Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart

Developmental Biology

Volumn 262, Issue 2, 2003, Pages 206-224

  Stennard, Fiona A ^a   Costa, Mauro W ^a,h   Elliott, David A ^a   Rankin, Scott ^b   Haast, Saskia J P ^a,c   Lai, Donna ^a   McDonald, Lachlan P A ^a   Niederreither, Karen ^d   Dolle, Pascal ^e   Bruneau, Benoit G ^f   Zorn, Aaron M ^b   Harvey, Richard P ^a,g  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e Laboratoire de Chimie des Interactions Moleculaires   (France)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g UNIVERSITY OF NEW SOUTH WALES   (Australia)

^h FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Cell migration; Embryonic development; GATA; Heart development; Nkx2 5; T box; Tbx genes; Tbx20; Tbx5; Transcription factor; Xenopus

Indexed keywords

COMPLEMENTARY DNA; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 5;

ANALYTIC METHOD; ARTICLE; BEHAVIOR; BINDING AFFINITY; CONTROLLED STUDY; DNA BINDING; DNA SPLICING; EMBRYO; EMBRYO DEVELOPMENT; ENDOCARDIUM; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INTERACTION; HEART DEVELOPMENT; HEART MUSCLE; IN VIVO STUDY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VERTEBRATE;

INVERTEBRATA; MURINAE; VERTEBRATA;

EID: 0141615095     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(03)00385-3     Document Type: Article

References (103)

