1995) 664-678
107. Biben C., and Harvey R.P. Homeodomain factor Nkx2-5 controls left/right asymmetric expression of bHLH gene eHand during murine heart development. Genes Dev 11 11 (1997) 1357-1369
108. Riley P.R., Gertsenstein M., Dawson K., and Cross J.C. Early exclusion of hand1-deficient cells from distinct regions of the left ventricular myocardium in chimeric mouse embryos. Dev Biol 227 1 (2000) 156-168
109. McFadden D.G., Barbosa A.C., Richardson J.A., Schneider M.D., Srivastava D., and Olson E.N. The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development 132 1 (2005) 189-201
110. Risebro C.A., Smart N., Dupays L., Breckenridge R., Mohun T.J., and Riley P.R. Hand1 regulates cardiomyocyte proliferation versus differentiation in the developing heart. Development 133 22 (2006) 4595-4606
111. Srivastava D., Cserjesi P., and Olson E.N. A subclass of bHLH proteins required for cardiac morphogenesis. Science 270 5244 (1995) 1995-1999
112. Srivastava D., Thomas T., Lin Q., Kirby M.L., Brown D., and Olson E.N. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat Genet 16 2 (1997) 154-160
113. Thomas T., Kurihara H., Yamagishi H., Kurihara Y., Yazaki Y., Olson E.N., et al. A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development 125 16 (1998) 3005-3014
114. Kraus F., Haenig B., and Kispert A. Cloning and expression analysis of the mouse T-box gene tbx20. Mech Dev 100 1 (2001) 87-91
115. Carson C.T., Kinzler E.R., and Parr B.A. Tbx12, a novel T-box gene, is expressed during early stages of heart and retinal development. Mech Dev 96 1 (2000) 137-140
116. Stennard F.A., Costa M.W., Lai D., Biben C., Furtado M.B., Solloway M.J., et al. Murine T-box transcription factor Tbx20 acts as a repressor during heart development, and is essential for adult heart integrity, function and adaptation. Development 132 10 (2005) 2451-2462
117. Takeuchi J.K., Mileikovskaia M., Koshiba-Takeuchi K., Heidt A.B., Mori A.D., Arruda E.P., et al. Tbx20 dose-dependently regulates transcription factor networks required for mouse heart and motoneuron development. Development 132 10 (2005) 2463-2474
118. Singh M.K., Christoffels V.M., Dias J.M., Trowe M.O., Petry M., Schuster-Gossler K., et al. Tbx20 is essential for cardiac chamber differentiation and repression of Tbx2. Development 132 12 (2005) 2697-2707
119. Cai C.L., Zhou W., Yang L., Bu L., Qyang Y., Zhang X., et al. T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis. Development 132 10 (2005) 2475-2487
120. Soufan A.T., van den Berg G., Ruijter J.M., de Boer P.A., Van Den Hoff M.J., and Moorman A.F. Regionalized sequence of myocardial growth and proliferation characterizes early chamber formation. Circ Res 99 (2006) 545-552
121. de la Cruz M.V., and Markwald R.R. Living morphogenesis of the heart (1999), Birkhauser, Boston
122. Harvey R.P. Seeking a regulatory roadmap for heart morphogenesis. Semin Cell Dev Biol 10 (1999) 99-107
123. Garcia-Martinez V., and Schoenwolf G.C. Primitive-streak origin of the cardiovascular system in avian embryos. Dev Biol 159 2 (1993) 706-719
124. de Jong F., Viragh S., and Moorman A.F. Cardiac development: a morphologically integrated molecular approach. Cariol Young 7 (1997) 131-146
125. Palmer S., Groves N., Schindeler A., Yeoh T., Biben C., Wang C.C., et al. The small muscle-specific protein Csl modifies cell shape and promotes myocyte fusion in an insulin-like growth factor 1-dependent manner. J Cell Biol 153 5 (2001) 985-998
126. Stennard F.A., and Harvey R.P. T-box transcription factors and their roles in regulatory hierarchies in the developing heart. Development 132 22 (2005) 4897-4910
127. Dunwoodie S.L., Rodriguez T.A., and Beddington R.S. Msg1 and Mrg1, founding members of a gene family, show distinct patterns of gene expression during mouse embryogenesis. Mech Dev 72 1-2 (1998) 27-40
128. Christoffels V.M., Keijser A.G., Houweling A.C., Clout D.E., and Moorman A.F. Patterning the embryonic heart: identification of five mouse Iroquois homeobox genes in the developing heart. Dev Biol 224 2 (2000) 263-274
129. Harvey R.P. Patterning the vertebrate heart. Nat Rev Genet 3 7 (2002) 544-556
130. Firulli A.B., McFadden D.G., Lin Q., Srivastava D., and Olson E.N. Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nat Genet 18 3 (1998) 266-270
131. Molkentin J.D., Lin Q., Duncan S.A., and Olson E.N. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 11 8 (1997) 1061-1072
132. Li S., Zhou D., Lu M.M., and Morrisey E.E. Advanced cardiac morphogenesis does not require heart tube fusion. Science 305 5690 (2004) 1619-1622
133. Liberatore C.M., Searcy-Schrick R.D., and Yutzey K.E. Ventricular expression of tbx5 inhibits normal heart chamber development. Dev Biol 223 1 (2000) 169-180
