Ascl1 coordinately regulates gene expression and the chromatin landscape during neurogenesis

Cell Reports

Volumn 10, Issue 9, 2015, Pages 1544-1556

  Raposo, Alexandre A S F ^a   Vasconcelos, Francisca F ^a   Drechsel, Daniela ^b   Marie, Corentine ^c   Johnston, Caroline ^d   Dolle, Dirk ^e,f   Bithell, Angela ^g   Gillotin, Sébastien ^b   van den Berg, Debbie L C ^b   Ettwiller, Laurence ^h   Flicek, Paul ^e,f   Crawford, Gregory E ⁱ   Parras, Carlos M ^c   Berninger, Benedikt ^j,k   Buckley, Noel J ^l   Guillemot, François ^a   Castro, Diogo S ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c SORBONNE UNIVERSITÉ   (France)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^g UNIVERSITY OF READING   (United Kingdom)

^h UNIVERSITY OF HEIDELBERG   (Germany)

ⁱ DUKE UNIVERSITY   (United States)

^j JOHANNES GUTENBERG UNIVERSITY   (Germany)

^k UNIVERSITY OF MUNICH   (Germany)

^l UNIVERSITY OF OXFORD   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84931281902     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.025     Document Type: Article

References (42)

1. Aaker, J.D., Patineau, A.L., Yang, H.-J., Ewart, D.T., Nakagawa, Y., McLoon, S.C., and Koyano-Nakagawa, N. (2010). Interaction of MTG family proteins with NEUROG2 and ASCL1 in the developing nervous system. Neurosci. Lett. 474, 46-51.
2. Alvarez-Rodríguez, R., and Pons, S. (2009). Expression of the proneural gene encoding Mash1 suppresses MYCN mitotic activity. J. Cell Sci. 122, 595-599.
3. Bellefroid, E.J., Bourguignon, C., Hollemann, T., Ma, Q., Anderson, D.J., Kintner, C., and Pieler, T. (1996). X-MyT1, a Xenopus C2HC-type zinc finger protein with a regulatory function in neuronal differentiation. Cell 87, 1191-1202.
4. Bergstrom, D.A., Penn, B.H., Strand, A., Perry, R.L., Rudnicki, M.A., and Tapscott, S.J. (2002). Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol. Cell 9, 587-600.
5. Berninger, B., Costa, M.R., Koch, U., Schroeder, T., Sutor, B., Grothe, B., and Götz, M. (2007a). Functional properties of neurons derived from in vitro reprogrammed postnatal astroglia. The Journal of neuroscience, 27 (32), 8654-8664.
6. Berninger, B., Guillemot, F., and Götz, M. (2007b). Directing neurotransmitter identity of neurones derived from expanded adult neural stem cells. Eur. J. Neurosci. 25, 2581-2590.
7. Bertrand, N., Castro, D.S., and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.
8. 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.
9. Boyle, A.P., Davis, S., Shulha, H.P., Meltzer, P., Margulies, E.H., Weng, Z., Furey, T.S., and Crawford, G.E. (2008). High-resolution mapping and characterization of open chromatin across the genome. Cell 132, 311-322.
10. Burk, O., and Klempnauer, K.H. (1991). Estrogen-dependent alterations in differentiation state of myeloid cells caused by a v-myb/estrogen receptor fusion protein. EMBO J. 10, 3713-3719.
11. Casarosa, S., Fode, C., and Guillemot, F. (1999). Mash1 regulates neurogenesis in the ventral telencephalon. Development 126, 525-534.
12. Castro, D.S., Skowronska-Krawczyk, D., Armant, O., Donaldson, I.J., Parras, C., Hunt, C., Critchley, J.A., Nguyen, L., Gossler, A., Göttgens, B., et al. (2006). Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev. Cell 11, 831-844.
13. Castro, D.S., Martynoga, B., Parras, C., Ramesh, V., Pacary, E., Johnston, C., Drechsel, D., Lebel-Potter, M., Garcia, L.G., Hunt, C., et al. (2011). A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev. 25, 930-945.
14. Conti, L., Pollard, S.M., Gorba, T., Reitano, E., Toselli, M., Biella, G., Sun, Y., Sanzone, S., Ying, Q.L., Cattaneo, E., and Smith, A. (2005). Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 3, e283.
15. Ernst, J., and Kellis, M. (2012). ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9, 215-216.
16. Forgacs, G., Yook, S.H., Janmey, P.A., Jeong, H., and Burd, C.G. (2004). Role of the cytoskeleton in signaling networks. J. Cell Sci. 117, 2769-2775.
17. Geoffroy, C.G., Critchley, J.A., Castro, D.S., Ramelli, S., Barraclough, C., Descombes, P., Guillemot, F., and Raineteau, O. (2009). Engineering of dominant active basic helix-loop-helix proteins that are resistant to negative regulation by postnatal central nervous system antineurogenic cues. Stem Cells 27, 847-856.