1. Arceci R.J., King A.A., Simon M.C., Orkin S.H., Wilson D.B. Mouse GATA-4 a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart . Mol. Cell. Biol. 13:1993;2235-2246.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., Struhl, K., 1996. Current Protocols in Molecular Biology. Chanda, V.B. (Ed.), Vol. 2. John Wiley and Sons, New York.
3. Basson C.T., Bachinsky D.R., Lin R.C., Levi T., Elkins J.A., Soults J., Grayzel D., Kroumpouzou E., Traill T.A., Leblanc-Straceski J., Renault B., Kucherlapati R., Seidman J.G., Seidman C.E. Mutations in human TBX5 cause limb and cardiac malformation in Holt-Oram syndrome. Nat. Genet. 15:1997;30-35.
4. Biben C., Harvey R.P. Homeodomain factor Nkx2-5 controls left-right asymmetric expression of bHLH eHand during murine heart development. Genes Dev. 11:1997;1357-1369.
5. Biben C., Palmer D.A., Elliott D.A., Harvey R.P. Homeobox genes and heart development. Cold Spring Harbor Symp. Quant. Biol. 62:1997;395-403.
6. Bodmer R., Venkatesh T.V. Heart development in Drosophila and vertebrates conservation of molecular mechanisms . Dev. Genet. 22:1998;181-186.
7. Brown D.D., Binder O., Pagratis M., Parr B., Conlon F. Developmental expression of the Xenopus laevis Tbx20 orthologue. Dev. Genes Evol. 212:2003;604-607.
8. Bruneau B.G., Logan M., Davis N., Levi T., Tabin C.J., Seidman J.G., Seidman C.E. Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram Syndrome. Dev. Biol. 211:1999;100-108.
9. Bruneau B.G., Nemer G., Schmitt J.P., Charron F., Robitaille L., Caron S., Conner D.A., Gessler M., Nemer M., Seidman C.E., Seidman J.G. A murine model of Holt-Oram Syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell. 106:2001;709-721.
10. Carreira S., Dexter T.J., Yavuzer U., Easty D.J., Goding C.R. Brachyury-related transcription factor Tbx2 and repression of the melanocyte-specific TRP-1 promoter. Mol. Cell. Biol. 1998:1998;5099-5108.
11. Carson C.T., Kinzler E.R., Parr B.A. Tbx12, a novel T-box gene, is expressed during early stages of heart and retinal development. Mech. Dev. 96:2000;137-140.
12. Casey E.S., O'Reilly M.A., Conlon F.L., Smith J.C. The T-box transcription factor Brachyury regulates expression of eFGF through binding to a non-palindromic respsonse element. Development. 125:1998;3887-3894.
13. Chapman D.L., Papaioannou V.E. Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature. 391:1998;695-697.
14. Charron F., Nemer M. GATA transcription factors and cardiac development. Semin. Cell Dev. Biol. 10:1999;85-91.
15. Chen C.Y., Schwartz R.J. Identification of novel DNA binding targets and regulatory domains of a murine Tinman homeodomain factor, Nkx-2.5. J. Biol. Chem. 270:1995;15628-15633.
16. Chen C.Y., Schwartz R.J. Recruitment of the Tinman homologue Nkx-2.5 by serum response factor activates cardiac α-actin gene transcription. Mol. Cell. Biol. 16:1996;6372-6384.
17. Chen F., Kook H., Milewski R., Gitler A.D., Lu M.M., Li J., Nazarian R., Schnepp R., Jen K., Biben C., Runke G., Mackay J., Novotny J., Schwartz R.J., Harvey R.P., Mullins M.C., Epstein J.A. Hop is an unusual homeobox gene that modulates cardiac development. Cell. 110:2002;713-723.
18. Christoffels V.M., Habets P.E.M.H., Franco D., Campione M., de Jong F., Lamers W.H., Bao Z.-Z., Palmer S., Biben C., Harvey R.P., Moorman F.M. Chamber formation and morphogenesis in the developing mammalian heart. Dev. Biol. 223:2000;266-278.
19. Ciruna B., Rossant J. FGF signaling regulates mesodermal cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell. 1:2001;37-49.
