The Mix family of homeobox genes-Key regulators of mesendoderm formation during vertebrate development

Developmental Biology

Volumn 367, Issue 2, 2012, Pages 163-177

  Pereira, Lloyd A ^a   Wong, Michael S ^b   Mei Lim, Sue ^b   Stanley, Edouard G ^b,c   Elefanty, Andrew G ^b,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

Development; Embryogenesis; Embryonic stem cell; Endoderm; Gene expression; Germ layer; Mesoderm; Mix Bix; Mixl1

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; BRACHYURY INDUCIBLE HOMEOBOX PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEIN; MESODERM INDUCING FACTOR INDUCIBLE HOMEOBOX PROTEIN; PROTEIN NODAL; REGULATOR PROTEIN; SMAD PROTEIN; T BOX TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL FATE; DEVELOPMENTAL BIOLOGY; DEVELOPMENTAL GENE; DNA BINDING; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENDODERM; GASTRULATION; GENE; GENE FUNCTION; GENE MUTATION; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC CONSERVATION; HUMAN; MESODERM; MESODERM INDUCING FACTOR INDUCIBLE HOMEOBOX 1 LIKE GENE; MESODERM INDUCING FACTOR INDUCIBLE HOMEOBOX GENE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; TRANSACTIVATION; XENOPUS LAEVIS;

AMPHIBIA; DANIO RERIO; MUS; VERTEBRATA;

EID: 84862151681     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.04.033     Document Type: Article

References (128)

1. Aebersold R., Mann M. Mass spectrometry-based proteomics. Nature 2003, 422:198-207.
2. Alexander J., Rothenberg M., Henry G.L., Stainier D.Y. Casanova plays an early and essential role in endoderm formation in zebrafish. Dev. Biol. 1999, 215:343-357.
3. Alexander J., Stainier D.Y. A molecular pathway leading to endoderm formation in zebrafish. Curr. Biol. 1999, 9:1147-1157.
4. Arnold S.J., Hofmann U.K., Bikoff E.K., Robertson E.J. Pivotal roles for eomesodermin during axis formation, epithelium-to-mesenchyme transition and endoderm specification in the mouse. Development 2008, 135:501-511.
5. Artinger M., Blitz I., Inoue K., Tran U., Cho K.W. Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev. 1997, 65:187-196.
6. Attisano L., Wrana J.L. Signal transduction by the TGF-beta superfamily. Science 2002, 296:1646-1647.
7. Berger M.F., Badis G., Gehrke A.R., Talukder S., Philippakis A.A., Pena-Castillo L., Alleyne T.M., Mnaimneh S., Botvinnik O.B., Chan E.T., Khalid F., Zhang W., Newburger D., Jaeger S.A., Morris Q.D., Bulyk M.L., Hughes T.R. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 2008, 133:1266-1276.
8. Blum M., Gaunt S.J., Cho K.W., Steinbeisser H., Blumberg B., Bittner D., De Robertis E.M. Gastrulation in the mouse: The role of the homeobox gene goosecoid. Cell 1992, 69:1097-1106.
9. Blythe S.A., Reid C.D., Kessler D.S., Klein P.S. Chromatin immunoprecipitation in early Xenopus laevis embryos. Dev. Dyn. 2009, 238:1422-1432.
10. Bruce A.E., Howley C., Dixon Fox M., Ho R.K. T-box gene eomesodermin and the homeobox-containing Mix/Bix gene mtx2 regulate epiboly movements in the zebrafish. Dev. Dyn. 2005, 233:105-114.
11. Burglin T. Comprehensive classification of homeobox genes. Guidebook to the Homeobox Genes 1994, Oxford University Press, Oxford. D. Duboule (Ed.).
12. Casey E.S., Tada M., Fairclough L., Wylie C.C., Heasman J., Smith J.C. Bix4 is activated directly by VegT and mediates endoderm formation in Xenopus development. Development 1999, 126:4193-4200.
