Chromatin remodelers in oligodendroglia.
CNS development
chromatin remodelers
oligodendrogenesis
transcription factors
transcription regulation
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
09
11
2019
revised:
09
04
2020
accepted:
16
04
2020
pubmed:
28
5
2020
medline:
19
8
2021
entrez:
28
5
2020
Statut:
ppublish
Résumé
Oligodendrocytes, the myelinating cells in the vertebrate central nervous system, produce myelin sheaths to enable saltatory propagation of action potentials. The process of oligodendrocyte myelination entails a stepwise progression from precursor specification to differentiation, which is coordinated by a series of transcriptional and chromatin remodeling events. ATP-dependent chromatin remodeling enzymes, which utilize ATP as an energy source to control chromatin dynamics and regulate the accessibility of chromatin to transcriptional regulators, are critical for oligodendrocyte lineage development and regeneration. In this review, we focus on the latest insights into the spatial and temporal specificity of chromatin remodelers during oligodendrocyte development, myelinogenesis, and regeneration. We will also bring together various plausible mechanisms by which lineage specific transcriptional regulators coordinate with chromatin remodeling factors for programming genomic landscapes to specifically modulate these different processes during developmental myelination and remyelination upon injury.
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1604-1618Subventions
Organisme : NIH HHS
ID : R01NS072427
Pays : United States
Organisme : NIH HHS
ID : R01NS075243
Pays : United States
Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Akazawa, C., Sasai, Y., Nakanishi, S., & Kageyama, R. (1992). Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. Journal of Biological Chemistry, 267(30), 21879-21885.
Alvarez-Saavedra, M., De Repentigny, Y., Lagali, P. S., Raghu Ram, E. V., Yan, K., Hashem, E., … Picketts, D. J. (2014). Snf2h-mediated chromatin organization and histone H1 dynamics govern cerebellar morphogenesis and neural maturation. Nature Communications, 5, 4181. https://doi.org/10.1038/ncomms5181
Artegiani, B., Lyubimova, A., Muraro, M., van Es, J. H., van Oudenaarden, A., & Clevers, H. (2017). A single-cell RNA sequencing study reveals cellular and molecular dynamics of the hippocampal neurogenic niche. Cell Reports, 21(11), 3271-3284. https://doi.org/10.1016/j.celrep.2017.11.050
Bajpai, R., Chen, D. A., Rada-Iglesias, A., Zhang, J., Xiong, Y., Helms, J., … Wysocka, J. (2010). CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature, 463(7283), 958-962. https://doi.org/10.1038/nature08733
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., … Zhao, K. (2007). High-resolution profiling of histone methylations in the human genome. Cell, 129(4), 823-837. https://doi.org/10.1016/j.cell.2007.05.009
Batsukh, T., Pieper, L., Koszucka, A. M., von Velsen, N., Hoyer-Fender, S., Elbracht, M., … Pauli, S. (2010). CHD8 interacts with CHD7, a protein which is mutated in CHARGE syndrome. Human Molecular Genetics, 19(14), 2858-2866. https://doi.org/10.1093/hmg/ddq189
Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L., & Weintraub, H. (1990). The protein id: A negative regulator of helix-loop-helix DNA binding proteins. Cell, 61(1), 49-59.
Bertrand, N., Castro, D. S., & Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nature Reviews. Neuroscience, 3(7), 517-530.
Bischof, M., Weider, M., Küspert, M., Nave, K.-A., & Wegner, M. (2015). Brg1-dependent chromatin Remodelling is not essentially required during Oligodendroglial differentiation. The Journal of Neuroscience, 35(1), 21-35. https://doi.org/10.1523/jneurosci.1468-14.2015
Cai, J., Qi, Y., Hu, X., Tan, M., Liu, Z., Zhang, J., … Qiu, M. (2005). Generation of Oligodendrocyte precursor cells from mouse dorsal spinal cord independent of Nkx6 regulation and Shh signaling. Neuron, 45(1), 41-53.
