A systematic survey and characterization of enhancers that regulate Sox3 in neuro-sensory development in comparison with Sox2 enhancers

Biology

Volumn 1, Issue 3, 2012, Pages 714-735

  Nishimura, Naoko ^a   Kamimura, Yoshifumi ^a   Ishida, Yoshiko ^a   Takemoto, Tatsuya ^a   Kondoh, Hisato ^a   Uchikawa, Masanori ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Conserved sequence blocks; Enhancers; Functional assay; Neuro sensory development; Sox2; Sox3

Indexed keywords

EID: 84886096869     PISSN: None     EISSN: 20797737     Source Type: Journal    
DOI: 10.3390/biology1030714     Document Type: Article

References (40)

1. Kamachi, Y.; Uchikawa, M.; Collignon, J.; Lovell-Badge, R.; Kondoh, H. Involvement of Sox1, 2 and 3 in the early and subsequent molecular events of lens induction. Development 1998, 125, 2521-2532.
2. Tanaka, S.; Kamachi, Y.; Tanouchi, A.; Hamada, H.; Jing, N.; Kondoh, H. Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol. Cell Biol. 2004, 24, 8834-8846.
3. Inoue, M.; Kamachi, Y.; Matsunami, H.; Imada, K.; Uchikawa, M.; Kondoh, H. PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 2007, 12, 1049-1061.
4. Kamachi, Y.; Iwafuchi, M.; Okuda, Y.; Takemoto, T.; Uchikawa, M.; Kondoh, H. 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. 2009, 85, 55-68.
5. Uchikawa, M.; Yoshida, M.; Iwafuchi-Doi, M.; Matsuda, K.; Ishida, Y.; Takemoto, T.; Kondoh, H. B1 and B2 Sox gene expression during neural plate development in chicken and mouse embryos: Universal versus species-dependent features. Dev. Growth Differ. 2011, 53, 761-771.
6. Collignon, J.; Sockanathan, S.; Hacker, A.; Cohen-Tannoudji, M.; Norris, D.; Rastan, S.; Stevanovic, M.; Goodfellow, P.N.; Lovell-Badge, R. A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 1996, 122, 509-520.
7. Wood, H.B.; Episkopou, V. Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech. Dev. 1999, 86, 197-201.
8. Okuda, Y.; Yoda, H.; Uchikawa, M.; Furutani-Seiki, M.; Takeda, H.; Kondoh, H.; Kamachi, Y. Comparative genomic and expression analysis of group B1 sox genes in zebrafish indicates their diversification during vertebrate evolution. Dev. Dyn. 2006, 235, 811-825.
9. Penzel, R.; Oschwald, R.; Chen, Y.; Tacke, L.; Grunz, H. Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int. J. Dev. Biol. 1997, 41, 667-477.
10. Rex, M.; Orme, A.; Uwanogho, D.; Tointon, K.; Wigmore, P.M.; Sharpe, P.T.; Scotting, P.J. Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev. Dyn. 1997, 209, 323-232.
11. Uwanogho, D.; Rex, M.; Cartwright, E.J.; Pearl, G.; Healy, C.; Scotting, P.J.; Sharpe, P.T. Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development. Mech. Dev. 1995, 49, 23-36.
12. Rogers, C.D.; Archer, T.C.; Cunningham, D.D.; Grammer, T.C.; Casey, E.M. Sox3 expression is maintained by FGF signaling and restricted to the neural plate by Vent proteins in the Xenopus embryo. Dev. Biol. 2008, 313, 307-319.
13. Schlosser, G.; Ahrens, K. Molecular anatomy of placode development in Xenopus laevis. Dev. Biol. 2004, 271, 439-466.
14. Uchikawa, M.; Kamachi, Y.; Kondoh, H. Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: Their expression during embryonic organogenesis of the chicken. Mech. Dev. 1999, 84, 103-120.
15. Nitta, K.R.; Takahashi, S.; Haramoto, Y.; Fukuda, M.; Onuma, Y.; Asashima, M. Expression of Sox1 during Xenopus early embryogenesis. Biochem. Biophys. Res. Commun. 2006, 351, 287-293.
16. Okuda, Y.; Ogura, E.; Kondoh, H.; Kamachi, Y. B1 SOX coordinate cell specification with patterning and morphogenesis in the early zebrafish embryo. PLoS Genet. 2010, 6, doi:10.1371/journal.pgen.1000936.
17. Rizzoti, K.; Lovell-Badge, R. SOX3 activity during pharyngeal segmentation is required for craniofacial morphogenesis. Development 2007, 134, 3437-3448.
18. Iwafuchi-Doi, M.; Yoshida, Y.; Onichtchouk, D.; Leichsenring, M.; Driever, W.; Takemoto, T.; Uchikawa, M.; Kamachi, Y.; Kondoh, H. The Pou5f1/Pou3f-dependent but SoxB-independent regulation of conserved enhancer N2 initiates Sox2 expression during epiblast to neural plate stages in vertebrates. Dev. Biol. 2011, 352, 354-366.
