A novel role for Ascl1 in the regulation of mesendoderm formation via HDAC-dependent antagonism of VegT

Development (Cambridge)

Volumn 143, Issue 3, 2016, Pages 492-503

  Gao, Li ^a   Zhu, Xuechen ^a   Chen, Geng ^a   Ma, Xin ^b   Zhang, Yan ^a   Khand, Aftab A ^a   Shi, Huijuan ^a   Gu, Fei ^a   Lin, Hao ^a   Chen, Yuemeng ^c   Zhang, Haiyan ^a   He, Lei ^a   Tao, Qinghua ^a  

^a TSINGHUA UNIVERSITY   (China)

^b Chinese Academy of Sciences   (China)

^c TIANJIN NORMAL UNIVERSITY   (China)

Author keywords

Ascl1; HDAC1; Mesendoderm; Transcriptional repressor; VegT; Xenopus

Indexed keywords

HISTONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; PROTEIN NODAL; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MASH1; ASCL1 PROTEIN, XENOPUS; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; MORPHOLINO OLIGONUCLEOTIDE; NERVE PROTEIN; T BOX TRANSCRIPTION FACTOR; VEGT PROTEIN, XENOPUS; XENOPUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; DEACETYLATION; EMBRYO; ENDODERM; FEMALE; GENE EXPRESSION; GENE REPRESSION; MESODERM; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; ANIMAL; CHEMISTRY; DRUG EFFECTS; ECTODERM; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; NONMAMMALIAN EMBRYO; PROTEIN TERTIARY STRUCTURE; XENOPUS LAEVIS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; ECTODERM; EMBRYO, NONMAMMALIAN; ENDODERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEACETYLASES; MESODERM; MORPHOLINOS; NERVE TISSUE PROTEINS; NEUROGENESIS; PROTEIN STRUCTURE, TERTIARY; T-BOX DOMAIN PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84956622580     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.126292     Document Type: Article

References (58)

