Erf and Etv3l are retinoic acid-inducible repressors required for primary neurogenesis

Development (Cambridge)

Volumn 140, Issue 15, 2013, Pages 3095-3106

  Janesick, Amanda ^a   Abbey, Rachelle ^a   Chung, Connie ^a   Liu, Sophia ^a   Taketani, Mao ^a,b   Blumberg, Bruce ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Differentiation; Ets repressors; Neural progenitor; Primary neurogenesis; Proliferation; Retinoic acid; Xenopus

Indexed keywords

4 [2 [5,6 DIHYDRO 5,5 DIMETHYL 8 (4 METHYLPHENYL) 2 NAPHTHYL]ETHYNYL]BENZOIC ACID; CYTOCHROME P450 26A1; FOXD4L1 PROTEIN; GEMININ; HISTONE H3; HISTONE H4; MESSENGER RNA; PROTEIN; RALDH2 PROTEIN; RETINOIC ACID; RETINOIC ACID INDUCIBLE PROTEIN I; RETINOIC ACID RECEPTOR ALPHA; RETINOIC ACID RECEPTOR GAMMA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ERF; TRANSCRIPTION FACTOR ETS 2; TRANSCRIPTION FACTOR ETV3L; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE CONSTRUCT; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; LOSS OF FUNCTION MUTATION; MICROTUBULE ASSEMBLY; MOLECULAR CLONING; MONOSYNAPTIC PATHWAY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; UPREGULATION; XENOPUS;

DIFFERENTIATION; ETS REPRESSORS; NEURAL PROGENITOR; PRIMARY NEUROGENESIS; PROLIFERATION; RETINOIC ACID; XENOPUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CELL PROLIFERATION; FIBROBLAST GROWTH FACTORS; GENE KNOCKDOWN TECHNIQUES; IN SITU HYBRIDIZATION; NEUROGENESIS; PROTO-ONCOGENE PROTEINS C-ETS; RECEPTORS, RETINOIC ACID; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRETINOIN; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84880307608     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.093716     Document Type: Article

References (101)

1. Anderson, R. B. and Holt, C. E. (2002). Expression of UNC-5 in the developing Xenopus visual system. Mech. Dev. 118, 157-160.
2. Andrews, P. W. (1984). Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev. Biol. 103, 285-293.
3. Archer, T. C., Jin, J. and Casey, E. S. (2011). Interaction of Sox1, Sox2, Sox3 and Oct4 during primary neurogenesis. Dev. Biol. 350, 429-440.
4. Arima, K., Shiotsugu, J., Niu, R., Khandpur, R., Martinez, M., Shin, Y., Koide, T., Cho, K. W., Kitayama, A., Ueno, N. et al. (2005). Global analysis of RARresponsive genes in the Xenopus neurula using cDNA microarrays. Dev. Dyn. 232, 414-431.
5. Aruga, J. (2004). The role of Zic genes in neural development. Mol. Cell. Neurosci. 26, 205-221.
6. Aruga, J. and Mikoshiba, K. (2011). Role of BMP, FGF, calcium signaling, and Zic proteins in vertebrate neuroectodermal differentiation. Neurochem. Res. 36, 1286-1292.
7. Aruga, J., Tohmonda, T., Homma, S. and Mikoshiba, K. (2002). Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev. Biol. 244, 329-341.
8. Balmer, J. E. and Blomhoff, R. (2002). Gene expression regulation by retinoic acid. J. Lipid Res. 43, 1773-1808.
9. Bellefroid, E. J., Bourguignon, C., Hollemann, T., Ma, Q., Anderson, D. J., Kintner, C. and Pieler, T. (1996). X-MyT1, a Xenopus C2HC-type zinc finger protein with a regulatory function in neuronal differentiation. Cell 87, 1191-1202.
10. Bertrand, V., Hudson, C., Caillol, D., Popovici, C. and Lemaire, P. (2003). Neural tissue in ascidian embryos is induced by FGF9/16/20, acting via a combination of maternal GATA and Ets transcription factors. Cell 115, 615-627.
11. Blumberg, B., Bolado, J., Jr, Moreno, T. A., Kintner, C., Evans, R. M. and Papalopulu, N. (1997). An essential role for retinoid signaling in anteroposterior neural patterning. Development 124, 373-379.
12. Branney, P. A., Faas, L., Steane, S. E., Pownall, M. E. and Isaacs, H. V. (2009). Characterisation of the fibroblast growth factor dependent transcriptome in early development. PLoS ONE 4, e4951.