13. Chambers I., Tomlinson S.R. The transcriptional foundation of pluripotency. Development 2009, 136:2311-2322.
14. Chen W.S., Manova K., Weinstein D.C., Duncan S.A., Plump A.S., Prezioso V.R., Bachvarova R.F., Darnell J.E. Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev. 1994, 8:2466-2477.
15. Chen X., Rubock M.J., Whitman M. A transcriptional partner for MAD proteins in TGF-beta signalling. Nature 1996, 383:691-696.
16. Chen X., Weisberg E., Fridmacher V., Watanabe M., Naco G., Whitman M. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 1997, 389:85-89.
17. Colas A., Cartry J., Buisson I., Umbhauer M., Smith J.C., Riou J.F. Mix.1/2-dependent control of FGF availability during gastrulation is essential for pronephros development in Xenopus. Dev. Biol. 2008, 320:351-365.
18. Conlon F.L., Lyons K.M., Takaesu N., Barth K.S., Kispert A., Herrmann B., Robertson E.J. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 1994, 120:1919-1928.
19. Costello I., Pimeisl I.M., Drager S., Bikoff E.K., Robertson E.J., Arnold S.J. The T-box transcription factor Eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation. Nat. Cell Biol. 2011, 13:1084-1091.
20. D'Amour K.A., Agulnick A.D., Eliazer S., Kelly O.G., Kroon E., Baetge E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 2005, 23:1534-1541.
21. Dale L., Jones C.M. BMP signalling in early Xenopus development. Bioessays 1999, 21:751-760.
22. Danilov V., Blum M., Schweickert A., Campione M., Steinbeisser H. Negative autoregulation of the organizer-specific homeobox gene goosecoid. J. Biol. Chem. 1998, 273:627-635.
23. Davis R.P., Ng E.S., Costa M., Mossman A.K., Sourris K., Elefanty A.G., Stanley E.G. Targeting a GFP reporter gene to the MIXL1 locus of human embryonic stem cells identifies human primitive streak-like cells and enables isolation of primitive hematopoietic precursors. Blood 2008, 111:1876-1884.
24. Derelle R., Lopez P., Le Guyader H., Manuel M. Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol. Dev. 2007, 9:212-219.
25. Doherty J.R., Zhu H., Kuliyev E., Mead P.E. Determination of the minimal domains of Mix.3/Mixer required for endoderm development. Mech. Dev. 2006, 123:56-66.
26. Dosch R., Gawantka V., Delius H., Blumenstock C., Niehrs C. Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. Development 1997, 124:2325-2334.
27. Drakos E., Rassidakis G.Z., Leventaki V., Guo W., Medeiros L.J., Nagarajan L. Differential expression of the human MIXL1 gene product in non-Hodgkin and Hodgkin lymphomas. Hum. Pathol. 2007, 38:500-507.
28. Ecochard V., Cayrol C., Rey S., Foulquier F., Caillol D., Lemaire P., Duprat A.M. A novel Xenopus mix-like gene milk involved in the control of the endomesodermal fates. Development 1998, 125:2577-2585.
29. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
30. Feng X.H., Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 2005, 21:659-693.
31. Gadue P., Huber T.L., Paddison P.J., Keller G.M. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc. Nat. Acad. Sci. U S A 2006, 103:16806-16811.
32. Gehring W.J., Affolter M., Burglin T. Homeodomain proteins. Annu. Rev. Biochem. 1994, 63:487-526.
33. Germain S., Howell M., Esslemont G.M., Hill C.S. Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif. Genes Dev. 2000, 14:435-451.
34. Gilchrist D.A., Fargo D.C., Adelman K. Using ChIP-chip and ChIP-seq to study the regulation of gene expression: Genome-wide localization studies reveal widespread regulation of transcription elongation. Methods 2009, 48:398-408.
35. Guo W., Chan A.P., Liang H., Wieder E.D., Molldrem J.J., Etkin L.D., Nagarajan L. A human Mix-like homeobox gene MIXL shows functional similarity to Xenopus Mix.1. Blood 2002, 100:89-95.
