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Role of SoxB1 transcription factors in development

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Abstract

SoxB1 factors, which include Sox1, 2, and 3, share more than 90% amino acid identity in their DNA binding HMG box and participate in diverse developmental events. They are known to exert cell-type-specific functions in concert with other transcription factors on Sox factor-dependent regulatory enhancers. Due to the high degree of sequence similarity both within and outside the HMG box, SoxB1 members show almost identical biological activities. As a result, they exhibit strong functional redundancy in regions where SoxB1 members are coexpressed, such as neural stem/progenitor cells in the developing central nervous system.

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References

  1. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:240–244

    Article  CAS  PubMed  Google Scholar 

  2. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, Vivian N, Goodfellow P, Lovell-Badge R (1990) A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346:245–250

    Article  CAS  PubMed  Google Scholar 

  3. Wright EM, Snopek B, Koopman P (1993) Seven new members of the Sox gene family expressed during mouse development. Nucleic Acids Res 21:744

    Article  CAS  PubMed  Google Scholar 

  4. Kiefer JC (2007) Back to basics: Sox genes. Dev Dyn 236:2356–2366

    Article  CAS  PubMed  Google Scholar 

  5. Bowles J, Schepers G, Koopman P (2000) Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227:239–255

    Article  CAS  PubMed  Google Scholar 

  6. Pevny LH, Lovell-Badge R (1997) Sox genes find their feet. Curr Opin Genet Dev 7:338–344

    Article  CAS  PubMed  Google Scholar 

  7. Wegner M (1999) From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 27:1409–1420

    Article  CAS  PubMed  Google Scholar 

  8. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R (2003) Multiple cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:126–140

    Article  CAS  PubMed  Google Scholar 

  9. Graham V, Khudyakou J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749–765

    Article  CAS  PubMed  Google Scholar 

  10. Kamachi Y, Uchikawa M, Kondoh H (2000) Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet 16:182–187

    Article  CAS  PubMed  Google Scholar 

  11. Harley VR, Lovell-Badge R, Goodfellow PN (1994) Definition of a consensus DNA binding site for SRY. Nucleic Acids Res 22:1500–1501

    Article  CAS  PubMed  Google Scholar 

  12. van de Wetering M, Clevers H (1992) Sequence-specific interaction of the HMG box proteins TCF-1 and SRY occurs within the minor groove of a Watson-Crick double helix. EMBO J 11:3039–3044

    PubMed  Google Scholar 

  13. Yuan H, Corbi N, Basilico C, Dailey L (1995) Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 9:2635–2645

    Article  CAS  PubMed  Google Scholar 

  14. Ambrosetti DC, Basilico C, Dailey L (1997) Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on protein-protein interactions facilitated by a specifc spatial arrangement of factor binding sites. Mol Cell Biol 17:6321–6329

    CAS  PubMed  Google Scholar 

  15. Ambrosetti DC, Scholer HR, Dailey L, Basilico C (2000) Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synergistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer. J Biol Chem 275:23387–23397

    Article  CAS  PubMed  Google Scholar 

  16. Okamoto K, Okazawa H, Okuda A, Sakai M, Muramatsu M, Hamada H (1990) A novel octamer binding transcription factor is differentially expressed in early embryonic cells. Cell 60:461–472

    Article  CAS  PubMed  Google Scholar 

  17. Rosner MB, Vigano MA, Ozato K, Timmons PM, Poirier F, Rigby PWJ, Staudt LM (1990) A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345:686–692

    Article  CAS  PubMed  Google Scholar 

  18. Scholer HR, Ruppert S, Suzuki N, Chowdhury K, Gruss P (1990) New type of POU domain in germ line-specific protein Oct-4. Nature 344:435–439

    Article  CAS  PubMed  Google Scholar 

  19. Okuda A, Fukushima A, Nishimoto M, Orimo A, Yamagishi T, Nabeshima Y, Kuro-o M, Nabeshima Y, Boon K, Keaveney M, Stunnenberg HG, Muramatsu M (1998) UTF1, a novel transcriptional coactivator expressed in pluripotent embryonic stem cells and extra-embryonic cells. EMBO J 17:2019-2032