18. Gratton, M.O., Torban, E., Jasmin, S.B., Theriault, F.M., German, M.S., Stifani, S., and Stifani, S. (2003). Hes6 promotes cortical neurogenesis and inhibits Hes1 transcription repression activity by multiple mechanisms. Mol. Cell. Biol. 23, 6922-6935.
19. Imayoshi, I., Isomura, A., Harima, Y., Kawaguchi, K., Kori, H., Miyachi, H., Fujiwara, T., Ishidate, F., and Kageyama, R. (2013). Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342, 1203-1208.
20. Kaltezioti, V., Kouroupi, G., Oikonomaki, M., Mantouvalou, E., Stergiopoulos, A., Charonis, A., Rohrer, H., Matsas, R., and Politis, P.K. (2010). Prox1 regulates the notch1-mediated inhibition of neurogenesis. PLoS Biol. 8, e1000565.
21. Karow, M., Sánchez, R., Schichor, C., Masserdotti, G., Ortega, F., Heinrich, C., Gascón, S., Khan, M.A., Lie, D.C., Dellavalle, A., et al. (2012). Reprogramming of pericyte-derived cells of the adult human brain into induced neuronal cells. Cell Stem Cell 11, 471-476.
22. Kriegstein, A., and Alvarez-Buylla, A. (2009). The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184.
23. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
24. Littlewood, T.D., Hancock, D.C., Danielian, P.S., Parker, M.G., and Evan, G.I. (1995). A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23, 1686-1690.
25. Martínez-Cerdeño, V., Noctor, S.C., Espinosa, A., Ariza, J., Parker, P., Orasji, S., Daadi, M.M., Bankiewicz, K., Alvarez-Buylla, A., and Kriegstein, A.R. (2010). Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats. Cell Stem Cell 6, 238-250.
26. Natarajan, A., Yardimci, G.G., Sheffield, N.C., Crawford, G.E., and Ohler, U. (2012). Predicting cell-type-specific gene expression from regions of open chromatin. Genome Res. 22, 1711-1722.
27. Ohsawa, R., Ohtsuka, T., and Kageyama, R. (2005). Mash1 and Math3 are required for development of branchiomotor neurons and maintenance of neural progenitors. J. Neurosci. 25, 5857-5865.
28. Park, P.J. (2009). ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10, 669-680.
29. Piper, J., Elze, M.C., Cauchy, P., Cockerill, P.N., Bonifer, C., and Ott, S. (2013). Wellington: a novel method for the accurate identification of digital genomic footprints from DNase-seq data. Nucleic Acids Res. 41, e201.
30. Pollard, S.M., Conti, L., Sun, Y., Goffredo, D., and Smith, A. (2006). Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb. Cortex 16 (Suppl 1), i112-i120.
31. Rheinbay, E., Suvà, 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.
32. Roemer, K., and Friedmann, T. (1993). Modulation of cell proliferation and gene expression by a p53-estrogen receptor hybrid protein. Proc. Natl. Acad. Sci. USA 90, 9252-9256.
33. Ruzinova, M.B., and Benezra, R. (2003). Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13, 410-418.
34. Song, L., and Crawford, G.E. (2010). DNase-seq: a high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells. Cold Spring Harbor Protoc. 2010, pdb.prot5384.
35. Song, L., Zhang, Z., Grasfeder, L.L., Boyle, A.P., Giresi, P.G., Lee, B.K., Sheffield, N.C., Gräf, S., Huss, M., Keefe, D., et al. (2011). Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res. 21, 1757-1767.
36. Thurman, R.E., Rynes, E., Humbert, R., Vierstra, J., Maurano, M.T., Haugen, E., Sheffield, N.C., Stergachis, A.B., Wang, H., Vernot, B., et al. (2012). The accessible chromatin landscape of the human genome. Nature 489, 75-82.
37. Vasconcelos, F.F., and Castro, D.S. (2014). Transcriptional control of vertebrate neurogenesis by the proneural factor Ascl1. Front. Cell. Neurosci. 8, 412.
38. Vierbuchen, T., Ostermeier, A., Pang, Z.P., Kokubu, Y., Südhof, T.C., and Wernig, M. (2010). Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041.
39. 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.
40. Wilkinson, G., Dennis, D., and Schuurmans, C. (2013). Proneural genes in neocortical development. Neuroscience 253, 256-273.
41. Zaret, K.S., and Carroll, J.S. (2011). Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25, 2227-2241.
42. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., and Liu, X.S. (2008). Modelbased analysis of ChIP-Seq (MACS). Genome Biol. 9, R137.