36. Guo W., Nagarajan L. Amino terminal tyrosine phosphorylation of human MIXL1. J. Mol. Signal 2006, 1:6.
37. Hart A.H., Hartley L., Sourris K., Stadler E.S., Li R., Stanley E.G., Tam P.P., Elefanty A.G., Robb L. Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo. Development 2002, 129:3597-3608.
38. Hart A.H., Willson T.A., Wong M., Parker K., Robb L. Transcriptional regulation of the homeobox gene Mixl1 by TGF-beta and FoxH1. Biochem. Biophys. Res. Commun. 2005, 333:1361-1369.
39. Haub O., Goldfarb M. Expression of the fibroblast growth factor-5 gene in the mouse embryo. Development 1991, 112:397-406.
40. Hebert J.M., Boyle M., Martin G.R. mRNA localization studies suggest that murine FGF-5 plays a role in gastrulation. Development 1991, 112:407-415.
41. Hellsten U., Harland R.M., Gilchrist M.J., Hendrix D., Jurka J., Kapitonov V., Ovcharenko I., Putnam N.H., Shu S., Taher L., Blitz I.L., Blumberg B., Dichmann D.S., Dubchak I., Amaya E., Detter J.C., Fletcher R., Gerhard D.S., Goodstein D., Graves T., Grigoriev I.V., Grimwood J., Kawashima T., Lindquist E., Lucas S.M., Mead P.E., Mitros T., Ogino H., Ohta Y., Poliakov A.V., Pollet N., Robert J., Salamov A., Sater A.K., Schmutz J., Terry A., Vize P.D., Warren W.C., Wells D., Wills A., Wilson R.K., Zimmerman L.B., Zorn A.M., Grainger R., Grammer T., Khokha M.K., Richardson P.M., Rokhsar D.S. The genome of the Western clawed frog Xenopus tropicalis. Science 2010, 328:633-636.
42. Henry G.L., Melton D.A. Mixer, a homeobox gene required for endoderm development. Science 1998, 281:91-96.
43. Hirata T., Yamanaka Y., Ryu S.L., Shimizu T., Yabe T., Hibi M., Hirano T. Novel mix-family homeobox genes in zebrafish and their differential regulation. Biochem. Biophys. Res. Commun. 2000, 271:603-609.
44. Hirst C.E., Ng E.S., Azzola L., Voss A.K., Thomas T., Stanley E.G., Elefanty A.G. Transcriptional profiling of mouse and human ES cells identifies SLAIN1, a novel stem cell gene. Dev. Biol. 2006, 293:90-103.
45. Hong S.K., Jang M.K., Brown J.L., McBride A.A., Feldman B. Embryonic mesoderm and endoderm induction requires the actions of non-embryonic Nodal-related ligands and Mxtx2. Development 2011, 138:787-795.
46. Howell M., Inman G.J., Hill C.S. A novel Xenopus Smad-interacting forkhead transcription factor (XFast-3) cooperates with XFast-1 in regulating gastrulation movements. Development 2002, 129:2823-2834.
47. Howell M., Itoh F., Pierreux C.E., Valgeirsdottir S., Itoh S., ten Dijke P., Hill C.S. Xenopus Smad4beta is the co-Smad component of developmentally regulated transcription factor complexes responsible for induction of early mesodermal genes. Dev. Biol. 1999, 214:354-369.
48. Huang H.C., Murtaugh L.C., Vize P.D., Whitman M. Identification of a potential regulator of early transcriptional responses to mesoderm inducers in the frog embryo. EMBO J. 1995, 14:5965-5973.
49. Izumi N., Era T., Akimaru H., Yasunaga M., Nishikawa S. Dissecting the molecular hierarchy for mesendoderm differentiation through a combination of embryonic stem cell culture and RNA interference. Stem Cells 2007, 25:1664-1674.
50. Izzi L., Silvestri C., von Both I., Labbe E., Zakin L., Wrana J.L., Attisano L. Foxh1 recruits Gsc to negatively regulate Mixl1 expression during early mouse development. EMBO J. 2007, 26:3132-3143.