13. Brewster, R., Lee, J. and Ruiz i Altaba, A. (1998). Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 393, 579-583.
14. Bylund, M., Andersson, E., Novitch, B. G. and Muhr, J. (2003). Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 6, 1162-1168.
15. Carlson, S. M., Chouinard, C. R., Labadorf, A., Lam, C. J., Schmelzle, K., Fraenkel, E. and White, F. M. (2011). Large-scale discovery of ERK2 substrates identifies ERK-mediated transcriptional regulation by ETV3. Sci. Signal. 4, rs11.
16. Chalmers, A. D., Welchman, D. and Papalopulu, N. (2002). Intrinsic differences between the superficial and deep layers of the Xenopus ectoderm control primary neuronal differentiation. Dev. Cell 2, 171-182.
17. Chamorro-Garcia, R., Kirchner, S., Li, X., Janesick, A., Casey, S. C., Chow, C. and Blumberg, B. (2012). Bisphenol A diglycidyl ether induces adipogenic differentiation of multipotent stromal stem cells through a peroxisome proliferator-activated receptor gamma-independent mechanism. Environ. Health Perspect. 120, 984-989.
18. Chen, J., Lai, F. and Niswander, L. (2012). The ubiquitin ligase mLin41 temporally promotes neural progenitor cell maintenance through FGF signaling. Genes Dev. 26, 803-815.
19. Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D. and Kintner, C. (1995). Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761-766.
20. Cornish, E. J., Hassan, S. M., Martin, J. D., Li, S. and Merzdorf, C. S. (2009). A microarray screen for direct targets of Zic1 identifies an aquaporin gene, aqp- 3b, expressed in the neural folds. Dev. Dyn. 238, 1179-1194.
21. Denny, P., Swift, S., Brand, N., Dabhade, N., Barton, P. and Ashworth, A. (1992). A conserved family of genes related to the testis determining gene, SRY. Nucleic Acids Res. 20, 2887.
22. Diez del Corral, R. and Storey, K. G. (2004). Opposing FGF and retinoid pathways: a signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 26, 857-869.
23. Diez del Corral, R., Olivera-Martinez, I., Goriely, A., Gale, E., Maden, M. and Storey, K. (2003). Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40, 65-79.
24. Dorey, K. and Amaya, E. (2010). FGF signalling: diverse roles during early vertebrate embryogenesis. Development 137, 3731-3742.
25. Duester, G. (2008). Retinoic acid synthesis and signaling during early organogenesis. Cell 134, 921-931.
26. Elkabetz, Y., Panagiotakos, G., Al Shamy, G., Socci, N. D., Tabar, V. and Studer, L. (2008). Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 22, 152-165.
27. Franco, P. G., Paganelli, A. R., Lopez, S. L. and Carrasco, A. E. (1999). Functional association of retinoic acid and hedgehog signaling in Xenopus primary neurogenesis. Development 126, 4257-4265.
28. Gudas, L. J. (1992). Retinoids, retinoid-responsive genes, cell differentiation, and cancer. Cell Growth Differ. 3, 655-662.
29. Hellsten, U., Harland, R. M., Gilchrist, M. J., Hendrix, D., Jurka, J., Kapitonov, V., Ovcharenko, I., Putnam, N. H., Shu, S., Taher, L. et al. (2010). The genome of the Western clawed frog Xenopus tropicalis. Science 328, 633-636.
30. Hendzel, M. J., Wei, Y., Mancini, M. A., Van Hooser, A., Ranalli, T., Brinkley, B. R., Bazett-Jones, D. P. and Allis, C. D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360.
31. Hester, K. D., Verhelle, D., Escoubet-Lozach, L., Luna, R., Rose, D. W. and Glass, C. K. (2007). Differential repression of c-myc and cdc2 gene expression by ERF and PE-1/METS. Cell Cycle 6, 1594-1604.
32. Hollenhorst, P. C., McIntosh, L. P. and Graves, B. J. (2011). Genomic and biochemical insights into the specificity of ETS transcription factors. Annu. Rev. Biochem. 80, 437-471.
33. Janesick, A., Shiotsugu, J., Taketani, M. and Blumberg, B. (2012). RIPPLY3 is a retinoic acid-inducible repressor required for setting the borders of the preplacodal ectoderm. Development 139, 1213-1224.
34. Kaldis, P. and Richardson, H. E. (2012). When cell cycle meets development. Development 139, 225-230.
35. Kee, N., Wilson, N., De Vries, M., Bradford, D., Key, B. and Cooper, H. M. (2008). Neogenin and RGMa control neural tube closure and neuroepithelial morphology by regulating cell polarity. J. Neurosci. 28, 12643-12653.