    Article  CAS  PubMed  Google Scholar 

  20. Fukushima A, Okuda A, Nishimoto M, Seki N, Hori T, Muramatsu M (1998) Characterization of functional domains of an embryonic stem cell coactivator UTF1 which are conserved and essential for potentiation of ATF-2 activity. J Biol Chem 273:25840–25849

    Article  CAS  PubMed  Google Scholar 

  21. Nishimoto M, Fukushima A, Okuda A, Muramatsu M (1999) The gene for the embryonic stem cell coactivator UTF1 carries a regulatory element which selectively interacts with a complex composed of Oct-3/4 and Sox-2. Mol Cell Biol 19:5453–5465

    CAS  PubMed  Google Scholar 

  22. Nowling TK, Johnson LR, Wiebe MS, Rizzino A (2000) Identification of the transactivation domain of the transcription factor Sox-2 and an associated co-activator. J Biol Chem 275:3810–3818

    Article  CAS  PubMed  Google Scholar 

  23. Nowling T, Bernadt C, Johnson L, Desler M, Rizzino A (2003) The co-activator p300 associates physically with and can mediate the action of the distal enhancer of the FGF-4 gene. J Biol Chem 278:13696–13705

    Article  CAS  PubMed  Google Scholar 

  24. Kamachi Y, Uchikawa M, Tanouchi A, Sekido R, Kondoh H (2001) Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev 15:1272–1286

    Article  CAS  PubMed  Google Scholar 

  25. Kondoh H, Uchikawa M, Kamachi Y (2004) Interplay of Pax6 and SOX2 in lens development as a paradigm of genetic switch mechanisms for cell differentiation. Int J Dev Biol 48:819–827

    Article  CAS  PubMed  Google Scholar 

  26. Inoue M, Kamachi Y, Matsunami H, Imada K, Uchikawa M, Kondoh H (2007) PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 12:1049–1061

    Article  CAS  PubMed  Google Scholar 

  27. Josephson R, Muller T, Picket J, Okabe S, Reynolds K, Turner PA, Zimmer A, McKay RD (1998) POU transcription factors control expression of CNS stem cell-specific gene. Development 125:3087–3100

    CAS  PubMed  Google Scholar 

  28. Tanaka S, Kamachi Y, Tanouchi A, Jing N, Kondoh H (2004) Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol Cell Biol 24:8834–8846

    Article  CAS  PubMed  Google Scholar 

  29. Tomioka M, Nishimoto M, Miyagi S, Katayanagi T, Fukui N, Niwa H, Muramatsu M, Okuda A (2002) Identification of Sox-2 regulatory region which is under the control of Oct-3/4-Sox2 complex. Nucleic Acids Res 30:3202–3213

    Article  CAS  PubMed  Google Scholar 

  30. Miyagi S, Saito T, Mizutani K, Masuyama N, Gotoh Y, Iwama A, Nakauchi H, Masui S, Niwa H, Nishimoto M, Muramatsu M, Okuda A (2004) The Sox-2 regulatory regions display their activities in two distinct types of multipotent stem cells. Mol Cell Biol 24:4207–4220

    Article  CAS  PubMed  Google Scholar 

  31. Miyagi S, Nishimoto M, Saito T, Ninomiya M, Sawamoto K, Okano H, Muramatsu M, Oguro H, Iwama A, Okuda A (2006) The Sox2 regulatory region 2 functions as neural stem cell-specific enhancer in the telencephalon. J Biol Chem 281:12281–13374

    Article  Google Scholar 

  32. Zappone MV, Galli R, Catena R, Meani N, De Biasi S, Mattei E, Tiveron C, Vescovi AL, Lovell-Badge R, Ottolenghi S, Nicolis SK (2000) Sox2 regulatory sequences direct expression of a β-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 127:2367–2382

    CAS  PubMed  Google Scholar 

  33. Catena R, Tiveron C, Ronchi A, Porta S, Ferri A, Tatangelo L, Cavallaro M, Favaro R, Ottolenghi S, Reinbold R, Scholer H, Nicolis SK (2004) Conserved POU binding DNA sites in the Sox2 upstream enhancer regulate gene expression in embryonic and neural stem cells. J Biol Chem 279:41846–41857

    Article  CAS  PubMed  Google Scholar 

  34. Uchikawa M, Ishida Y, Takemoto T, Kamachi Y, Kondoh H (2003) Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell 5:509–519

