Occupancy of tissue-specific cis-regulatory modules by Otx2 and TLE/Groucho for embryonic head specification

Nature Communications

Volumn 5, Issue , 2014, Pages

  Yasuoka, Yuuri ^a,b   Suzuki, Yutaka ^a   Takahashi, Shuji ^a,f   Someya, Haruka ^c   Sudou, Norihiro ^a,g   Haramoto, Yoshikazu ^a,c   Cho, Ken W ^e   Asashima, Makoto ^a,d   Sugano, Sumio ^a   Taira, Masanori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^c TOKYO METROPOLITAN UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f HIROSHIMA UNIVERSITY   (Japan)

^g TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COREPRESSOR PROTEIN; GOOSECOID PROTEIN; TLE PROTEIN; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ESG PROTEIN, XENOPUS; OTX2 PROTEIN, XENOPUS; PROTEIN BINDING; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OTX; XENOPUS PROTEIN;

DEVELOPMENTAL BIOLOGY; EMBRYO; EMBRYONIC DEVELOPMENT; FROG; FUNCTIONAL ROLE; GENE EXPRESSION; GENOME; MOLECULAR ANALYSIS;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; FEMALE; GASTRULA; GENE ACTIVATION; GENE CONTROL; GENE REPRESSION; GENE TARGETING; HEAD SPECIFICATION; MALE; NANODEVICE; NONHUMAN; PROTEIN BINDING; RNA SEQUENCE; UPREGULATION; XENOPUS TROPICALIS; ANIMAL; ANTIBODY SPECIFICITY; BINDING SITE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEAD; METABOLISM; PROMOTER REGION; XENOPUS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; FEMALE; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAD; MALE; ORGAN SPECIFICITY; OTX TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; XENOPUS; XENOPUS PROTEINS;

EID: 84904185974     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5322     Document Type: Article

References (56)