36. Klappacher, G. W., Lunyak, V. V., Sykes, D. B., Sawka-Verhelle, D., Sage, J., Brard, G., Ngo, S. D., Gangadharan, D., Jacks, T., Kamps, M. P. et al. (2002). An induced Ets repressor complex regulates growth arrest during terminal macrophage differentiation. Cell 109, 169-180.
37. Klein, S. L., Strausberg, R. L., Wagner, L., Pontius, J., Clifton, S. W. and Richardson, P. (2002). Genetic and genomic tools for Xenopus research: The NIH Xenopus initiative. Dev. Dyn. 225, 384-391.
38. Koide, T., Downes, M., Chandraratna, R. A., Blumberg, B. and Umesono, K. (2001). Active repression of RAR signaling is required for head formation. Genes Dev. 15, 2111-2121.
39. Koinuma, D., Tsutsumi, S., Kamimura, N., Taniguchi, H., Miyazawa, K., Sunamura, M., Imamura, T., Miyazono, K. and Aburatani, H. (2009). Chromatin immunoprecipitation on microarray analysis of Smad2/3 binding sites reveals roles of ETS1 and TFAP2A in transforming growth factor beta signaling. Mol. Cell. Biol. 29, 172-186.
40. Kolm, P. J. and Sive, H. L. (1995). Efficient hormone-inducible protein function in Xenopus laevis. Dev. Biol. 171, 267-272.
41. Kroll, K. L., Salic, A. N., Evans, L. M. and Kirschner, M. W. (1998). Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 125, 3247-3258.
42. Kuo, J. S., Patel, M., Gamse, J., Merzdorf, C., Liu, X., Apekin, V. and Sive, H. (1998). Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 125, 2867-2882.
43. Laudet, V., Hanni, C., Stehelin, D. and Duterque-Coquillaud, M. (1999). Molecular phylogeny of the ETS gene family. Oncogene 18, 1351-1359.
44. Le Gallic, L., Sgouras, D., Beal, G., Jr and Mavrothalassitis, G. (1999). Transcriptional repressor ERF is a Ras/mitogen-activated protein kinase target that regulates cellular proliferation. Mol. Cell. Biol. 19, 4121-4133.
45. Lee, H. C., Tseng, W. A., Lo, F. Y., Liu, T. M. and Tsai, H. J. (2009). FoxD5 mediates anterior-posterior polarity through upstream modulator Fgf signaling during zebrafish somitogenesis. Dev. Biol. 336, 232-245.
46. Li, R., Pei, H. and Watson, D. K. (2000). Regulation of Ets function by protein - protein interactions. Oncogene 19, 6514-6523.
47. Lim, L. S., Loh, Y. H., Zhang, W., Li, Y., Chen, X., Wang, Y., Bakre, M., Ng, H. H. and Stanton, L. W. (2007). Zic3 is required for maintenance of pluripotency in embryonic stem cells. Mol. Biol. Cell 18, 1348-1358.
48. Lim, J. W., Hummert, P., Mills, J. C. and Kroll, K. L. (2011). Geminin cooperates with Polycomb to restrain multi-lineage commitment in the early embryo. Development 138, 33-44.
49. Lin, C. Y., Su, W. T. and Li, L. T. (2012). Heat-induced antigen retrieval applied in zebrafish: whole-mount in situ immunofluorescence microscopy. Microsc. Microanal. 18, 493-496.
50. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
51. Maden, M. (2007). Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 8, 755-765.
52. Marchal, L., Luxardi, G., Thome, V. and Kodjabachian, L. (2009). BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proc. Natl. Acad. Sci. USA 106, 17437-17442.
53. Mason, I. (2007). Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat. Rev. Neurosci. 8, 583-596.
54. Mathews, M. B., Bernstein, R. M., Franza, B. R., Jr and Garrels, J. I. (1984). Identity of the proliferating cell nuclear antigen and cyclin. Nature 309, 374-376.
55. Mavrothalassitis, G. and Ghysdael, J. (2000). Proteins of the ETS family with transcriptional repressor activity. Oncogene 19, 6524-6532.
56. McGarry, T. J. and Kirschner, M. W. (1998). Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93, 1043-1053.
57. Merzdorf, C. S. (2007). Emerging roles for zic genes in early development. Dev. Dyn. 236, 922-940.
58. Miyagi, S., Kato, H. and Okuda, A. (2009). Role of SoxB1 transcription factors in development. Cell. Mol. Life Sci. 66, 3675-3684.
