FoxG1 and TLE2 act cooperatively to regulate ventral telencephalon formation

Development

Volumn 137, Issue 9, 2010, Pages 1553-1562

  Roth, Martin ^a,c   Bonev, Boyan ^a   Lindsay, Jennefer ^a   Lea, Robert ^a   Panagiotaki, Niki ^a   Houart, Corinne ^b   Papalopulu, Nancy ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c ASTRAZENECA   (United Kingdom)

Author keywords

FoxG1; Telencephalon; TLE; Xenopus

Indexed keywords

CELL PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; MESSENGER RNA; PROTEIN TLE2; TRANSCRIPTION FACTOR FOXG1; UNCLASSIFIED DRUG; XENOPUS PROTEIN;

ARTICLE; FOREBRAIN; GENE EXPRESSION; GENE MUTATION; NERVOUS SYSTEM DEVELOPMENT; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; SEQUENCE HOMOLOGY; TELENCEPHALON; XENOPUS; ANIMAL; ANIMAL EMBRYO; BINDING SITE; CELL LINE; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; METABOLISM; NICK END LABELING; PRENATAL DEVELOPMENT; WESTERN BLOTTING;

XENOPUS TROPICALIS;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CELL LINE; EMBRYO, NONMAMMALIAN; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; PROTEIN BINDING; TELENCEPHALON; XENOPUS; XENOPUS PROTEINS;

EID: 77951248574     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.044909     Document Type: Article

References (56)