    Article  Google Scholar 

  35. Kondoh H, Uchikawa M (2008) Dissection of chick genomic regulatory regions. Methods Cell Biol 87:313–316

    Article  CAS  PubMed  Google Scholar 

  36. Kamachi Y, Iwafuchi M, Okuda Y, Takemoto T, Uchikawa M, Kondoh H (2009) Evolution of non-coding regulatory sequences involved in the developmental process: reflection of differential employment of paralogous genes as highlighted by Sox2 and group B1 Sox genes. Proc Jpn Acad Ser B Phys Biol Sci 85:55–68

    Article  CAS  PubMed  Google Scholar 

  37. Griffin C, Kleinjan DA, Doe B, van Heyningen V (2002) New 3’ elements control Pax6 expression in the developing pretectum, neural retina and olfactory region. Mech Dev 112:89–100

    Article  CAS  PubMed  Google Scholar 

  38. Kleinjan DA, Seawright A, Childs AJ, van Heyningen V (2004) Conserved elements in Pax6 intron 7 involved in (auto)regulation and alternative transcription. Dev Biol 265:462–477

    Article  CAS  PubMed  Google Scholar 

  39. Kammandel B, Chowdhury K, Stoykova A, Aparicio S, Brenner S, Gruss P (1999) Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity. Dev Biol 205:79–97

    Article  CAS  PubMed  Google Scholar 

  40. Kurokawa D, Takasaki N, Kiyonari H, Nakayama R, Kimura-Yoshida C, Matsuo I, Aizawa S (2004) Regulation of Otx2 expression and its functions in mouse epiblast and anterior neuroectoderm. Development 131:3307–3317

    Article  CAS  PubMed  Google Scholar 

  41. Kimura-Yoshida C, Kitajima K, Oda-Ishii I, Tian E, Suzuki M, Yamamoto M, Suzuki T, Kobayashi M, Aizawa S, Matsuo I (2004) Characterization of the pufferfish Otx2 cis-regulators reveals evolutionarily conserved genetic mechanisms for vertebrate head specification. Development 131:57–71

    Article  CAS  PubMed  Google Scholar 

  42. Wood HB, Episkopou V (1999) Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86:197–201

    Article  CAS  PubMed  Google Scholar 

  43. D’Amour KA, Gage FH (2003) Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells. Proc Natl Acad Sci USA 100:11866–11872

    Article  PubMed  Google Scholar 

  44. Ivanova N, Dobrin R, Lu R, Kotenko L, Levorse J, DeCoste C, Schafer X, Lun Y, Lemischka IR (2006) Dissecting self-renewal in stem cells with RNA interference. Nature 442:533–538

    Article  CAS  PubMed  Google Scholar 

  45. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA, Ko MSH, Niwa H (2007) Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 9:625–635

    Article  CAS  PubMed  Google Scholar 

  46. Tokuzawa Y, Kaiho E, Maruyama M, Takahashi K, Mitsui K, Maeda M, Niwa H, Yamanaka S (2003) Fbx15 is a novel target of Oct3/4 but is dispensable for embryonic stem cell self-renewal and mouse development. Mol Cell Biol 23:2699–2708

    Article  CAS  PubMed  Google Scholar 

  47. Kuroda T, Tada M, Kubota H, Kimura H, Hatano SY, Suemori H, Nakatsuji N, Tada T (2005) Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 25:2475–2485

    Article  CAS  PubMed  Google Scholar 

  48. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P (2005) Transcriptional regulation of Nanog by OCT4 and SOX2. J Biol Chem 280:24731–24737

    Article  CAS  PubMed  Google Scholar 

  49. Nakatake Y, Fukui N, Iwamatsu Y, Masui S, Takahashi K, Yagi R, Miyazaki J, Matoba R, Ko MS, Niwa H (2006) Klf4 cooperates with Oct3/4 and Sox2 to activate the Lefty1 core promoter in embryonic stem cells. Mol Cell Biol 26:7772–7782

    Article  CAS  PubMed  Google Scholar 

  50. Chew J-L, Loh Y-H, Zhang W, Chen X, Tam W-L, Yeap L-S, Li P, Ang Y-S, Lim B, Robson P, Ng H-H (2005) Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 25:6031–6046