59. Mizuseki, K., Kishi, M., Matsui, M., Nakanishi, S. and Sasai, Y. (1998). Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development 125, 579-587.
60. Moody, S. A. and Je, H. S. (2002). Neural induction, neural fate stabilization, and neural stem cells. Scientific World Journal 2, 1147-1166.
61. Moreno, T. A. and Kintner, C. (2004). Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev. Cell 6, 205-218.
62. Morikawa, M., Koinuma, D., Tsutsumi, S., Vasilaki, E., Kanki, Y., Heldin, C. H., Aburatani, H. and Miyazono, K. (2011). ChIP-seq reveals cell type-specific binding patterns of BMP-specific Smads and a novel binding motif. Nucleic Acids Res. 39, 8712-8727.
63. Muffato, M., Louis, A., Poisnel, C. E. and Roest Crollius, H. (2010). Genomicus: a database and a browser to study gene synteny in modern and ancestral genomes. Bioinformatics 26, 1119-1121.
64. Nakata, K., Nagai, T., Aruga, J. and Mikoshiba, K. (1997). Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc. Natl. Acad. Sci. USA 94, 11980-11985.
65. Nakata, K., Nagai, T., Aruga, J. and Mikoshiba, K. (1998). Xenopus Zic family and its role in neural and neural crest development. Mech. Dev. 75, 43-51.
66. Neilson, K. M., Klein, S. L., Mhaske, P., Mood, K., Daar, I. O. and Moody, S. A. (2012). Specific domains of FoxD4/5 activate and repress neural transcription factor genes to control the progression of immature neural ectoderm to differentiating neural plate. Dev. Biol. 365, 363-375.
67. Niederreither, K. and Dolle, P. (2008). Retinoic acid in development: towards an integrated view. Nat. Rev. Genet. 9, 541-553.
68. Nieuwkoop, P. O. and Faber, J. (1967). A Normal Table of Xenopus Laevis (Daudin): A Systematical and Chronological Survey of The Development From The Fertilized Egg Till The End of Metamorphosis. Amsterdam: North-Holland Publishing Company.
69. Oikawa, T. and Yamada, T. (2003). Molecular biology of the Ets family of transcription factors. Gene 303, 11-34.
70. Papadaki, C., Alexiou, M., Cecena, G., Verykokakis, M., Bilitou, A., Cross, J. C., Oshima, R. G. and Mavrothalassitis, G. (2007). Transcriptional repressor erf determines extraembryonic ectoderm differentiation. Mol. Cell. Biol. 27, 5201-5213.
71. Papalopulu, N. and Kintner, C. (1996). A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm. Development 122, 3409-3418.
72. Penzel, R., Oschwald, R., Chen, Y., Tacke, L. and Grunz, H. (1997). Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int. J. Dev. Biol. 41, 667-677.
73. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
74. Rhinn, M. and Dolle, P. (2012). Retinoic acid signalling during development. Development 139, 843-858.
75. Rogers, C. D., Moody, S. A. and Casey, E. S. (2009). Neural induction and factors that stabilize a neural fate. Birth Defects Res. C Embryo Today 87, 249-262.
76. Sawka-Verhelle, D., Escoubet-Lozach, L., Fong, A. L., Hester, K. D., Herzig, S., Lebrun, P. and Glass, C. K. (2004). PE-1/METS, an antiproliferative Ets repressor factor, is induced by CREB-1/CREM-1 during macrophage differentiation. J. Biol. Chem. 279, 17772-17784.
77. Seo, S., Herr, A., Lim, J. W., Richardson, G. A., Richardson, H. and Kroll, K. L. (2005a). Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev. 19, 1723-1734.
78. Seo, S., Richardson, G. A. and Kroll, K. L. (2005b). The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD. Development 132, 105-115.
79. Sgouras, D. N., Athanasiou, M. A., Beal, G. J., Jr, Fisher, R. J., Blair, D. G. and Mavrothalassitis, G. J. (1995). ERF: an ETS domain protein with strong transcriptional repressor activity, can suppress ets-associated tumorigenesis and is regulated by phosphorylation during cell cycle and mitogenic stimulation. EMBO J. 14, 4781-4793.
80. Sharpe, C. R. (1992). Two isoforms of retinoic acid receptor alpha expressed during Xenopus development respond to retinoic acid. Mech. Dev. 39, 81-93.
81. Sharpe, C. R. and Goldstone, K. (1997). Retinoid receptors promote primary neurogenesis in Xenopus. Development 124, 515-523.
82. Sharpe, C. and Goldstone, K. (2000). The control of Xenopus embryonic primary neurogenesis is mediated by retinoid signalling in the neurectoderm. Mech. Dev. 91, 69-80.