19. Nishiguchi, S.; Wood, H.; Kondoh, H.; Lovell-Badge, R.; Episkopou, V. Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. Genes Dev. 1998, 12, 776-781.
20. Ekonomou, A.; Kazanis, I.; Malas, S.; Wood, H.; Alifragis, P.; Denaxa, M.; Karagogeos, D.; Constanti, A.; Lovell-Badge, R.; Episkopou, V. Neuronal migration and ventral subtype identity in the telencephalon depend on SOX1. PLoS Biol. 2005, 3, doi:10.1371/journal.pbio.0030186.
21. Avilion, A.A.; Nicolis, S.K.; Pevny, L.H.; Perez, L.; Vivian, N.; Lovell-Badge, R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003, 17, 126-140.
22. Rizzoti, K.; Brunelli, S.; Carmignac, D.; Thomas, P.Q.; Robinson, I.C.; Lovell-Badge, R. SOX3 is required during the formation of the hypothalamo-pituitary axis. Nat. Genet. 2004, 36, 247-255.
23. Weiss, J.; Meeks, J.J.; Hurley, L.; Raverot, G.; Frassetto, A.; Jameson, J.L. Sox3 is required for gonadal function, but not sex determination, in males and females. Mol. Cell Biol. 2003, 23, 8084-8891.
24. Graham, V.; Khudyakov, J.; Ellis, P.; Pevny, L. SOX2 functions to maintain neural progenitor identity. Neuron 2003, 39, 749-765.
25. Pevny, L.H.; Nicolis, S.K. Sox2 roles in neural stem cells. Int. J. Biochem. Cell Biol. 2010, 42, 421-424.
26. Dee, C.T.; Hirst, C.S.; Shih, Y.H.; Tripathi, V.B.; Patient, R.K.; Scotting, P.J. Sox3 regulates both neural fate and differentiation in the zebrafish ectoderm. Dev. Biol. 2008, 320, 289-301.
27. Uchikawa, M.; Ishida, Y.; Takemoto, T.; Kamachi, Y.; Kondoh, H. Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev. Cell 2003, 4, 509-519.
28. Okamoto, R.; Uchikawa, M.; Kondoh, H. Twenty-seven enhancers and additional enhancer candidates for Sox2 regulation are distributed within a 200 kb region of the chicken genome. Nucleic Acids Res. 2012, Submitted.
29. Takemoto, T.; Uchikawa, M.; Kamachi, Y.; Kondoh, H. Convergence of Wnt and FGF signals in the genesis of posterior neural plate through activation of the Sox2 enhancer N-1. Development 2006, 133, 297-306.
30. Saigou, Y.; Kamimura, Y.; Inoue, M.; Kondoh, H.; Uchikawa, M. Regulation of Sox2 in the preplacodal cephalic ectoderm and central nervous system by enhancer N-4. Dev. Growth Differ. 2010, 52, 397-408.
31. Iwafuchi-Doi, M.; Matsuda, K.; Murakami, K.; Niwa, H.; Tesar, P.; Aruga, J.; Matsuo, I.; Kondoh, H. Transcriptional regulatory networks in epiblast cells and during anterior neural plate development as modeled in epiblast stem cells. Development 2012, 139, 3926-3937.
32. Kondoh, H.; Takemoto, T. Axial stem cells deriving both posterior neural and mesodermal tissues during gastrulation. Curr. Opin. Genet. Dev. 2012, 22, 374-380.
33. Takemoto, T.; Uchikawa, M.; Yoshida, M.; Bell, D.M.; Lovell-Badge, R.; Papaioannou, V.E.; Kondoh, H. Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 2011, 470, 394-398.
34. van Rooijen, C.; Simmini, S.; Bialecka, M.; Neijts, R.; van de Ven, C.; Beck, F.; Deschamps, J. Evolutionarily conserved requirement of Cdx for post-occipital tissue emergence. Development 2012, 139, 2576-2583.
35. Brunelli, S.; Silva Casey, E.; Bell, D.; Harland, R.; Lovell-Badge, R. Expression of Sox3 throughout the developing central nervous system is dependent on the combined action of discrete, evolutionarily conserved regulatory elements. Genesis 2003, 36, 12-24.
36. Kondoh, H.; Uchikawa, M. Dissection of chick genomic regulatory regions. Meth. Cell Biol. 2008, 87, 313-336.
37. Kovacevic Grujicic, N.; Mojsin, M.; Krstic, A.; Stevanovic, M. Functional characterization of the human SOX3 promoter: identification of transcription factors implicated in basal promoter activity. Gene 2005, 344, 287-297.
38. Krstic, A.; Mojsin, M.; Stevanovic, M. Regulation of SOX3 gene expression is driven by multiple NF-Y binding elements. Arch. Biochem. Biophys. 2007, 467, 163-173.
39. Mojsin, M.; Stevanovic, M. PBX1 and MEIS1 up-regulate SOX3 gene expression by direct interaction with a consensus binding site within the basal promoter region. Biochem. J. 2009, 425, 107-116.
40. Sawicki, J.A.; Morris, R.J.; Monks, B.; Sakai, K.; Miyazaki, J. A composite CMV-IE enhancer/beta-actin promoter is ubiquitously expressed in mouse cutaneous epithelium. Exp. Cell Res. 1998, 244, 367-369.