    Article  CAS  PubMed  Google Scholar 

  51. Okumura-Nakanishi S, Saito M, Niwa H, Ishikawa F (2005) Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J Biol Chem 280:5307–5317

    Article  CAS  PubMed  Google Scholar 

  52. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J (2005) Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:917–929

    Article  CAS  PubMed  Google Scholar 

  53. Wiebe MS, Nowling TK, Rizzino A (2003) Identification of novel domains within Sox-2 and Sox-11 invovled in autoinhibition of DNA binding and partnership specificity. J Biol Chem 278:17901–17911

    Article  CAS  PubMed  Google Scholar 

  54. Maruyama M, Ichisaka T, Nakagawa M, Yamanaka S (2005) Differential roles of Sox15 and Sox2 in transcriptional control in mouse embryonic stem cells. J Biol Chem 280:24371–24379

    Article  CAS  PubMed  Google Scholar 

  55. Gu P, Goodwin B, Chung AC, Xu X, Wheeler DA, Price RR, Galardi C, Peng L, Latour AM, Koller BH, Gossen J, Kliewer SA, Cooney AJ (2005) Orphan nuclear receptor LRH-1 is required to maintain Oct4 expression at the epiblast stage of embryonic development. Mol Cell Biol 25:3492–3505

    Article  CAS  PubMed  Google Scholar 

  56. Schoorlemmer J, van Puijenbroek A, van Den Eijnden M, Jonk L, Palas C, Kruijer W (1994) Characterization of a negative retinoic acid response element in the murine Oct4 promoter. Mol Cell Biol 14:1122–1136

    CAS  PubMed  Google Scholar 

  57. Boer B, Kopp J, Mallanna S, Desler M, Chakravarthy H, Wilder PJ, Bernadt C, Rizzino A (2007) Elevating the levels of Sox2 in embryonal carcinoma cells and embryonic stem cells inhibits the expression of Sox2:Oct-3/4 target genes. Nucleic Acids Res 35:1773–1786

    Article  CAS  PubMed  Google Scholar 

  58. Kopp J, Oremsbee BD, Desler M, Rizzino A (2008) Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells. Stem Cells 26:903–911

    Article  CAS  PubMed  Google Scholar 

  59. Niwa H, Miyazaki J, Smith AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372–376

    Article  CAS  PubMed  Google Scholar 

  60. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch DK, Young RA (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947–956

    Article  CAS  PubMed  Google Scholar 

  61. Lee TI, Jenner R, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, Abe K, Murray HL, Zucker JP, Yuan B, Bell GW, Herbolsheimer E, Hannett NM, Sun K, Odom DT, Otte AP, Volkert TL, Bartel DP, Melton DA, Gifford DK, Jaenisch R, Young RA (2006) Control of developmental regulators by polycomb in human embryonic stem cells. Cell 125:301–313

    Article  CAS  PubMed  Google Scholar 

  62. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    Article  CAS  PubMed  Google Scholar 

  63. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:1–12

    Article  Google Scholar 

  64. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S (2007) Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26:101–106

    Article  PubMed  Google Scholar 

  65. Kim JB, Zaehres H, Wu G, Gentile L, Ko K, Sebastiano V, Arauzo-Bravo MJ, Ruau D, Han DW, Zenke M, Scholer HR (2008) Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454:646–650

    Article  CAS  PubMed  Google Scholar 

  66. Shi Y, Do JT, Desponts C, Hahm HS, Scholer HR, Ding S (2008) A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2:525–528

    Article  CAS  PubMed  Google Scholar 

  67. Kim JB, Sebastiano V, Wu G, Arauzo-Bravo MJ, Sasse P, Gentile L, Ko K, Ruau D, Ehrich M, van den Boom D, Meyer J, Hubner K, Ortmeier CO, Zenke M, Fleischmann BK, Zaehres H, Scholer HR (2009) Oct4-induced pluripotency in adult neural stem cells. Cell 136:411–419

    Article  CAS  PubMed  Google Scholar 

  68. Shi Y, Desponts C, Do JT, Hahm HS, Scholer HR, Ding S (2008) Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell 3:568–574

    Article  CAS  PubMed  Google Scholar 

  69. Uwanogho DA, Rex M, Cartwright EJ, Pearl G, Healy C, Scotting PJ, Sharpe PT (1995) Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development. Mech Dev 49:23–36