Cai, Y., Brophy, P. D., Levitan, I., Stifani, S., & Dressler, G. R. (2003). Groucho suppresses Pax2 transactivation by inhibition of JNK-mediated phosphorylation. The EMBO Journal, 22(20), 5522-5529. https://doi.org/10.1093/emboj/cdg536
Chen, G., Fernandez, J., Mische, S., & Courey, A. J. (1999). A functional interaction between the histone deacetylase Rpd3 and the corepressor Groucho in drosophila development. Genes & Development, 13(17), 2218-2230.
Cirillo, L. A., Lin, F. R., Cuesta, I., Friedman, D., Jarnik, M., & Zaret, K. S. (2002). Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Molecular Cell, 9(2), 279-289. https://doi.org/10.1016/s1097-2765(02)00459-8
Cirillo, L. A., McPherson, C. E., Bossard, P., Stevens, K., Cherian, S., Shim, E. Y., … Zaret, K. S. (1998). Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. The EMBO Journal, 17(1), 244-254. https://doi.org/10.1093/emboj/17.1.244
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., … Jaenisch, R. (2010). Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proceedings of the National Academy of Sciences, 107(50), 21931-21936. https://doi.org/10.1073/pnas.1016071107
Dawson, M. R., Polito, A., Levine, J. M., & Reynolds, R. (2003). NG2-expressing glial progenitor cells: An abundant and widespread population of cycling cells in the adult rat CNS. Molecular and Cellular Neurosciences, 24(2), 476-488.
Deng, W., Rupon, J. W., Krivega, I., Breda, L., Motta, I., Jahn, K. S., … Blobel, G. A. (2014). Reactivation of developmentally silenced globin genes by forced chromatin looping. Cell, 158(4), 849-860. https://doi.org/10.1016/j.cell.2014.05.050
Doi, T., Ogata, T., Yamauchi, J., Sawada, Y., Tanaka, S., & Nagao, M. (2017). Chd7 collaborates with Sox2 to regulate activation of oligodendrocyte precursor cells after spinal cord injury. The Journal of Neuroscience, 37(43), 10290-10309. https://doi.org/10.1523/jneurosci.1109-17.2017
Durak, O., Gao, F., Kaeser-Woo, Y. J., Rueda, R., Martorell, A. J., Nott, A., … Tsai, L. H. (2016). Chd8 mediates cortical neurogenesis via transcriptional regulation of cell cycle and Wnt signaling. Nature Neuroscience, 19(11), 1477-1488. https://doi.org/10.1038/nn.4400
Elsesser, O., Fröb, F., Küspert, M., Tamm, E. R., Fujii, T., Fukunaga, R., & Wegner, M. (2019). Chromatin remodeler Ep400 ensures oligodendrocyte survival and is required for myelination in the vertebrate central nervous system. Nucleic Acids Research, 47(12), 6208-6224. https://doi.org/10.1093/nar/gkz376
Emery, B., Agalliu, D., Cahoy, J. D., Watkins, T. A., Dugas, J. C., Mulinyawe, S. B., … Barres, B. A. (2009). Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell, 138(1), 172-185.
Feng, W., Kawauchi, D., Körkel-Qu, H., Deng, H., Serger, E., Sieber, L., … Liu, H.-K. (2017). Chd7 is indispensable for mammalian brain development through activation of a neuronal differentiation programme. Nature Communications, 8, 14758. https://doi.org/10.1038/ncomms14758
Feng, W., Khan, M. A., Bellvis, P., Zhu, Z., Bernhardt, O., Herold-Mende, C., & Liu, H.-K. (2013). The chromatin remodeler CHD7 regulates adult neurogenesis via activation of SoxC transcription factors. Cell Stem Cell, 13(1), 62-72.