1. Ali, F. R., Cheng, K., Kirwan, P., Metcalfe, S., Livesey, F. J., Barker, R. A. and Philpott, A. (2014). The phosphorylation status of Ascl1 is a key determinant of neuronal differentiation and maturation in vivo and in vitro. Development 141, 2216-2224.
2. Amamoto, R. and Arlotta, P. (2014). Development-inspired reprogramming of the mammalian central nervous system. Science 343, 1239882.
3. Artus, J. and Chazaud, C. (2014). A close look at the mammalian blastocyst: epiblast and primitive endoderm formation. Cell. Mol. Life Sci. 71, 3327-3338.
4. Bertrand, N., Castro, D. S. and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.
5. Blythe, S. A., Reid, C. D., Kessler, D. S. and Klein, P. S. (2009). Chromatin immunoprecipitation in early Xenopus laevis embryos. Dev. Dyn. 238, 1422-1432.
6. Borromeo, M. D., Meredith, D. M., Castro, D. S., Chang, J. C., Tung, K.-C., Guillemot, F. and Johnson, J. E. (2014). A transcription factor network specifying inhibitory versus excitatory neurons in the dorsal spinal cord. Development 141, 2803-2812.
7. Cao, Y. (2013). Regulation of germ layer formation by pluripotency factors during embryogenesis. Cell Biosci. 3, 15.
8. Cao, Y., Siegel, D. and Knochel, W. (2006). Xenopus POU factors of subclass V inhibit activin/nodal signaling during gastrulation. Mech. Dev. 123, 614-625.
9. Cao, Y., Siegel, D., Donow, C., Knochel, S., Yuan, L. and Knochel, W. (2007). POU-V factors antagonize maternal VegT activity and beta-Catenin signaling in Xenopus embryos. EMBO J. 26, 2942-2954.
10. Cao, Y., Siegel, D., Oswald, F. and Knochel, W. (2008). Oct25 represses transcription of nodal/activin target genes by interaction with signal transducers during Xenopus gastrulation. J. Biol. Chem. 283, 34168-34177.
11. Casey, E. S., Tada, M., Fairclough, L., Wylie, C. C., Heasman, J. and Smith, J. C. (1999). Bix4 is activated directly by VegT and mediates endoderm formation in Xenopus development. Development 126, 4193-4200.
12. Castro, D. S. and Guillemot, F. (2011). Old and new functions of proneural factors revealed by the genome-wide characterization of their transcriptional targets. Cell Cycle 10, 4026-4031.
13. Cha, S.-W., Tadjuidje, E., Tao, Q., Wylie, C. and Heasman, J. (2008). Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. Development 135, 3719-3729.
14. Collart, C., Owens, N. D. L., Bhaw-Rosun, L., Cooper, B., De Domenico, E., Patrushev, I., Sesay, A. K., Smith, J. N., Smith, J. C. and Gilchrist, M. J. (2014). High-resolution analysis of gene activity during the Xenopus mid-blastula transition. Development 141, 1927-1939.
15. De Robertis, E. M. and Kuroda, H. (2004). Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285-308.
16. Ding, Y., Zhang, Y., Xu, C., Tao, Q.-H. and Chen, Y.-G. (2013). HECT domaincontaining E3 ubiquitin ligase NEDD4L negatively regulates Wnt signaling by targeting dishevelled for proteasomal degradation. J. Biol. Chem. 288, 8289-8298.
17. Ferreiro, B., Kintner, C., Zimmerman, K., Anderson, D. and Harris, W. A. (1994). XASH genes promote neurogenesis in Xenopus embryos. Development 120, 3649-3655.
18. Fletcher, R. B., Baker, J. C. and Harland, R. M. (2006). FGF8 spliceforms mediate early mesoderm and posterior neural tissue formation in Xenopus. Development 133, 1703-1714.
19. Gardner, E. J., Nizami, Z. F., Talbot, C. C., Jr. and Gall, J. G. (2012). Stable intronic sequence RNA (sisRNA), a new class of noncoding RNA from the oocyte nucleus of Xenopus tropicalis. Genes Dev. 26, 2550-2559.
20. Gu, F., Shi, H., Gao, L., Zhang, H. and Tao, Q. H. (2012). Maternal Mga is required for Wnt signaling and organizer formation in the early Xenopus embryo. Acta Biochim. Biophys. Sin. (Shanghai) 44, 939-947.
21. Hardwick, L. J. A., Ali, F. R., Azzarelli, R. and Philpott, A. (2014). Cell ccycle regulation of proliferation versus differentiation in the central nervous system. Cell Tiisue Res. 359, 1895-1898.
22. Heasman, J. (2006). Maternal determinants of embryonic cell fate. Semin. Cell Dev. Biol. 17, 93-98.
23. Henke, R. M., Meredith, D. M., Borromeo, M. D., Savage, T. K. and Johnson, J. E. (2009). Ascl1 and Neurog2 form novel complexes and regulate Delta-like3 (Dll3) expression in the neural tube. Dev. Biol. 328, 529-540.
24. Horb, M. E. and Thomsen, G. H. (1997). A vegetally localized T-box transcription factor in Xenopus eggs specifies mesoderm and endoderm and is essential for embryonic mesoderm formation. Development 124, 1689-1698.
25. Huang, C., Chan, J. A. and Schuurmans, C. (2014). Proneural bHLH genes in development and disease. Curr. Top. Dev. Biol. 110, 75-127.
26. Jiang, T., Collins, B. J., Jin, N., Watkins, D. N., Brock, M. V., Matsui, W., Nelkin, B. D. and Ball, D. W. (2009). Achaete-scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer. Cancer Res. 69, 845-854.
27. Johnson, J. E., Birren, S. J. and Anderson, D. J. (1990). Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346, 858-861.
28. Johnson, J. E., Birren, S. J., Saito, T. and Anderson, D. J. (1992). DNA binding and transcriptional regulatory activity of mammalian achaete-scute homologous (MASH) proteins revealed by interaction with a muscle-specific enhancer. Proc. Natl. Acad. Sci. USA 89, 3596-3600.
29. Kuroda, H., Fuentealba, L., Ikeda, A., Reversade, B. and De Robertis, E. M. (2005). Default neural induction: neuralization of dissociated Xenopus cells is mediated by Ras/MAPK activation. Genes Dev. 19, 1022-1027.