51. Jackson S.A., Schiesser J., Stanley E.G., Elefanty A.G. Differentiating embryonic stem cells pass through 'temporal windows' that mark responsiveness to exogenous and paracrine mesendoderm inducing signals. PLoS One 2010, 5:e10706.
52. Joosten P.H., Toepoel M., van Oosterhout D., Afink G.B., van Zoelen E.J. A regulating element essential for PDGFRA transcription is recognized by neural tube defect-associated PRX homeobox transcription factors. Biochim. Biophys. Acta 2002, 1588:254-260.
53. Keller G. Embryonic stem cell differentiation: Emergence of a new era in biology and medicine. Genes Dev. 2005, 19:1129-1155.
54. Keller G.M. In vitro differentiation of embryonic stem cells. Curr. Opin. Cell Biol. 1995, 7:862-869.
55. Kennedy M., D'Souza S.L., Lynch-Kattman M., Schwantz S., Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 2007, 109:2679-2687.
56. Kikuchi Y., Trinh L.A., Reiter J.F., Alexander J., Yelon D., Stainer D.Y.R. The zebrafish bonnie and clyde gene encodes a Mix family homeodomain protein that regulates the generation of endodermal precursors. Genes Dev. 2000, 14:1279-1289.
57. Kofron M., Puck H., Standley H., Wylie C., Old R., Whitman M., Heasman J. New roles for FoxH1 in patterning the early embryo. Development 2004, 131:5065-5078.
58. Koide T., Hayata T., Cho K.W. Xenopus as a model system to study transcriptional regulatory networks. Proc. Nat. Acad. Sci. U S A 2005, 102:4943-4948.
59. LaBonne C., Whitman M. Mesoderm induction by activin requires FGF-mediated intracellular signals. Development 1994, 120:463-472.
60. Langenbacher A.D., Huang J., Chen Y., Chen J.N. Sodium pump activity in the yolk syncytial layer regulates zebrafish heart tube morphogenesis. Dev Biol. 2012, 362:263-270.
61. Latinkic B.V., Smith J.C. Goosecoid and mix.1 repress Brachyury expression and are required for head formation in Xenopus. Development 1999, 126:1769-1779.
62. Latinkic B.V., Umbhauer M., Neal K.A., Lerchner W., Smith J.C., Cunliffe V. The Xenopus Brachyury promoter is activated by FGF and low concentrations of activin and suppressed by high concentrations of activin and by paired-type homeodomain proteins. Genes Dev. 1997, 11:3265-3276.
63. Lemaire P., Darras S., Caillol D., Kodjabachian L. A role for the vegetally expressed Xenopus gene Mix.1 in endoderm formation and in the restriction of mesoderm to the marginal zone. Development 1998, 125:2371-2380.
64. Levine M., Tjian R. Transcription regulation and animal diversity. Nature 2003, 424:147-151.
65. Lim S.M., Pereira L., Wong M.S., Hirst C.E., Van Vranken B.E., Pick M., Trounson A., Elefanty A.G., Stanley E.G. Enforced expression of Mixl1 during mouse ES cell differentiation suppresses hematopoietic mesoderm and promotes endoderm formation. Stem Cells 2009, 27:363-374.
66. Loose M., Patient R. A genetic regulatory network for Xenopus mesendoderm formation. Dev. Biol. 2004, 271:467-478.
67. Lowe L.A., Yamada S., Kuehn M.R. Genetic dissection of nodal function in patterning the mouse embryo. Development 2001, 128:1831-1843.
68. Luu O., Nagel M., Wacker S., Lemaire P., Winklbauer R. Control of gastrula cell motility by the Goosecoid/Mix.1/ Siamois network: Basic patterns and paradoxical effects. Dev. Dyn. 2008, 237:1307-1320.
69. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Nat. Acad. Sci. U S A 1981, 78:7634-7638.
70. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
71. Mead P.E., Brivanlou I.H., Kelley C.M., Zon L.I. BMP-4-responsive regulation of dorsal-ventral patterning by the homeobox protein Mix.1. Nature 1996, 382:357-360.