Ferri, E., Petosa, C., & McKenna, C. E. (2016). Bromodomains: Structure, function and pharmacology of inhibition. Biochemical Pharmacology, 106, 1-18. https://doi.org/10.1016/j.bcp.2015.12.005
Filbin, M., & Monje, M. (2019). Developmental origins and emerging therapeutic opportunities for childhood cancer. Nature Medicine, 25(3), 367-376. https://doi.org/10.1038/s41591-019-0383-9
García-Marqués, J., Núñez-Llaves, R., & López-Mascaraque, L. (2014). NG2-glia from pallial progenitors produce the largest clonal clusters of the brain: Time frame of clonal generation in cortex and olfactory bulb. The Journal of Neuroscience, 34(6), 2305-2313. https://doi.org/10.1523/jneurosci.3060-13.2014
Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R., & Young, R. A. (2007). A chromatin landmark and transcription initiation at most promoters in human cells. Cell, 130(1), 77-88. https://doi.org/10.1016/j.cell.2007.05.042
Hargreaves, D. C., & Crabtree, G. R. (2011). ATP-dependent chromatin remodeling: Genetics, genomics and mechanisms. Cell Research, 21(3), 396-420. https://doi.org/10.1038/cr.2011.32
He, D., Marie, C., Zhao, C., Kim, B., Wang, J., Deng, Y., … Lu, Q. R. (2016). Chd7 cooperates with Sox10 and regulates the onset of CNS myelination and remyelination. Nature Neuroscience, Advance Online Publication, 19, 678-689. https://doi.org/10.1038/nn.4258
Ho, L., & Crabtree, G. R. (2010). Chromatin remodelling during development. Nature, 463(7280), 474-484. https://doi.org/10.1038/nature08911
Ho, L., Jothi, R., Ronan, J. L., Cui, K., Zhao, K., & Crabtree, G. R. (2009). An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proceedings of the National Academy of Sciences, 106(13), 5187-5191. https://doi.org/10.1073/pnas.0812888106
Jin, Q., Yu, L.-R., Wang, L., Zhang, Z., Kasper, L. H., Lee, J.-E., … Ge, K. (2011). Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. The EMBO Journal, 30(2), 249-262. https://doi.org/10.1038/emboj.2010.318
Kageyama, R., Ohtsuka, T., & Kobayashi, T. (2007). The Hes gene family: Repressors and oscillators that orchestrate embryogenesis. Development, 134(7), 1243-1251. https://doi.org/10.1242/dev.000786
Kastenhuber, E. R., & Lowe, S. W. (2017). Putting p53 in context. Cell, 170(6), 1062-1078. https://doi.org/10.1016/j.cell.2017.08.028
Kim, T.-K., & Shiekhattar, R. (2015). Architectural and functional commonalities between enhancers and promoters. Cell, 162(5), 948-959. https://doi.org/10.1016/j.cell.2015.08.008
Kondo, T., & Raff, M. (2000). The Id4 HLH protein and the timing of oligodendrocyte differentiation. The EMBO Journal, 19(9), 1998-2007.
Kuspert, M., Hammer, A., Bosl, M. R., & Wegner, M. (2011). Olig2 regulates Sox10 expression in oligodendrocyte precursors through an evolutionary conserved distal enhancer. Nucleic Acids Research, 39(4), 1280-1293. https://doi.org/10.1093/nar/gkq951
Lang, J., Maeda, Y., Bannerman, P., Xu, J., Horiuchi, M., Pleasure, D., & Guo, F. (2013). Adenomatous polyposis coli regulates oligodendroglial development. The Journal of Neuroscience, 33(7), 3113-3130. https://doi.org/10.1523/jneurosci.3467-12.2013
Lawrence, M., Daujat, S., & Schneider, R. (2016). Lateral thinking: How histone modifications regulate gene expression. Trends in Genetics, 32(1), 42-56. https://doi.org/10.1016/j.tig.2015.10.007
Liu, A., Li, J., Marin-Husstege, M., Kageyama, R., Fan, Y., Gelinas, C., & Casaccia-Bonnefil, P. (2006). A molecular insight of Hes5-dependent inhibition of myelin gene expression: Old partners and new players. The EMBO Journal, 25(20), 4833-4842.
Liu, C., Sage, J. C., Miller, M. R., Verhaak, R. G. W., Hippenmeyer, S., Vogel, H., … Zong, H. (2011). Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell, 146(2), 209-221.