20. Clamp M., Andrews D., Barker D., Bevan P., Cameron G., Chen Y., Clark L., Cox T., Cuff J., Curwen V., Down T., Durbin R., Eyras E., Gilbert J., Hammond M., Hubbard T., Kasprzyk A., Keefe D., Lehvaslaiho H., Iyer V., Melsopp C., Mongin E., Pettett R., Potter S., Rust A., Schmidt E., Searle S., Slater G., Smith J., Spooner W., Stabenau A., Stalker J., Stupka E., Ureta-Vidal A., Vastrik I., Birney E. Ensembl 2002 accommodating comparative genomics . Nucleic Acids Res. 31:2003;38-42.
21. Coll M., Seidman J.G., Muller C. Structure of the DNA-bound T-box domain of human TBX3, a transcription factor responsible for ulnar mammary syndrome. Structure. 10:2002;343-356.
22. Conlon F.L., Fairclough L., Price B.M.J., Casey E.S., Smith J.C. Determinants of T box protein specificity. Development. 128:2001;3749-3758.
23. Cripps R.M., Olson E. Control of cardiac development by an evolutionarily conserved transcriptional network. Dev. Biol. 246:2002;14-28.
24. Cunliffe V., Smith J. Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue. Nature. 358:1992;427-430.
25. Delorme B., Dahl E., Jarry-Guichard T., Briand J.-P., Willecke K., Gros D., Theveniau-Ruissy M. Expression pattern of connexin gene products at the early developmental stages of the mouse cardiovascular system. Circ. Res. 81:1997;423-437.
26. Durocher D., Charron F., Warren R., Schwartz R.J., Nemer M. The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. EMBO J. 16:1997;5687-5696.
27. Durocher D., Chen C.Y., Ardati A., Schwatrz R.J., Nemer M. The ANF promoter is a downstream target for Nkx-2.5 in the myocardium. Mol. Biol. Cell. 16:1996;4648-4655.
28. Elliott, D.A., Kirk, E., Yeoh, T., Chander, S., McKenzie, F., Taylor, P., Grossfeld, P., Fatkin, D., Jones, O., Hayes, P., Feneley, M., Harvey, R.P., 2003. Cardiac homeobox gene NKX2-5 mutations and congenital heart disease: associations with atrial septal defect and hyperplastic left heart syndrome. J. Am. Coll. Cardiol., in press.
29. Engleka M.J., Craig E.J., Kessler D.S. VegT activation of Sox17 at the midblastula transition alters the response to nodal signals in the vegetal endodermal domain. Dev. Biol. 237:2001;159-172.
30. Ghosh T.K., Packham E.A., Bonser A.J., Robinson T.E., Cross S.J., Brok J.D. Characterisation of the TBX5 binding site and analysis of mutations that cause Holt-Oram Syndrome. Hum. Mol. Genet. 10:2001;1983-1994.
31. Gibson-Brown J.J., Agulnik S.I., Chapman D.L., Alexiou M., Garvey N., Silver L.M., Papaioannou V.E. Evidence of a role for T-box genes in the evolutiono of limb morphogenesis and the specification of forelimb/hindlimb identity. Mech. Dev. 56:1996;93-101.
32. Goldmuntz E., Geiger E., Benson W. NKX2.5 mutations in patients with tetralogy of fallot. Circulation. 104:2001;2565-2568.
33. Griffin K.J.P., Amacher S.L., Kimmel C.B., Kimelman D. Molecular identification of spadetail regulation of zebrafish trunk and tail mesoderm formation by T-box genes . Development. 125:1998;3379-3388.
34. Griffin K.J.P., Stoller J., Gibson M., Chen S., Yelon D., Stainier D.Y.R., Kimelman D. A conserved role for H15-related T-box transcription factors in zebrafish and Drosophila heart formation. Dev. Biol. 218:2000;235-247.
35. Grow M.W., Krieg P.A. Tinman function is essential for vertebrate heart development elimination of cardiac differentiation by dominant inhibitory mutants of the tinman-related genes, XNkx2-3 and XNkx2-5 . Dev. Biol. 204:1998;187-196.
36. Habets P.E.M.H., Moorman A.F.M., Clout D.E.W., van Roon M.A., Lingbeek M., van Lohuizen M., Campione M., Christoffels V.M. Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular cana implication for cardiac chamber formation . Genes Dev. 16:2002;1234-1246.
37. Harvey R.P. NK-2 homeobox genes and heart development. Dev. Biol. 178:1996;203-216.
38. Harvey R.P. Molecular determinants of cardiac development and congenital disease. Rossant J., Tam P.P.L. Mouse Development Patterning, Morphogenesis, and Organogenesis . 2002;331-370 Academic Press, San Diego.