    Article  CAS  PubMed  Google Scholar 

  70. Collignon J, Sockanathan S, Hacker A, Cohentannoudji M, Norris D, Rastan S, Stevanovic M, Goodfellow P, Lovell-Badge R (1996) A comparison of the properties of Sox3 with Sry and two related genes Sox1 and Sox2. Development 122:509–520

    CAS  PubMed  Google Scholar 

  71. Rex M, Orme A, Uwanogho D, Tointon K, Wigmore PM, Sharpe PT, Scotting PJ (1997) Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev Dyn 209:323–332

    Article  CAS  PubMed  Google Scholar 

  72. Sasai Y (2001) Roles of Sox factors in neural determination: conserved signaling in evolution? Int J Dev Biol 45:321–326

    CAS  PubMed  Google Scholar 

  73. Suh H, Consiglio A, Ray J, Sawai T, D’Amour KA, Gage FH (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1:515–528

    Article  CAS  PubMed  Google Scholar 

  74. Pevny LH, Sockanathan S, Placzek M, Lovell-Badge R (1998) A role for SOX1 in neural determination. Development 125:1967–1978

    CAS  PubMed  Google Scholar 

  75. Kishi M, Mizuseki K, Sasai N, Yamazaki H, Shiota K, Nakanishi S, Sasai Y (2000) Requirement of Sox2-mediated signaling for differentiation of early Xenopus neuroectoderm. Development 127:791–800

    CAS  PubMed  Google Scholar 

  76. Sanchez-Soriano N, Russell S (1998) The Drosophila Sox-domain protein Dichaete is required for the development of the central nervous system midline. Development 125:3989–3996

    Google Scholar 

  77. Buescher M, Hing FS, Chia W (2002) Formation of neuroblasts in the embryonic central nervous system of Drosophila melanogaster is controlled by SoxNeuro. Development 129:4193–4203

    CAS  PubMed  Google Scholar 

  78. Overto PM, Meadows LA, Urban J, Russell S (2002) Evidence for differential and redundant function of Sox genes Dichaete and SoxN during CNS development in Drosophila. Development 129:4219–4228

    Google Scholar 

  79. Ferri ALM, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi PP, Sala M, DeBiasi S, Nicolis SK (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131:3805–3819

    Article  CAS  PubMed  Google Scholar 

  80. Taranova OV, Magness ST, Fagan BM, Wu Y, Surzenko N, Hutton SR, Pevny LH (2006) SOX2 is a does-dependent regulator of retinal neural progenitor competence. Genes Dev 20:1187–1202

    Article  CAS  PubMed  Google Scholar 

  81. Nishiguchi S, Wood H, Kondoh H, Lovell-Badge R, Episkopou V (1998) Sox1 directly regulates the γ-crystallin genes and is essential for lens development in mice. Genes Dev 12:776–781

    Article  CAS  PubMed  Google Scholar 

  82. Malas S, Postlethwate M, Ekonomou A, Whalley B, Nishiguchi S, Wood H, Meldrum B, Constanti A, Episkopou V (2003) SOX1-deficient mice suffer from epilepsy associated with abnormal ventral forebrain development and olfactory cortex hyperexitability. Neuroscience 119:421–432

    Article  CAS  PubMed  Google Scholar 

  83. Bylund M, Andersson E, Novitch BG, Muhr J (2003) Vertebrate neurogenesis is counteracted by Sox1–3 activty. Nat Neurosci 6:1162–1168

    Article  CAS  PubMed  Google Scholar 

  84. Hatakeyama J, Kageyama R (2004) Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol 15:83–89

    Article  CAS  PubMed  Google Scholar 

  85. Hatakeyama J, Bessho Y, Katoh K, Ookawara S, Fujioka M, Guillemot F, Kageyama R (2004) Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131:5539–5550

    Article  CAS  PubMed  Google Scholar 

  86. Bani-Yaghoub M, Tremblay RG, Lei JX, Zhang D, Zurakowski B, Sandhu JK, Smith B, Ribecco-Lutkiewicz M, Kennedy J, Walker PR, Sikorska M (2006) Role of Sox2 in the development of the mouse neocortex. Dev Biol 295:52–66