1. Ahlgren, S., Vogt, P. and Bronner-Fraser, M. (2003). Excess FoxG1 causes overgrowth of the neural tube. J. Neurobiol. 57, 337-349. (Pubitemid 37433467)
2. Ahn, J. W., Lee, Y. A., Ahn, J. H. and Choi, C. Y. (2009). Covalent conjugation of Groucho with SUMO-1 modulates its corepressor activity. Biochem. Biophys. Res. Commun. 379, 160-165.
3. Bachy, I., Berthon, J. and Retaux, S. (2002). Defining pallial and subpallial divisions in the developing Xenopus forebrain. Mech. Dev. 117, 163-172. (Pubitemid 36158720)
4. Bajoghli, B. (2007). Evolution of the Groucho/Tle gene family: gene organization and duplication events. Dev. Genes Evol. 217, 613-618.
5. Bourguignon, C., Li, J. and Papalopulu, N. (1998). XBF-1, a winged helix transcription factor with dual activity, has a role in positioning neurogenesis in Xenopus competent ectoderm. Development 125, 4889-4900. (Pubitemid 29026770)
6. Buscarlet, M. and Stifani, S. (2007). The 'Marx' of Groucho on development and disease. Trends Cell Biol. 17, 353-361.
7. Buscarlet, M., Perin, A., Laing, A., Brickman, J. M. and Stifani, S. (2008). Inhibition of cortical neuron differentiation by Groucho/TLE1 requires interaction with WRPW, but not Eh1, repressor peptides. J. Biol. Chem. 283, 24881-24888.
8. Carruthers, S., Mason, J. and Papalopulu, N. (2003). Depletion of the cell-cycle inhibitor p27(Xic1) impairs neuronal differentiation and increases the number of ElrC(+) progenitor cells in Xenopus tropicalis. Mech. Dev. 120, 607-616. (Pubitemid 36623322)
9. Chen, G. and Courey, A. J. (2000). Groucho/TLE family proteins and transcriptional repression. Gene 249, 1-16. (Pubitemid 30265483)
10. Chen, G., Fernandez, J., Mische, S. and Courey, A. J. (1999). A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 13, 2218-2230. (Pubitemid 29426727)
11. Choudhury, B. K., Kim, J., Kung, H. F. and Li, S. S. (1997). Cloning and developmental expression of Xenopus cDNAs encoding the Enhancer of split groucho and related proteins. Gene 195, 41-48. (Pubitemid 27336959)
12. Danesin, C., Peres, J. N., Johansson, M., Snowden, V., Cording, A., Papalopulu, N. and Houart, C. (2009). Integration of telencephalic Wnt and hedgehog signaling center activities by Foxg1. Dev. Cell 16, 576-587.
13. Dehni, G., Liu, Y., Husain, J. and Stifani, S. (1995). TLE expression correlates with mouse embryonic segmentation, neurogenesis, and epithelial determination. Mech. Dev. 53, 369-381.
14. Dou, C., Lee, J., Liu, B., Liu, F., Massague, J., Xuan, S. and Lai, E. (2000). BF-1 interferes with transforming growth factor beta signaling by associating with Smad partners. Mol. Cell. Biol. 20, 6201-6211. (Pubitemid 30650207)
15. Eagleson, G. W. and Harris, W. A. (1990). Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. J. Neurobiol. 21, 427-440.
16. Gasperowicz, M. and Otto, F. (2005). Mammalian Groucho homologs: redundancy or specificity? J. Cell. Biochem. 95, 670-687. (Pubitemid 41420155)
17. Goldstein, R. E., Cook, O., Dinur, T., Pisante, A., Karandikar, U. C., Bidwai, A. and Paroush, Z. (2005). An eh1-like motif in odd-skipped mediates recruitment of Groucho and repression in vivo. Mol. Cell. Biol. 25, 10711-10720. (Pubitemid 41747117)
18. Good, P. J. (1995). A conserved family of elav-like genes in vertebrates. Proc. Natl. Acad. Sci. USA 92, 4557-4561.
19. Grbavec, D., Lo, R., Liu, Y. and Stifani, S. (1998). Transducin-like Enhancer of split 2, a mammalian homologue of Drosophila Groucho, acts as a transcriptional repressor, interacts with Hairy/Enhancer of split proteins, and is expressed during neuronal development. Eur. J. Biochem. 258, 339-349. (Pubitemid 28557897)
20. Hanashima, C., Shen, L., Li, S. C. and Lai, E. (2002). Brain factor-1 controls the proliferation and differentiation of neocortical progenitor cells through independent mechanisms. J. Neurosci. 22, 6526-6536. (Pubitemid 35386409)
21. Hanashima, C., Li, S. C., Shen, L., Lai, E. and Fishell, G. (2004). Foxg1 suppresses early cortical cell fate. Science 303, 56-59. (Pubitemid 38055766)
22. Hardcastle, Z. and Papalopulu, N. (2000). Distinct effects of XBF-1 in regulating the cell cycle inhibitor p27(XIC1) and imparting a neural fate. Development 127, 1303-1314. (Pubitemid 30179519)
23. Hasson, P. and Paroush, Z. (2006). Crosstalk between the EGFR and other signalling pathways at the level of the global transcriptional corepressor Groucho/TLE. Br. J. Cancer 94, 771-775.
24. Hebert, J. M. and Fishell, G. (2008). The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci. 9, 678-685.
25. Hoffman, B. G., Zavaglia, B., Beach, M. and Helgason, C. D. (2008). Expression of Groucho/TLE proteins during pancreas development. BMC Dev. Biol. 8, 81.
26. Houghton, L., Freeman, A. and Morgan, B. A. (2003). Expression and regulation of Groucho-related genes in the embryonic chicken feather bud. Dev. Dyn. 226, 587-595. (Pubitemid 36396867)
27. Jennings, B. H. and Ish-Horowicz. (2008). The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 9, 205.1-205.7.
28. Kaestner, K. H., Knochel, W. and Martinez, D. E. (2000). Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14, 142-146. (Pubitemid 30070978)
29. Kobayashi, M., Nishikawa, K., Suzuki, T. and Yamamoto, M. (2001). The homeobox protein Six3 interacts with the Groucho corepressor and acts as a transcriptional repressor in eye and forebrain formation. Dev. Biol. 232, 315-326. (Pubitemid 32337096)
30. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