134. Stennard F.A., Costa M.W., Elliott D.A., Rankin S., Haast S.J., Lai D., et al. Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart. Dev Biol 262 2 (2003) 206-224
135. Christoffels V.M., Hoogaars W.M., Tessari A., Clout D.E., Moorman A.F., and Campione M. T-box transcription factor Tbx2 represses differentiation and formation of the cardiac chambers. Dev Dyn 229 4 (2004) 763-770
136. Harrelson Z., Kelly R.G., Goldin S.N., Gibson-Brown J.J., Bollag R.J., Silver L.M., et al. Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development. Development 131 20 (2004) 5041-5052
137. Hoogaars W.M., Tessari A., Moorman A.F., de Boer P.A., Hagoort J., Soufan A.T., et al. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc Res 62 3 (2004) 489-499
138. Davenport T.G., Jerome-Majewska L.A., and Papaioannou V.E. Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development 130 10 (2003) 2263-2273
139. Yamada M., Revelli J.P., Eichele G., Barron M., and Schwartz R.J. Expression of chick Tbx-2, Tbx-3, and Tbx-5 genes during early heart development: evidence for BMP2 induction of Tbx2. Dev Biol 228 1 (2000) 95-105
140. Ma L., Lu M.F., Schwartz R.J., and Martin J.F. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132 24 (2005) 5601-5611
141. Rutenberg J.B., Fischer A., Jia H., Gessler M., Zhong T.P., and Mercola M. Developmental patterning of the cardiac atrioventricular canal by Notch and Hairy-related transcription factors. Development 133 21 (2006) 4381-4390
142. Brown D.D., Martz S.N., Binder O., Goetz S.C., Price B.M., Smith J.C., et al. Tbx5 and Tbx20 act synergistically to control vertebrate heart morphogenesis. Development 132 3 (2005) 553-563
143. Garcia-Bellido A. Genetic control of wing disc development in Drosophila. Ciba Found Symp 29 (1975) 161-182
144. Barolo S., and Posakony J.W. Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 16 10 (2002) 1167-1181
145. Halfon M.S., Carmena A., Gisselbrecht S., Sackerson C.M., Jimenez F., Baylies M.K., et al. Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103 1 (2000) 63-74
146. Pashmforoush M., Lu J.T., Chen H., Amand T.S., Kondo R., Pradervand S., et al. Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell 117 3 (2004) 373-386
147. Thomas P.S., Kasahara H., Edmonson A.M., Izumo S., Yacoub M.H., Barton P.J., et al. Elevated expression of Nkx-2.5 in developing myocardial conduction cells. Anat Rec 263 3 (2001) 307-313
148. Reecy J.M., Li X., Yamada M., DeMayo F.J., Newman C.S., Harvey R.P., et al. Identification of upstream regulatory regions in the heart-expressed homeobox gene Nkx2-5. Development 126 4 (1999) 839-849
149. Tanaka M., Wechsler S.B., Lee I.W., Yamasaki N., Lawitts J.A., and Izumo S. Complex modular cis-acting elements regulate expression of the cardiac specifying homeobox gene Csx/Nkx2.5. Development 126 7 (1999) 1439-1450
150. Chi X., Chatterjee P.K., Wilson III W., Zhang S.X., Demayo F.J., and Schwartz R.J. Complex cardiac Nkx2-5 gene expression activated by noggin-sensitive enhancers followed by chamber-specific modules. Proc Natl Acad Sci USA 102 38 (2005) 13490-13495
151. Schwartz R.J., and Olson E.N. Building the heart piece by piece: modularity of cis-elements regulating Nkx2-5 transcription. Development 126 19 (1999) 4187-4192
152. Lee K.H., Evans S., Ruan T.Y., and Lassar A.B. SMAD-mediated modulation of YY1 activity regulates the BMP response and cardiac-specific expression of a GATA4/5/6-dependent chick Nkx2.5 enhancer. Development 131 19 (2004) 4709-4723
153. Galvin K.M., and Shi Y. Multiple mechanisms of transcriptional repression by YY1. Mol Cell Biol 17 7 (1997) 3723-3732
154. Thomas M.J., and Seto E. Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key?. Gene 236 2 (1999) 197-208
155. Yao Y.L., Yang W.M., and Seto E. Regulation of transcription factor YY1 by acetylation and deacetylation. Mol Cell Biol 21 17 (2001) 5979-5991
156. Rezai-Zadeh N., Zhang X., Namour F., Fejer G., Wen Y.D., Yao Y.L., et al. Targeted recruitment of a histone H4-specific methyltransferase by the transcription factor YY1. Genes Dev 17 8 (2003) 1019-1029
157. Sparrow D.B., Cai C., Kotecha S., Latinkic B., Cooper B., Towers N., et al. Regulation of the tinman homologues in Xenopus embryos. Dev Biol 227 1 (2000) 65-79
158. Fishman M.C., and Olson E.N. Parsing the heart: genetic modules for organ assembly. Cell 91 2 (1997) 153-156
159. Kitano H. Systems biology: a brief overview. Science 295 5560 (2002) 1662-1664
160. Solloway M.J., and Robertson E.J. Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126 8 (1999) 1753-1768
161. Zhang H., and Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122 10 (1996) 2977-2986
162. Jeong J., Mao J., Tenzen T., Kottmann A.H., and McMahon A.P. Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 18 8 (2004) 937-951