Liu, Z., Hu, X., Cai, J., Liu, B., Peng, X., Wegner, M., & Qiu, M. (2007). Induction of oligodendrocyte differentiation by Olig2 and Sox10: Evidence for reciprocal interactions and dosage-dependent mechanisms. Developmental Biology, 302(2), 683-693.
Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C. D., & Rowitch, D. H. (2002). Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell, 109(1), 75-86.
Lu, Q. R., Yuk, D., Alberta, J. A., Zhu, Z., Pawlitzky, I., Chan, J., … Rowitch, D. H. (2000). Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron, 25(2), 317-329.
Malarkey, C. S., & Churchill, M. E. (2012). The high mobility group box: The ultimate utility player of a cell. Trends in Biochemical Sciences, 37(12), 553-562. https://doi.org/10.1016/j.tibs.2012.09.003
Marie, C., Clavairoly, A., Frah, M., Hmidan, H., Yan, J., Zhao, C., … Parras, C. (2018). Oligodendrocyte precursor survival and differentiation requires chromatin remodeling by Chd7 and Chd8. Proceedings of the National Academy of Sciences, 115(35), E8246-E8255. https://doi.org/10.1073/pnas.1802620115
Marques, S., van Bruggen, D., Vanichkina, D. P., Floriddia, E. M., Munguba, H., Väremo, L., … Castelo-Branco, G. (2018). Transcriptional convergence of Oligodendrocyte lineage progenitors during development. Developmental Cell, 46(4), 504-517.e507. https://doi.org/10.1016/j.devcel.2018.07.005
Marques, S., Zeisel, A., Codeluppi, S., van Bruggen, D., Mendanha Falcão, A., Xiao, L., … Castelo-Branco, G. (2016). Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science, 352(6291), 1326-1329. https://doi.org/10.1126/science.aaf6463
Marshall, C. A. G., Novitch, B. G., & Goldman, J. E. (2005). Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. The Journal of Neuroscience, 25(32), 7289-7298.
Matsumoto, S., Banine, F., Feistel, K., Foster, S., Xing, R., Struve, J., & Sherman, L. S. (2016). Brg1 directly regulates olig2 transcription and is required for oligodendrocyte progenitor cell specification. Developmental Biology, 413(2), 173-187. https://doi.org/10.1016/j.ydbio.2016.04.003
Matsumoto, S., Banine, F., Struve, J., Xing, R., Adams, C., Liu, Y., … Sherman, L. S. (2006). Brg1 is required for murine neural stem cell maintenance and gliogenesis. Developmental Biology, 289(2), 372-383.
Micucci, J. A., Layman, W. S., Hurd, E. A., Sperry, E. D., Frank, S. F., Durham, M. A., … Martin, D. M. (2014). CHD7 and retinoic acid signaling cooperate to regulate neural stem cell and inner ear development in mouse models of CHARGE syndrome. Human Molecular Genetics, 23(2), 434-448. https://doi.org/10.1093/hmg/ddt435
Nakatani, H., Martin, E., Hassani, H., Clavairoly, A., Maire, C. L., Viadieu, A., … Parras, C. (2013). Ascl1/Mash1 promotes brain oligodendrogenesis during myelination and Remyelination. The Journal of Neuroscience, 33(23), 9752-9768. https://doi.org/10.1523/JNEUROSCI.0805-13.2013
Nielsen, J. A., Hudson, L. D., & Armstrong, R. C. (2002). Nuclear organization in differentiating oligodendrocytes. Journal of Cell Science, 115(21), 4071-4079. https://doi.org/10.1242/jcs.00103
Nishiyama, M., Nakayama, K., Tsunematsu, R., Tsukiyama, T., Kikuchi, A., & Nakayama, K. I. (2004). Early embryonic death in mice lacking the β-catenin-binding protein Duplin. Molecular and Cellular Biology, 24(19), 8386-8394. https://doi.org/10.1128/mcb.24.19.8386-8394.2004
Nishiyama, M., Oshikawa, K., Tsukada, Y.-I., Nakagawa, T., Iemura, S.-I., Natsume, T., … Nakayama, K. I. (2009). CHD8 suppresses p53-mediated apoptosis through histone H1 recruitment during early embryogenesis. Nature Cell Biology, 11(2), 172-182.