72. Mead P.E., Zhou Y., Lustig K.D., Huber T.L., Kirschner M.W., Zon L.I. Cloning of Mix-related homeodomain proteins using fast retrieval of gel shift activities, (FROGS), a technique for the isolation of DNA-binding proteins. Proc. Nat. Acad. Sci. U S A 1998, 95:11251-11256.
73. Mizutani A., Koinuma D., Tsutsumi S., Kamimura N., Morikawa M., Suzuki H.I., Imamura T., Miyazono K., Aburatani H. Cell type-specific target selection by combinatorial binding of Smad2/3 proteins and hepatocyte nuclear factor 4alpha in HepG2 cells. J. Biol. Chem. 2011, 286:29848-29860.
74. Moens C.B., Selleri L. Hox cofactors in vertebrate development. Dev. Biol. 2006, 291:193-206.
75. Mohn D., Chen S.W., Dias D.C., Weinstein D.C., Dyer M.A., Sahr K., Ducker C.E., Zahradka E., Keller G., Zaret K.S., Gudas L.J., Baron M.H. Mouse Mix gene is activated early during differentiation of ES and F9 stem cells and induces endoderm in frog embryos. Dev. Dyn. 2003, 226:446-459.
76. Mossman A.K., Sourris K., Ng E., Stanley E.G., Elefanty A.G. Mixl1 and Oct4 proteins are transiently co-expressed in differentiating mouse and human embryonic stem cells. Stem Cells Dev. 2005, 14:656-663.
77. Ng E.S., Azzola L., Sourris K., Robb L., Stanley E.G., Elefanty A.G. The primitive streak gene Mixl1 is required for efficient haematopoiesis and BMP4-induced ventral mesoderm patterning in differentiating ES cells. Development 2005, 132:873-884.
78. Noyes M.B., Christensen R.G., Wakabayashi A., Stormo G.D., Brodsky M.H., Wolfe S.A. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 2008, 133:1277-1289.
79. Pan G.J., Chang Z.Y., Scholer H.R., Pei D. Stem cell pluripotency and transcription factor Oct4. Cell Res. 2002, 12:321-329.
80. Pan G.J., Pei D.Q. Identification of two distinct transactivation domains in the pluripotency sustaining factor nanog. Cell Res. 2003, 13:499-502.
81. Park C., Afrikanova I., Chung Y.S., Zhang W.J., Arentson E., Fong Gh, G., Rosendahl A., Choi K. A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 2004, 131:2749-2762.
82. Park P.J. ChIP-seq: Advantages and challenges of a maturing technology. Nat. Rev. Genet. 2009, 10:669-680.
83. Peale F.V., Sugden L., Bothwell M. Characterization of CMIX, a chicken homeobox gene related to the Xenopus gene mix.1. Mech. Dev. 1998, 75:167-170.
84. Pearce J.J., Evans M.J. Mml, a mouse mix-like gene expressed in the primitive streak. Mech. Dev. 1999, 87:189-192.
85. Pereira L.A., Wong M.S., Lim S.M., Sides A., Stanley E.G., Elefanty A. Brachyury and related Tbx proteins interact with the Mixl1 homeodomain protein and negatively regulate Mixl1 transcriptional activity. PLoS One 2011, 6:e28394.
86. Pereira L.A., Wong M.S., Mossman A.K., Sourris K., Janes M.E., Knezevic K., Hirst C.E., Lim S.M., Pimanda J.E., Stanley E.G., Elefanty A. Pdgfrα and Flk1 are direct target genes of Mixl1 in differentiating embryonic stem cells. Stem Cell Res. 2012, 8:165-179.
87. Pick M., Azzola L., Mossman A., Stanley E.G., Elefanty A.G. Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. Stem Cells 2007, 25:2206-2214.
88. Poulain M., Lepage T. Mezzo, a paired-like homeobox protein is an immediate target of Nodal signalling and regulates endoderm specification in zebrafish. Development 2002, 129:4901-4914.