39. Harvey R.P., Biben C., Elliot D.A. Transcriptional control and pattern formation in the developing vertebrate heart studies on NK-2 class homeodomain factors . Harvey R.P., Rosenthal N. Heart Development. 1999;111-129 Academic Press, San Diego.
40. Hatcher C.J., Goldstein M.M., Mah C.S., Delia C.S., Basson C.T. Identification and localisation of TBX5 transcription factor during human cardiac morphogenesis. Dev. Dyn. 219:2000;90-95.
41. Hatcher C.J., Kim M.-S., Mah C.S., Goldstein M.M., Wong B., Mikawa T., Basson C.T. TBX5 transcription factor regulates cell proliferation during cardiogenesis. Dev. Biol. 230:2001;177-188.
42. He M., Wen L., Campbell C.E., Wu J.Y., Rao Y. Transcription repression by Xenopus ET and its human ortholog TBX3, a gene involved in ulnar-mammary syndrome. Proc. Natl. Acad. Sci. USA. 96:1999;10212-10217.
43. Hiroi Y., Kudoh S., Monzen K., Ikeda Y., Yazaki Y., Nagai R., Komuro I. Tbx5 associates with Nkx2.5 and synergistically promotes cardiomyocyte differentiation. Nat. Genet. 28:2001;276-280.
44. Horb M.E., Thomsen G.H. Tbx5 is essential for heart development. Development. 126:1999;1739-1751.
45. Hsueh Y.-P., Wang T.-F., Yang F.-C., Sheng M. Nuclear tanslocation and transcription regulation by the membrane-associated guanylate kinase CASK/LIN-2. Nature. 404:2000;298-302.
46. Isaac A., Rodriguez-Esteban C., Ryan A., Altabef M., Tsukui T., Patel K., Tickle C., Izpisua-Belmonte J.-C. Tbx genes and limb identity in chick embryo development. Development. 125:1998;1867-1875.
47. Jayaseelan R., Poizat C., Baker R.K., Abdishoo S., Isterabadi L.B., Lyons G.E., Kedes L. A novel cardiac-restricted target for doxorubicin, CARP, a nuclear modulator of gene expression in cardiac progenitor cells and cardiomyocytes. J. Biol. Chem. 272:1997;22800-22808.
48. Jerome L.A., Papaioannou V.E. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet. 27:2001;286-291.
49. Kasahara H., Bartunkova S., Schinke M., Tanaka M., Izumo S. Cardiac and extracardiac expression of the Csx/Nkx2.5 homeodomain protein. Circ. Res. 82:1998;936-946.
50. Kasahara H., Lee B., Schott J.J., Benson D.W., Seidman J.G., Seidman C.E., Izumo S. Loss of function and inhibitory effects of human CSX/NKX2.5 homeoprotein mutations associated with congenital heart disease. J. Clin. Invest. 106:2000;299-308.
51. Kasahara H., Usheva A., Ueyama T., Alki H., Horikoshi N., Izumo S. Characterization of homo- and heterodimerization of cardiac Csx/Nkx2.5 homeoprotein. J. Biol. Chem. 276:2001;4570-4580.
52. Kelly R.G., Buckingham M.E. The anterior heart-forming field journey to the arterial pole of the heart . Trends Genet. 18:2002;210-216.
53. Kispert A., Herrmann B.G. The Brachyury gene encodes a novel DNA binding protein. EMBO J. 12:1993;3211-3220.
54. Kispert A., Koschorz B., Herrmann B.G. The T protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J. 14:1995;4763-4772.
55. Kofron M., Demel T., Xanthos J., Lohr J., Sun B., Sive H., Osada S.-I., Wright C., Wylie C., Heasman J. Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFβ growth factors. Development. 126:1999;5759-5770.
56. Koshiba-Takeuchi K., Takeuchi J.K., Mataumoto K., Momose T., Uno K., Hoepker V., Ogura K., Takahashi N., Nakamura H., Yasuda K., Ogura T. Tbx5 and the retinotectum projection. Science. 287:2000;134-137.
57. Kraus F., Haenig B., Kispert A. Cloning and expression analysis of the mouse T-box gene Tbx18. Mech. Dev. 100:2001;83-86.
58. Kraus F., Haenig B., Kispert A. Cloning and expression analysis of the mouse T-box gene Tbx20. Mech. Dev. 100:2001;87-91.
59. Lee Y., Shioi T., Kasahara H., Jobe S.M., Wiese R.J., Markham B.E., Izumo S. The cardiac tissue-restriced homeobox protein Csx/Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol. Cell. Biol. 18:1998;3120-3129.