83. Sharrocks, A. D. (2001). The ETS-domain transcription factor family. Nat. Rev. Mol. Cell Biol. 2, 827-837.
84. Shiotsugu, J., Katsuyama, Y., Arima, K., Baxter, A., Koide, T., Song, J., Chandraratna, R. A. and Blumberg, B. (2004). Multiple points of interaction between retinoic acid and FGF signaling during embryonic axis formation. Development 131, 2653-2667.
85. Sive, H. L. and Cheng, P. F. (1991). Retinoic acid perturbs the expression of Xhox.lab genes and alters mesodermal determination in Xenopus laevis. Genes Dev. 5, 1321-1332.
86. Sive, H. L., Grainger, R. M. and Harland, R. M. (1998). Early Development of Xenopus Laevis. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
87. Solter, M., Koster, M., Hollemann, T., Brey, A., Pieler, T. and Knochel, W. (1999). Characterization of a subfamily of related winged helix genes, XFD- 12/12_/12_ (XFLIP), during Xenopus embryogenesis. Mech. Dev. 89, 161-165.
88. Spella, M., Britz, O., Kotantaki, P., Lygerou, Z., Nishitani, H., Ramsay, R. G., Flordellis, C., Guillemot, F., Mantamadiotis, T. and Taraviras, S. (2007). Licensing regulators Geminin and Cdt1 identify progenitor cells of the mouse CNS in a specific phase of the cell cycle. Neuroscience 147, 373-387.
89. Sullivan, S. A., Akers, L. and Moody, S. A. (2001). foxD5a, a Xenopus winged helix gene, maintains an immature neural ectoderm via transcriptional repression that is dependent on the C-terminal domain. Dev. Biol. 232, 439-457.
90. Tabar, V., Panagiotakos, G., Greenberg, E. D., Chan, B. K., Sadelain, M., Gutin, P. H. and Studer, L. (2005). Migration and differentiation of neural precursors derived from human embryonic stem cells in the rat brain. Nat. Biotechnol. 23, 601-606.
91. Tabb, M. M., Kholodovych, V., Grun, F., Zhou, C., Welsh, W. J. and Blumberg, B. (2004). Highly chlorinated PCBs inhibit the human xenobiotic response mediated by the steroid and xenobiotic receptor (SXR). Environ. Health Perspect. 112, 163-169.
92. Tropepe, V., Li, S., Dickinson, A., Gamse, J. T. and Sive, H. L. (2006). Identification of a BMP inhibitor-responsive promoter module required for expression of the early neural gene zic1. Dev. Biol. 289, 517-529.
93. Verykokakis, M., Papadaki, C., Vorgia, E., Le Gallic, L. and Mavrothalassitis, G. (2007). The RAS-dependent ERF control of cell proliferation and differentiation is mediated by c-Myc repression. J. Biol. Chem. 282, 30285-30294.
94. Wagner, L. E., 2nd, Li, W. H., Joseph, S. K. and Yule, D. I. (2004). Functional consequences of phosphomimetic mutations at key cAMP-dependent protein kinase phosphorylation sites in the type 1 inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 279, 46242-46252.
95. Wasylyk, B., Hagman, J. and Gutierrez-Hartmann, A. (1998). Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem. Sci. 23, 213-216.
96. Wegner, M. and Stolt, C. C. (2005). From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci. 28, 583-588.
97. Wills, A. E., Choi, V. M., Bennett, M. J., Khokha, M. K. and Harland, R. M. (2010). BMP antagonists and FGF signaling contribute to different domains of the neural plate in Xenopus. Dev. Biol. 337, 335-350.
98. Wilson, P. A. and Hemmati-Brivanlou, A. (1995). Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376, 331-333.
99. Wullimann, M. F., Rink, E., Vernier, P. and Schlosser, G. (2005). Secondary neurogenesis in the brain of the African clawed frog, Xenopus laevis, as revealed by PCNA, Delta-1, Neurogenin-related-1, and NeuroD expression. J. Comp. Neurol. 489, 387-402.
100. Yan, B., Neilson, K. M. and Moody, S. A. (2009). foxD5 plays a critical upstream role in regulating neural ectodermal fate and the onset of neural differentiation. Dev. Biol. 329, 80-95.
101. Yan, B., Neilson, K. M. and Moody, S. A. (2010). Microarray identification of novel downstream targets of FoxD4L1/D5, a critical component of the neural ectodermal transcriptional network. Dev. Dyn. 239, 3467-3480.