    Article  CAS  PubMed  Google Scholar 

  87. Holmberg J, Hansson E, Malewicz M, Sanberg M, Perlmann T, Lendahl U, Muhr J (2008) SoxB1 transcription factors and Notch signaling use distinct mechanisms to regulate proneural gene function and neural progenitor differentiation. Development 135:1843–1851

    Article  CAS  PubMed  Google Scholar 

  88. Cavallaro M, Mariani J, Lancini C, Latorre E, Caccia R, Gullo F, Valotta M, DeBiasi S, Spinardi L, Ronchi A, Wanke E, Brunelli S, Favaro R, Ottolenghi S, Nicolis S (2008) Impaired generation of mature neurons by neural stem cells from hypomorphic Sox2 mutants. Development 135:541–557

    Article  CAS  PubMed  Google Scholar 

  89. Rissoti K, Brunelli S, Carmignac D, Thomas PQ, Robinson IC, Lovell-Badge R (2004) SOX3 is required during the formation of the hypothalamo-pituitary axis. Nat Genet 36:247–255

    Article  Google Scholar 

  90. Miyagi S, Masui S, Niwa H, Saito T, Shimazaki T, Okano H, Nishimoto M, Muramatsu M, Iwama A, Okuda A (2008) Consequence of the loss of Sox2 in the developing brain of the mouse. FEBS Lett 582:2811–2815

    Article  CAS  PubMed  Google Scholar 

  91. Nakashima K, Takizawa T, Ochiai W, Yanagisawa M, Hisatsune M, Nakafuku M, Miyazono K, Kishimoto T, Kageyama R, Taga T (2001) BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci USA 98:5868–5873

    Article  CAS  PubMed  Google Scholar 

  92. Kuwabara T, Hsieh J, Nakashima K, Taira K, Gage FH (2004) A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 116:779–793

    Article  CAS  PubMed  Google Scholar 

  93. Fantes J, Ragge NK, Lynch SA, McGill NI, Collin JR, Howard-Peebles PN, Hayward C, Vivian AJ, Williamson K, van Heyningen V, FitzPatrick DR (2003) Mutations in SOX2 cause anophthalmia. Nat Genet 33:461–463

    Article  CAS  PubMed  Google Scholar 

  94. Ragge NK, Lorenz B, Schneider A, Bushby K, de Sanctis L, Salt A, Collin JR, Vivian AJ, Free SL, Thompson P, Williamson KA, Sisodiya SM, van Heyningen V, Fitzpatrick DR (2005) SOX2 anophthalmia syndrome. Am J Med Genet A 135:1–7

    PubMed  Google Scholar 

  95. Faivre L, Williamson KA, Faber V, Laurent N, Grimaldi M, Thauvin-Robinet C, Durand C, Mugneret F, Gouyon JB, Bron A, Huet F, Hayward C, Heyningen VV, Fitzpatrick DR (2006) Recurrence of SOX2 anophthalmia syndrome with gonosomal mosaicism in a phenotypically normal mother. Am J Med Genet A 140A:636–639

    Article  CAS  Google Scholar 

  96. Weiss J, Meeks JJ, Hurley L, Raverot G, Frassetto A, Jameson JL (2003) Sox3 is required for gonadal function, but not sex determination, in males and females. Mol Cell Biol 23:8084–8091

    Article  CAS  PubMed  Google Scholar 

  97. Laumonnier F, Ronce N, Hamel BC, Thomas P, Lespinasse J, Raynaud M, Paringaux C, Van Bokhoven H, Kalscheuer V, Fryns JP, Chelly J, Moraine C, Briault S (2002) Transcription factor SOX3 is involved in X-linked mental retardation with growth hormone deficiency. Am J Hum Genet 71:1450–1455

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are indebted to the members of Okuda’s laboratory for many stimulating discussions. We gratefully acknowledge financial support from the Ministry of Education, Science, Sports, Science and Technology for our previous work on the expression and function of Sox2 in mouse ES cells and neural stem/progenitor cells.

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Correspondence to Akihiko Okuda.

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Miyagi, S., Kato, H. & Okuda, A. Role of SoxB1 transcription factors in development. Cell. Mol. Life Sci. 66, 3675–3684 (2009). https://doi.org/10.1007/s00018-009-0097-0

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