1. Arendt, D. & Nubler-Jung, K. Common ground plans in early brain development in mice and flies. Bioessays 18, 255-259 (1996).
2. Reichert, H. & Simeone, A. Developmental genetic evidence for a monophyletic origin of the bilaterian brain. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1533-1544 (2001). (Pubitemid 32996713)
3. Heasman, J. Patterning the early Xenopus embryo. Development 133, 1205-1217 (2006).
4. Blumberg, B., Wright, C. V., De Robertis, E. M. & Cho, K. W. Organizer-specific homeobox genes in Xenopus laevis embryos. Science 253, 194-196 (1991). (Pubitemid 21917140)
5. Cho, K. W., Blumberg, B., Steinbeisser, H. & De Robertis, E. M. Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111-1120 (1991). (Pubitemid 121001524)
6. Taira, M., Jamrich, M., Good, P. J. & Dawid, I. B. The LIM domain-containing homeo box gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos. Genes Dev. 6, 356-366 (1992).
7. Taira, M., Otani, H., Saint-Jeannet, J. P. & Dawid, I. B. Role of the LIM class homeodomain protein Xlim-1 in neural and muscle induction by the Spemann organizer in Xenopus. Nature 372, 677-679 (1994).
8. Blitz, I. L. & Cho, K. W. Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. Development 121, 993-1004 (1995).
9. Pannese, M. et al. The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121, 707-720 (1995).
10. Koide, T., Hayata, T. & Cho, K. W. Xenopus as a model system to study transcriptional regulatory networks. Proc. Natl Acad. Sci. USA 102, 4943-4948 (2005).
11. Mochizuki, T. et al. Xlim-1 and LIM domain binding protein 1 cooperate with various transcription factors in the regulation of the goosecoid promoter. Dev. Biol. 224, 470-485 (2000). (Pubitemid 30661025)
12. 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. 257, 190-204 (2003). (Pubitemid 36438653)
13. Artinger, M., Blitz, I., Inoue, K., Tran, U. & Cho, K. W. Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev. 65, 187-196 (1997). (Pubitemid 27314600)
14. Latinkic, B. V. et al. 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. 11, 3265-3276 (1997). (Pubitemid 27528065)
15. Yao, J. & Kessler, D. S. Goosecoid promotes head organizer activity by direct repression of Xwnt8 in Spemann's organizer. Development 128, 2975-2987 (2001). (Pubitemid 32771629)
16. Sudou, N., Yamamoto, S., Ogino, H. & Taira, M. Dynamic in vivo binding of transcription factors to cis-regulatory modules of cer and gsc in the stepwise formation of the Spemann-Mangold organizer. Development 139, 1651-1661 (2012).
17. Acampora, D. et al. Forebrain and midbrain regions are deleted in Otx2-/-mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121, 3279-3290 (1995).
18. Matsuo, I., Kuratani, S., Kimura, C., Takeda, N. & Aizawa, S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9, 2646-2658 (1995).
19. Rivera-Perez, J. A., Mallo, M., Gendron-Maguire, M., Gridley, T. & Behringer, R. R. Goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development 121, 3005-3012 (1995).
20. Shawlot, W. & Behringer, R. R. Requirement for Lim1 in head-organizer function. Nature 374, 425-430 (1995).
21. Ang, S. L. et al. A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122, 243-252 (1996).
22. Vignali, R. et al. Xotx5b, a new member of the Otx gene family, may be involved in anterior and eye development in Xenopus laevis. Mech. Dev. 96, 3-13 (2000). (Pubitemid 30625262)
23. Kuroda, H., Hayata, T., Eisaki, A. & Asashima, M. Cloning a novel developmental regulating gene, Xotx5: its potential role in anterior formation in Xenopus laevis. Dev. Growth Differ. 42, 87-93 (2000). (Pubitemid 30202836)
24. Sander, V., Reversade, B. & De Robertis, E. M. The opposing homeobox genes Goosecoid and Vent1/2 self-regulate Xenopus patterning. EMBO J. 26, 2955-2965 (2007). (Pubitemid 46975771)
25. Agulnick, A. D. et al. Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins. Nature 384, 270-272 (1996). (Pubitemid 26396977)
26. Chen, L. et al. Ssdp proteins interact with the LIM-domain-binding protein Ldb1 to regulate development. Proc. Natl Acad. Sci. USA 99, 14320-14325 (2002). (Pubitemid 35257670)
27. Jimenez, G., Verrijzer, C. P. & Ish-Horowicz, D. A conserved motif in goosecoid mediates groucho-dependent repression in Drosophila embryos. Mol. Cell. Biol. 19, 2080-2087 (1999). (Pubitemid 29098266)
28. Puelles, E. et al. Otx2 regulates the extent, identity and fate of neuronal progenitor domains in the ventral midbrain. Development 131, 2037-2048 (2004). (Pubitemid 38702037)
29. Akkers, R. C. et al. A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev. Cell. 17, 425-434 (2009).
30. Noyes, M. B. et al. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133, 1277-1289 (2008). (Pubitemid 351852912)
31. Wilson, D., Sheng, G., Lecuit, T., Dostatni, N. & Desplan, C. Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 7, 2120-2134 (1993).
32. Ferreiro, B., Artinger, M., Cho, K. & Niehrs, C. Antimorphic goosecoids. Development 125, 1347-1359 (1998). (Pubitemid 28239346)
33. Hiratani, I., Mochizuki, T., Tochimoto, N. & Taira, M. Functional domains of the LIM homeodomain protein Xlim-1 involved in negative regulation, transactivation, and axis formation in Xenopus embryos. Dev. Biol. 229, 456-467 (2001). (Pubitemid 32108705)
34. Chen, X. et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117 (2008). (Pubitemid 351787745)
35. Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858 (2009).
36. van Heeringen, S. J. et al. Principles of nucleation of H3K27 methylation during embryonic development. Genome Res. 24, 401-410 (2014).
37. Whyte, W. A. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307-319 (2013).
38. Choo, S. W., White, R. & Russell, S. Genome-wide analysis of the binding of the hox protein ultrabithorax and the hox cofactor homothorax in Drosophila. PLoS ONE 6, e14778 (2011).
39. Slattery, M., Ma, L., Negre, N., White, K. P. & Mann, R. S. Genome-wide tissue-specific occupancy of the hox protein ultrabithorax and hox cofactor homothorax in Drosophila. PLoS ONE 6, e14686 (2011).
40. Sandmann, T. et al. A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev. 21, 436-449 (2007).
41. Zeitlinger, J. et al. Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev. 21, 385-390 (2007).
42. Izzi, L. et al. Foxh1 recruits Gsc to negatively regulate Mixl1 expression during early mouse development. EMBO J. 26, 3132-3143 (2007). (Pubitemid 47057493)
43. Shanmugam, K., Green, N. C., Rambaldi, I., Saragovi, H. U. & Featherstone, M. S. PBX and MEIS as non-DNA-binding partners in trimeric complexes with HOX proteins. Mol. Cell. Biol. 19, 7577-7588 (1999). (Pubitemid 29493421)
44. Mii, Y. & Masanori, T. Secreted Frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. Development 136, 4083-4088 (2009).
45. Yasuoka, Y. et al. Evolutionary origins of blastoporal expression and organizer activity of the vertebrate gastrula organizer gene lhx1 and its ancient metazoan paralog lhx3. Development 136, 2005-2014 (2009).
46. Harland, R. M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695 (1991).
47. Suga, A., Hikasa, H. & Taira, M. Xenopus ADAMTS1 negatively modulates FGF signaling independent of its metalloprotease activity. Dev. Biol. 295, 26-39 (2006). (Pubitemid 44041323)
48. Kato, Y., Habas, R., Katsuyama, Y., Naar, A. M. & He, X. A component of the ARC/Mediator complex required for TGF beta/Nodal signalling. Nature 418, 641-646 (2002).
49. Yamashita, R. et al. Genome-wide characterization of transcriptional start sites in humans by integrative transcriptome analysis. Genome Res. 21, 775-789 (2011).
50. Johnson, D. S., Mortazavi, A., Myers, R. M. & Wold, B. Genome-wide mapping of in vivo protein-DNA interactions. Science 316, 1497-1502 (2007). (Pubitemid 46906620)
51. Ye, T. et al. seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res. 39, e35 (2011).
52. Machanick, P. & Bailey, T. L. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27, 1696-1697 (2011).
53. Pavesi, G., Mereghetti, P., Mauri, G. & Pesole, G. Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res. 32, W199-W203 (2004). (Pubitemid 38997329)
54. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008). (Pubitemid 351911867)
55. Yoon, S. J., Wills, A. E., Chuong, E., Gupta, R. & Baker, J. C. HEB and E2A function as SMAD/FOXH1 cofactors. Genes Dev. 25, 1654-1661 (2011).
56. Taira, M., Otani, H., Jamrich, M. & Dawid, I. B. Expression of the LIM class homeobox gene Xlim-1 in pronephros and CNS cell lineages of Xenopus embryos is affected by retinoic acid and exogastrulation. Development 120, 1525-1536 (1994). (Pubitemid 24175894)