30. Levine, A. J. and Brivanlou, A. H. (2007). Proposal of a model of mammalian neural induction. Dev. Biol. 308, 247-256.
31. Lustig, K. D., Kroll, K. L., Sun, E. E. and Kirschner, M. W. (1996). Expression cloning of a Xenopus T-related gene (Xombi) involved in mesodermal patterning and blastopore lip formation. Development 122, 4001-4012.
32. Massague, J. and Chen, Y. G. (2000). Controlling TGF-beta signaling. Genes Dev. 14, 627-644.
33. Nieuwkoop, P. D. and Faber, J. (1994). Normal Table of Xenopus Laevis (Daudin), 3rd edn. New York: Garland Publishing.
34. Parlier, D., Ariza, A., Christulia, F., Genco, F., Vanhomwegen, J., Kricha, S., Souopgui, J. and Bellefroid, E. J. (2008). Xenopus zinc finger transcription factor IA1 (Insm1) expression marks anteroventral noradrenergic neuron progenitors in Xenopus embryos. Dev. Dyn. 237, 2147-2157.
35. Perron, M., Opdecamp, K., Butler, K., Harris, W. A. and Bellefroid, E. J. (1999). X-ngnr-1 and Xath3 promote ectopic expression of sensory neuron markers in the neurula ectoderm and have distinct inducing properties in the retina. Proc. Natl. Acad. Sci. USA 96, 14996-15001.
36. Raposo, A. A. S. F., Vasconcelos, F. F., Drechsel, D., Marie, C., Johnston, C., Dolle, D., Bithell, A., Gillotin, S., van den Berg, D. L. C., Ettwiller, L. et al. (2015). Ascl1 coordinately regulates gene expression and the chromatin landscape during neurogenesis. Cell Rep. 10, 1544-1556.
37. Rheinbay, E., Suva, M. L., Gillespie, S. M., Wakimoto, H., Patel, A. P., Shahid, M., Oksuz, O., Rabkin, S. D., Martuza, R. L., Rivera, M. N. et al. (2013). An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma. Cell Rep. 3, 1567-1579.
38. Rogers, K. W. and Schier, A. F. (2011). Morphogen gradients: from generation to interpretation. Annu. Rev. Cell Dev. Biol. 27, 377-407.
39. Sive, H., Grainger, R. and Harland, R. M. (2000). Early Development Xenopus laevis: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
40. Snir, M., Ofir, R., Elias, S. and Frank, D. (2006). Xenopus laevis POU91 protein, an Oct3/4 homologue, regulates competence transitions from mesoderm to neural cell fates. EMBO J. 25, 3664-3674.
41. Stennard, F., Carnac, G. and Gurdon, J. B. (1996). The Xenopus T-box gene, Antipodean, encodes a vegetally localised maternal mRNA and can trigger mesoderm formation. Development 122, 4179-4188.
42. Stern, C. D. (2005). Neural induction: old problem, new findings, yet more questions. Development 132, 2007-2021.
43. Sugimori, M., Nagao, M., Parras, C. M., Nakatani, H., Lebel, M., Guillemot, F. and Nakafuku, M. (2008). Ascl1 is required for oligodendrocyte development in the spinal cord. Development 135, 1271-1281.
44. Tada, M., Casey, E. S., Fairclough, L. and Smith, J. C. (1998). Bix1, a direct target of Xenopus T-box genes, causes formation of ventral mesoderm and endoderm. Development 125, 3997-4006.
45. Tao, Q., Yokota, C., Puck, H., Kofron, M., Birsoy, B., Yan, D., Asashima, M., Wylie, C. C., Lin, X. and Heasman, J. (2005). Maternal Wnt11 activates the canonical Wnt signaling pathway required for axis formation in Xenopus embryos. Cell 120, 857-871.
46. Taverner, N. V., Kofron, M., Shin, Y., Kabitschke, C., Gilchrist, M. J., Wylie, C., Cho, K. W. Y., Heasman, J. and Smith, J. C. (2005). Microarray-based identification of VegT targets in Xenopus. Mech. Dev. 122, 333-354.
47. Tian, T. and Meng, A. M. (2006). Nodal signals pattern vertebrate embryos. Cell. Mol. Life Sci. 63, 672-685.
48. Torres-Padilla, M.-E. and Chambers, I. (2014). Transcription factor heterogeneity in pluripotent stem cells: a stochastic advantage. Development 141, 2173-2181.
49. Turner, D. L. and Weintraub, H. (1994). Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8, 1434-1447.
50. Wapinski, O. L., Vierbuchen, T., Qu, K., Lee, Q. Y., Chanda, S., Fuentes, D. R., Giresi, P. G., Ng, Y. H., Marro, S., Neff, N. F. et al. (2013). Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell 155, 621-635.
51. Wilkinson, G., Dennis, D. and Schuurmans, C. (2013). Proneural genes in neocortical development. Neuroscience 253, 256-273.
52. Wylie, L. A., Hardwick, L. J. A., Papkovskaia, T. D., Thiele, C. J. and Philpott, A. (2015). Ascl1 phospho-status regulates neuronal differentiation in a Xenopus developmental model of neuroblastoma. Dis. Models Mech. 8, 429-441.
53. Xanthos, J. B., Kofron, M., Wylie, C. and Heasman, J. (2001). Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128, 167-180.
54. Yasuo, H. and Lemaire, P. (1999). A two-step model for the fate determination of presumptive endodermal blastomeres in Xenopus embryos. Curr. Biol. 9, 869-879.
55. Zhang, J. and King, M. L. (1996). Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. Development 122, 4119-4129.
56. Zhang, J., Houston, D. W., King, M. L., Payne, C., Wylie, C. and Heasman, J. (1998). The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 94, 515-524.
57. Zhang, Y., Ding, Y., Chen, Y.-G. and Tao, Q. (2014). NEDD4L regulates convergent extension movements in Xenopus embryos via Disheveledmediated non-canonical Wnt signaling. Dev. Biol. 392, 15-25.
58. Zimmerman, K., Shih, J., Bars, J., Collazo, A. and Anderson, D. J. (1993). XASH-3, a novel Xenopus achaete-scute homolog, provides an early marker of planar neural induction and position along the mediolateral axis of the neural plate. Development 119, 221-232.