89. Robb L., Hartley L., Begley C.G., Brodnicki T.C., Copeland N.G., Gilbert D.J., Jenkins N.A., Elefanty A.G. Cloning, expression analysis, and chromosomal localization of murine and human homologues of a Xenopus mix gene. Dev. Dyn. 2000, 219:497-504.
90. Robb L., Tam P.P. Gastrula organiser and embryonic patterning in the mouse. Semin. Cell Dev. Biol. 2004, 15:543-554.
91. Rosa F.M. Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell 1989, 57:965-974.
92. 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 2000, 404:95-99.
93. Ryan K., Garrett N., Mitchell A., Gurdon J.B. Eomesodermin, a key early gene in Xenopus mesoderm differentiation. Cell 1996, 87:989-1000.
94. Sahr K., Dias D.C., Sanchez R., Chen D., Chen S.W., Gudas L.J., Baron M.H. Structure, upstream promoter region, and functional domains of a mouse and human Mix paired-like homeobox gene. Gene 2002, 291:135-147.
95. Sakaguchi T., Kikuchi Y., Kuroiwa A., Takeda H., Stainier D.Y. The yolk syncytial layer regulates myocardial migration by influencing extracellular matrix assembly in zebrafish. Development 2006, 133:4063-4072.
96. Schier A.F. Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 2003, 19:589-621.
97. Selbach M., Mann M. Protein interaction screening by quantitative immunoprecipitation combined with knockdown (QUICK). Nat. Methods 2006, 3:981-983.
98. Shen M.M. Nodal signaling: Developmental roles and regulation. Development 2007, 134:1023-1034.
99. Shiraki N., Lai C.J., Hishikari Y., Kume S. TGF-beta signaling potentiates differentiation of embryonic stem cells to Pdx-1 expressing endodermal cells. Genes Cells 2005, 10:503-516.
100. Smith J., Wardle F., Loose M., Stanley E., Patient R. Germ layer induction in ESC--following the vertebrate roadmap. Curr. Protoc. Stem Cell Biol 2007, Chapter 1, Unit 1D 1.
101. Smith J.C. Making mesoderm-upstream and downstream of Xbra. Int. J. Dev. Biol. 2001, 45:219-224.
102. Smith J.C., Price B.M., Van Nimmen K., Huylebroeck D. Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 1990, 345:729-731.
103. Stein S., Roeser T., Kessel M. CMIX, a paired-type homeobox gene expressed before and during formation of the avian primitive streak. Mech. Dev. 1998, 75:163-165.
104. Swiers G., Chen Y.H., Johnson A.D., Loose M. A conserved mechanism for vertebrate mesoderm specification in urodele amphibians and mammals. Dev. Biol. 2010, 343:138-152.
105. Tada M., Casey E.S., Fairclough L., Smith J.C. Bix1, a direct target of Xenopus T-box genes, causes formation of ventral mesoderm and endoderm. Development 1998, 125:3997-4006.
106. Tada S., Era T., Furusawa C., Sakurai H., Nishikawa S., Kinoshita M., Nakao K., Chiba T., Nishikawa S. Characterization of mesendoderm: A diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 2005, 132:4363-4374.
107. Tam P.P., Khoo P.L., Lewis S.L., Bildsoe H., Wong N., Tsang T.E., Gad J.M., Robb L. Sequential allocation and global pattern of movement of the definitive endoderm in the mouse embryo during gastrulation. Development 2007, 134:251-260.
108. Trindade M., Messenger N., Papin C., Grimmer D., Fairclough L., Tada M., Smith J.C. Regulation of apoptosis in theXenopus embryo by Bix3. Development 2003, 130:4611-4622.
109. Trinh L.A., Meyer D., Stainier D.Y. The Mix family homeodomain gene bonnie and clyde functions with other components of the Nodal signaling pathway to regulate neural patterning in zebrafish. Development 2003, 130:4989-4998.
110. Tucker S.C., Wisdom R. Site-specific heterodimerization by paired class homeodomain proteins mediates selective transcriptional responses. J. Biol. Chem. 1999, 274:32325-32332.