60. Li Q.Y., Newbury-Ecob R.A., Terrett J.A., Wilson D.I., Curtis A.R.J., Yi C.H., Gebuhr T., Bullen P.J., Robson S.C., Strachan T., Bonnet D., Lyonnet S., Young I.D., Raeburn A., Buckler A.J., Law D.J., Brook J.D. Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat. Genet. 15:1997;21-29.
61. Liberatore C.M., Searcy-Schrick R.D., Yutzey K.E. Ventricular expression of tbx5 inhibits normal heart chamber development. Dev. Biol. 223:2000;169-180.
62. Lindsay E.A., Vitelli F., Su H., Morishima M., Huynh T., Pramparo T., Jurecic V., Ogunrinu G., Sutherland H.F., Scambler P.J., Bradley A., Baldini A. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature. 410:2001;97-101.
63. Logan M., Tabin C.J. Role of Pitx1 upstream of Tbx4 in specification of hindlimb identity. Science. 283:1999;1736-1739.
64. Lyons I., Parsons L.M., Hartley L., Li R., Andrews J.E., Robb L., Harvey R.P. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeobox gene Nkx2-5. Genes Dev. 9:1995;1654-1666.
65. Mattaj I.W., Englmeier L. Nucleocytoplasmic transport the soluble phase . Annu. Rev. Biochem. 67:1998;265-306.
66. Meins M., Henderson D.J., Bhattasharya S.S., Sowden J.C. Characterisation of the human TBX20 gene, a new member of the T-box gene family closely related to the Drosophila H15 gene. Genomics. 67:2000;317-332.
67. Merscher S., Funke B., Epstein J.A., Heyer J., Puech A., Lu M.M., Xavier R.J., Demay M.B., Russell R.G., Factor S., Tokooya K., Jore B.S., Lopez M., Pandita R.K., Lia M., Carrion D., Xu H., Schorle H., Kobler J.B., Scambler P., Wynshaw-Boris A., Skoultchi A.I., Morrow B.E., Kucherlapati R. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell. 104:2001;619-629.
68. Moorman A.F.M., de Jong F., Denyn M.M.F.J., Lamers W.H. Development of the cardiac conduction system. Circ. Res. 82:1998;629-644.
69. Morin S., Paradis P., Aries A., Nemer M. Serum response factor-GATA ternary complex required for nuclear signalling by a G-protein-coupled receptor. Mol. Cell. Biol. 21:2001;1044-1936.
70. Muller C.W., Herrmann B.G. Crystallographic structure of the T domain-DNA complex of the Brachyury transcription factor. Nature. 389:1997;884-888.
71. Nakajima Y., Yamagishi T., Hokari S., Nakamura H. Mechanisms involved in valvuloseptal endocardial cushion formation in early cardiogenesis roles of transforming growth factor (TGF)-beta and bone morphogenetic protein (BMP) . Anat. Rec. 258:2000;119-127.
72. Nemer G., Nemer M. Cooperative interaction between GATA5 and NF-ATc regulates endothelial-endocardial differentiation of cardiogenic cells. Development. 129:2002;4045-4055.
73. Niederreither K., Vermot J., Messaddeq N., Schuhbaur B., Chambon P., Dolle P. Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development. 128:2001;1019-1031.
74. Packham E.A., Brook J.D. T-box genes in human disorders. Hum. Mol. Genet. 12:2003;R37-R44.
75. Palmer S., Groves N., Schindeler A., Yeoh T., Biben C., Wang C.-C., Sparrow D.B., Barnett L., Jenkins N., Copeland N., Koentgen F., Mohun T., Harvey R.P. The small muscle-specific protein Csl modifies cell shape and promotes myocyte fusion in an IGF-1 dependent manner. J. Cell Biol. 153:2001;985-998.
76. Papaioannou V.E., Silver L.M. The T-box gene family. Bioessays. 20:1998;9-19.
77. Pasumarthi K.B., Field L.J. Cardiomyocyte cell cycle regulation. Circ. Res. 90:2002;1044-1054.
78. Paxton C., Zhao H., Chin Y., Langner K., Reecy J. Murine Tbx2 contains domains that activate and repress gene transcription. Genes Dev. 283:2002;117-124.
79. Prall O., Elliott D.A., Harvey R.P. Developmental paradigms in heart disease insights from tinman . Ann. Med. 34:2002;148-156.
80. Ranganayakulu G., Elliot D.A., Harvey R.P., Olson E.N. Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development. 125:1998;3037-3048.