31. Leon, C. and Lobe, C. G. (1997). Grg3, a murine Groucho-related gene, is expressed in the developing nervous system and in mesenchyme-induced epithelial structures. Dev. Dyn. 208, 11-24. (Pubitemid 27030480)
32. Li, J., Chang, H. W., Lai, E., Parker, E. J. and Vogt, P. K. (1995). The oncogene qin codes for a transcriptional repressor. Cancer Res. 55, 5540-5544.
33. Manuel, M., Martynoga, B., Yu, T., West, J. D., Mason, J. O. and Price, D. J. (2010). The transcription factor Foxg1 regulates the competence of telencephalic cells to adopt subpallial fates in mice. Development 137, 487-497.
34. Marcal, N., Patel, H., Dong, Z., Belanger-Jasmin, S., Hoffman, B., Helgason, C. D., Dang, J. and Stifani, S. (2005). Antagonistic effects of Grg6 and Groucho/TLE on the transcription repression activity of brain factor 1/FoxG1 and cortical neuron differentiation. Mol. Cell. Biol. 25, 10916-10929. (Pubitemid 41747135)
35. Martynoga, B., Morrison, H., Price, D. J. and Mason, J. O. (2005). Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev. Biol. 283, 113-127. (Pubitemid 40828845)
36. Molenaar, M., Brian, E., Roose, J., Clevers, H. and Destree, O. (2000). Differential expression of the Groucho-related genes 4 and 5 during early development of Xenopus laevis. Mech. Dev. 91, 311-315. (Pubitemid 30125929)
37. Murphy, D. B., Wiese, S., Burfeind, P., Schmundt, D., Mattei, M. G., Schulz-Schaeffer, W. and Thies, U. (1994). Human brain factor 1, a new member of the fork head gene family. Genomics 21, 551-557. (Pubitemid 24189885)
38. Nuthall, H. N., Husain, J., McLarren, K. W. and Stifani, S. (2002). Role for Hes1-induced phosphorylation in Groucho-mediated transcriptional repression. Mol. Cell. Biol. 22, 389-399. (Pubitemid 34027485)
39. Nuthall, H. N., Joachim, K. and Stifani, S. (2004). Phosphorylation of serine 239 of Groucho/TLE1 by protein kinase CK2 is important for inhibition of neuronal differentiation. Mol. Cell. Biol. 24, 8395-8407. (Pubitemid 39245062)
40. Perron, M., Furrer, M. P., Wegnez, M. and Theodore, L. (1999). Xenopus elavlike genes are differentially expressed during neurogenesis. Mech. Dev. 84, 139-142. (Pubitemid 29331661)
41. Regad, T., Roth, M., Bredenkamp, N., Illing, N. and Papalopulu, N. (2007). The neural progenitor-specifying activity of FoxG1 is antagonistically regulated by CKI and FGF. Nat. Cell Biol. 9, 531-540. (Pubitemid 46696534)
42. Roose, J., Molenaar, M., Peterson, J., Hurenkamp, J., Brantjes, H., Moerer, P., van de Wetering, M., Destree, O. and Clevers, H. (1998). The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395, 608-612. (Pubitemid 28475715)
43. Seoane, J., Le H. V., Shen, L., Anderson, S. A. and Massague, J. (2004). Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117, 211-223. (Pubitemid 38496241)
44. Shen, Q., Wang, Y., Dimos, J. T., Fasano, C. A., Phoenix, T. N., Lemischka, I. R., Ivanova, N. B., Stifani, S., Morrisey, E. E. and Temple, S. (2006). The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat. Neurosci. 9, 743-751.
45. Sonderegger, C. K. and Vogt, P. K. (2003). Binding of the corepressor TLE1 to Qin enhances Qin-mediated transformation of chicken embryo fibroblasts. Oncogene 22, 1749-1757.
46. Tan, K., Shaw, A. L., Madsen, B., Jensen, K., Taylor-Papadimitriou, J. and Freemont, P. S. (2003). Human PLU-1 has transcriptional repression properties and interacts with the developmental transcription factors BF-1 and PAX9. J. Biol. Chem. 278, 20507-20513. (Pubitemid 36806347)
47. Tao, W. and Lai, E. (1992). Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 8, 957-966.
48. Xuan, S., Baptista, C. A., Balas, G., Tao, W., Soares, V. C. and Lai, E. (1995). Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14, 1141-1152.
49. Yaklichkin, S., Steiner, A. B., Lu, Q. and Kessler, D. S. (2007a). FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. J. Biol. Chem. 282, 2548-2557. (Pubitemid 47076798)
50. Yaklichkin, S., Vekker, A., Stayrook, S., Lewis, M. and Kessler, D. S. (2007b). Prevalence of the EH1 Groucho interaction motif in the metazoan Fox family of transcriptional regulators. BMC Genomics 8, 201.
51. Yamane, K., Tateishi, K., Klose, R. J., Fang, J., Fabrizio, L. A., Erdjument- Bromage, H., Taylor-Papadimitriou, J., Tempst, P. and Zhang, Y. (2007). PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol. Cell 25, 801-812. (Pubitemid 46436533)
52. Yao, J., Liu, Y., Husain, J., Lo, R., Palaparti, A., Henderson, J. and Stifani, S. (1998). Combinatorial expression patterns of individual TLE proteins during cell determination and differentiation suggest non-redundant functions for mammalian homologs of Drosophila Groucho. Dev. Growth Differ. 40, 133-146. (Pubitemid 28180617)
53. Yao, J., Liu, Y., Lo, R., Tretjakoff, I., Peterson, A. and Stifani, S. (2000). Disrupted development of the cerebral hemispheres in transgenic mice expressing the mammalian Groucho homologue transducin-like-enhancer of split 1 in postmitotic neurons. Mech. Dev. 93, 105-115. (Pubitemid 30216500)
54. Yao, J., Lai, E. and Stifani, S. (2001). The winged-helix protein brain factor 1 interacts with groucho and hes proteins to repress transcription. Mol. Cell. Biol. 21, 1962-1972. (Pubitemid 32479620)
55. Zamparini, A. L., Watts, T., Gardner, C. E., Tomlinson, S. R., Johnston, G. I. and Brickman, J. M. (2006). Hex acts with beta-catenin to regulate anteroposterior patterning via a Groucho-related co-repressor and Nodal. Development 133, 3709-3722. (Pubitemid 44614292)
56. Zhao, X. F., Suh, C. S., Prat, C. R., Ellingsen, S. and Fjose, A. (2009). Distinct expression of two foxg1 paralogues in zebrafish. Gene Expr. Patterns 9, 266-272.