111. van den Eijnden-Van Raaij A.J., van Zoelent E.J., van Nimmen K., Koster C.H., Snoek G.T., Durston A.J., Huylebroeck D. Activin-like factor from a Xenopus laevis cell line responsible for mesoderm induction. Nature 1990, 345:732-734.
112. Vize P.D. DNA sequences mediating the transcriptional response of the Mix.2 homeobox gene to mesoderm induction. Dev. Biol. 1996, 177:226-231.
113. Wardle F.C., Papaioannou V.E. Teasing out T-box targets in early mesoderm. Curr. Opin. Genet. Dev. 2008, 18:418-425.
114. Watabe T., Kim S., Candia A., Rothbacher U., Hashimoto C., Inoue K., Cho K.W. Molecular mechanisms of Spemann's organizer formation: Conserved growth factor synergy between Xenopus and mouse. Genes Dev. 1995, 9:3038-3050.
115. Weisberg E., Winnier G.E., Chen X., Farnsworth C.L., Hogan B.L., Whitman M. A mouse homologue of FAST-1 transduces TGF beta superfamily signals and is expressed during early embryogenesis. Mech. Dev. 1998, 79:17-27.
116. Wilkinson D.G., Bhatt S., Herrmann B.G. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 1990, 343:657-659.
117. Willey S., Ayuso-Sacido A., Zhang H., Fraser S.T., Sahr K.E., Adlam M.J., Kyba M., Daley G.Q., Keller G., Baron M.H. Acceleration of mesoderm development and expansion of hematopoietic progenitors in differentiating ES cells by the mouse Mix-like homeodomain transcription factor. Blood 2006, 107:3122-3130.
118. Wilson D., Sheng G., Lecuit T., Dostatni N., Desplan C. Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 1993, 7:2120-2134.
119. Wilson D.S., Sheng G., Jun S., Desplan C. Conservation and diversification in homeodomain-DNA interactions: A comparative genetic analysis. Proc. Nat. Acad. Sci. U S A 1996, 93:6886-6891.
120. Wolpert L. The Triumph of the Embryo 1991, Oxford University Press, New York.
121. Xanthos J.B., Kofron M., Tao Q., Schaible K., Wylie C., Heasman J. The roles of three signaling pathways in the formation and function of the Spemann organizer. Development 2002, 129:4027-4043.
122. Xanthos J.B., Kofron M., Wylie C., Heasman J. Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 2001, 128:167-180.
123. Xi Q., Wang Z., Zaromytidou A.-I., Zhang X.H.-F., Chow-Tsang L.-F., Liu J.X., Kim H., Barias A., Manova-Todora K., Kaartinen V., Studer L., Mark W., Patel D.J., Massagué J. A poised chromatin platform for TGF-Β access to master regulators. Cell 2011, 147:1511-1524.
124. Xu C., Fan Z.P., Muller P., Fogley R., Dibiase A., Trompouki E., Unternaehrer J., Xiong F., Torregroza I., Evans T., Megason S.G., Daley G.Q., Schier A.F., Young R.A., Zon L.I. Nanog-like Regulates Endoderm Formation through the Mxtx2-Nodal Pathway. Dev. Cell 2012, 22:625-638.
125. Yamamoto S., Hikasa H., Ono H., Taira M. Molecular link in the sequential induction of the Spemann organizer: Direct activation of the cerberus gene by Xlim-1, Xotx2, Mix.1, and Siamois, immediately downstream from Nodal and Wnt signaling. Dev. Biol. 2003, 257:190-204.
126. Zhang H., Fraser S.T., Papazoglu C., Hoatlin M.E., Baron M.H. Transcriptional activation by the Mixl1 homeodomain protein in differentiating mouse embryonic stem cells. Stem Cells 2009, 27:2884-2895.
127. Zhang J., King M.L. Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. Development 1996, 122:4119-4129.
128. Zhu H., Doherty J.R., Kuliyev E., Mead P.E. CDK9/cyclin complexes modulate endoderm induction by direct interaction with Mix.3/mixer. Dev. Dyn. 2009, 238:1346-1357.