81. Redkar A., Mongomery M., Litvin J. Fate map of early avian cardiac progenitor cells. Development. 128:2001;2269-2279.
82. Ross S.A., McCAffery R.J., Drager U., De Luca L.M. Retinoids in embryonal development. Physiol. Rev. 80:2000;1021-1054.
83. Russ A.P., Wattler S., Colledge W.H., Aparicio S.A., Carlton M.B., Pearce J.J., Barton S.C., Surani M.A., Ryan K., Nehls M.C., Wilson V., Evans M.J. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature. 404:2000;95-99.
84. Sadowski I., Ptashne M. A vector for expressing GAL4(1-147) fusions in mammalian cells. Nucleic Acids Res. 17:1989;7539.
85. Seth A., Gonzalez F.A., Gupta S., Raden D.L., Davis R.J. Signal transduction within the nucleus by mitogen-activated protein kinase. J. Biol. Chem. 267:1992;24796-24804.
86. Shiojima I., Komuro I., Oka T., Hiroi Y., Mizuno T., Takimoto E., Monzen K., Aikawa H., Yamazaki T., Kudoh S., Yazaki Y. Context-dependent transcriptional cooperation mediated by cardiac transcription factors Csx/Nkx-2.5 and GATA-4. J. Biol. Chem. 274:1999;8231-8239.
87. Silver P.A., Lei E.P. Protein and RNA export from the nucleus. Dev. Cell. 2:2002;261-272.
88. Sinha, S., Abraham, S., R.M., G., Campbell, C.E., 2000. Differential DNA binding and transcriptional modulation by three T-box proteins, T, TBX1 and TBX2. Gene 258, 15-29.
89. Smith J. T-box genes what they do and how they do it . Trends Genet. 15:1999;154-158.
90. Stennard F., Carnac G., Gurdon J.B. The Xenopus T-box gene, Antipodean, encodes a vegetally localised maternal mRNA and can trigger mesoderm formation. Development. 122:1996;4179-4188.
91. Szeto D.P., Griffin K.J., Kimelman D.K. hrT is required for cardiovascular development in zebrafish. Development. 129:2002;5093-5101.
92. Tada M., Smith J. Xwnt11 is a target of Xenopus Brachyury regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway . Development. 127:2000;2227-2238.
93. Takeuchi J.K., Koshiba-Takeuchi K., Matsumoto K., Vogel-Hopker A., Naitoh-Matsuo M., Ogura K., Takahashi N., Yasuda K., Ogura K. Tbx5 and Tbx4 genes determine the wing/leg identity of limb buds. Nature. 398:1999;810-814.
94. Tanaka M., Chen Z., Bartunkova S., Yamasaki N., Izumo S. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes for heart development. Development. 126:1999;1269-1280.
95. van den Hoff M.J.B., Moorman A.F.M., Ruijter J.M., Lamers W.H., Bennington R.W., Markwald R.R., Wessels A. Myocardialization of the cardiac outflow tract. Dev. Biol. 212:1999;477-490.
96. Vaughan C.J., Basson C.J. Molecular determinants of atrial and ventricular septal defects and patent ductus arteriosus. Am. J. Med. Genet. (Semin. Med. Genet.). 97:2001;304-309.
97. Watada H., Mirmira R.G., Kalamaras J., German M.S. Intramolecular control of transcriptional activity by the NK2-specific domain in NK-2 homeodomain proteins. Proc. Natl. Acad. Sci. USA. 97:2000;9443-9448.
98. Webb S., Brown N.A., Anderson R.H. Formation of the atrioventricular septal structures in the normal mouse. Circ. Res. 82:1998;645-656.
99. Wolberger C. Multiprotein-DNA complexes in transcriptional regulation. Annu. Rev. Biophys. Biomol. Struct. 28:1999;29-56.
100. Xanthos J.B., Kofron M., Wylie C., Heasman J. Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development. 128:2001;167-180.
101. Yamomoto A., Amacher S.L., Kim S., Geissert D., Kimmel C.B., De Robertis E.M. Zebrafish paraxial protocadherin is a downstream target of spadetail involved in morphogenesis of gastrula mesoderm. Development. 125:1998;3389-3397.
102. Zaffran S., Frasch M. Early signals in cardiac development. Circ. Res. 91:2002;457-469.
103. Zou Y., Evans S., Chen J., Kou H.-C., Harvey R.P., Chien K.R. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development. 124:1997;793-804.