Norton, J. D., Deed, R. W., Craggs, G., & Sablitzky, F. (1998). Id helix-loop-helix proteins in cell growth and differentiation. Trends in Cell Biology, 8(2), 58-65.
Novitch, B. G., Chen, A. I., & Jessell, T. M. (2001). Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron, 31(5), 773-789.
Panne, D. (2008). The enhanceosome. Current Opinion in Structural Biology, 18(2), 236-242. https://doi.org/10.1016/j.sbi.2007.12.002
Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J. (2011). A unique chromatin signature uncovers early developmental enhancers in humans. Nature, 470(7333), 279-283.
Raposo, A. A. S. F., Vasconcelos, F. F., Drechsel, D., Marie, C., Johnston, C., Dolle, D., … Castro, D. S. (2015). Ascl1 coordinately regulates gene expression and the chromatin landscape during neurogenesis. Cell Reports, 10(9), 1544-1556.
Rodriguez-Paredes, M., Ceballos-Chavez, M., Esteller, M., Garcia-Dominguez, M., & Reyes, J. C. (2009). The chromatin remodeling factor CHD8 interacts with elongating RNA polymerase II and controls expression of the cyclin E2 gene. Nucleic Acids Research, 37(8), 2449-2460. https://doi.org/10.1093/nar/gkp101
Sakamoto, I., Kishida, S., Fukui, A., Kishida, M., Yamamoto, H., Hino, S.-I., … Kikuchi, A. (2000). A novel β-catenin-binding protein inhibits β-catenin-dependent Tcf activation and Axis formation. Journal of Biological Chemistry, 275(42), 32871-32878.
Schnetz, M. P., Bartels, C. F., Shastri, K., Balasubramanian, D., Zentner, G. E., Balaji, R., … Scacheri, P. C. (2009). Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Research, 19(4), 590-601. https://doi.org/10.1101/gr.086983.108
Sekiya, T., & Zaret, K. S. (2007). Repression by Groucho/TLE/Grg proteins: Genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Molecular Cell, 28(2), 291-303. https://doi.org/10.1016/j.molcel.2007.10.002
Soufi, A., Garcia, M. F., Jaroszewicz, A., Osman, N., Pellegrini, M., & Zaret, K. S. (2015). Pioneer transcription factors target partial DNA motifs on nucleosomes to initiate reprogramming. Cell, 161(3), 555-568.
Stolt, C. C., Rehberg, S., Ader, M., Lommes, P., Riethmacher, D., Schachner, M., … Wegner, M. (2002). Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes & Development, 16(2), 165-170.
Turnescu, T., Arter, J., Reiprich, S., Tamm, E. R., Waisman, A., & Wegner, M. (2018). Sox8 and Sox10 jointly maintain myelin gene expression in oligodendrocytes. GLIA, 66(2), 279-294.
Van Nostrand, J. L., Brady, C. A., Jung, H., Fuentes, D. R., Kozak, M. M., Johnson, T. M., … Attardi, L. D. (2014). Inappropriate p53 activation during development induces features of CHARGE syndrome. Nature, 514(7521), 228-232. https://doi.org/10.1038/nature13585
Vogl, M. R., Reiprich, S., Küspert, M., Kosian, T., Schrewe, H., Nave, K.-A., & Wegner, M. (2013). Sox10 cooperates with the mediator subunit 12 during terminal differentiation of Myelinating glia. The Journal of Neuroscience, 33(15), 6679-6690. https://doi.org/10.1523/jneurosci.5178-12.2013
Wang, S., Sdrulla, A., Johnson, J. E., Yokota, Y., & Barres, B. A. (2001). A role for the helix-loop-helix protein Id2 in the control of oligodendrocyte development. Neuron, 29(3), 603-614.
Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., … Zhao, K. (2008). Combinatorial patterns of histone acetylations and methylations in the human genome. Nature Genetics, 40(7), 897-903. https://doi.org/10.1038/ng.154
Wapinski, O. L., Vierbuchen, T., Qu, K., Lee, Q. Y., Chanda, S., Fuentes, D. R., … Wernig, M. (2013). Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell, 155(3), 621-635.
Wegener, A., Deboux, C., Bachelin, C., Frah, M., Kerninon, C., Seilhean, D., … Nait-Oumesmar, B. (2015). Gain of Olig2 function in oligodendrocyte progenitors promotes remyelination. Brain, 138(1), 120-135. https://doi.org/10.1093/brain/awu375
Weider, M., Küspert, M., Bischof, M., Vogl, M. R., Hornig, J., Loy, K., … Wegner, M. (2012). Chromatin-remodeling factor Brg1 is required for Schwann cell differentiation and myelination. Developmental Cell, 23(1), 193-201.
Weng, Q., Wang, J., Wang, J., He, D., Cheng, Z., Zhang, F., … Lu, Q. R. (2019). Single-cell transcriptomics uncovers glial progenitor diversity and cell fate determinants during development and gliomagenesis. Cell Stem Cell, 24(5), 707-723. e708.
Whittaker, D. E., Riegman, K. L., Kasah, S., Mohan, C., Yu, T., Sala, B. P., … Basson, M. A. (2017). The chromatin remodeling factor CHD7 controls cerebellar development by regulating reelin expression. The Journal of Clinical Investigation, 127(3), 874-887. https://doi.org/10.1172/JCI83408
Woodage, T., Basrai, M. A., Baxevanis, A. D., Hieter, P., & Collins, F. S. (1997). Characterization of the CHD family of proteins. Proceedings of the National Academy of Sciences, 94(21), 11472-11477. https://doi.org/10.1073/pnas.94.21.11472
Xin, M., Yue, T., Ma, Z., Wu, F.-f., Gow, A., & Lu, Q. R. (2005). Myelinogenesis and axonal recognition by Oligodendrocytes in brain are uncoupled in Olig1-null mice. The Journal of Neuroscience, 25(6), 1354-1365.
Yates, J. A., Menon, T., Thompson, B. A., & Bochar, D. A. (2010). Regulation of HOXA2 gene expression by the ATP-dependent chromatin remodeling enzyme CHD8. FEBS Letters, 584(4), 689-693. https://doi.org/10.1016/j.febslet.2010.01.022
Ye, F., Chen, Y., Hoang, T., Montgomery, R. L., Zhao, X.-H., Bu, H., … Lu, Q. R. (2009). HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the [beta]-catenin-TCF interaction. Nature Neuroscience, 12(7), 829-838.
Yen, K., Vinayachandran, V., & Pugh, B. F. (2013). SWR-C and INO80 chromatin remodelers recognize nucleosome-free regions near +1 nucleosomes. Cell, 154(6), 1246-1256. https://doi.org/10.1016/j.cell.2013.08.043
Yip, D. J., Corcoran, C. P., Alvarez-Saavedra, M., DeMaria, A., Rennick, S., Mears, A. J., … Picketts, D. J. (2012). Snf2l regulates Foxg1-dependent progenitor cell expansion in the developing brain. Developmental Cell, 22(4), 871-878. https://doi.org/10.1016/j.devcel.2012.01.020
Yu, Y., Chen, Y., Kim, B., Wang, H., Zhao, C., He, X., … Lu, Q. R. (2013). Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell, 152(1-2), 248-261.
Yue, T., Xian, K., Hurlock, E., Xin, M., Kernie, S. G., Parada, L. F., & Lu, Q. R. (2006). A critical role for dorsal progenitors in cortical myelination. The Journal of Neuroscience, 26(4), 1275-1280. https://doi.org/10.1523/JNEUROSCI.4717-05.2006
Zaret, K. S., & Mango, S. E. (2016). Pioneer transcription factors, chromatin dynamics, and cell fate control. Current Opinion in Genetics & Development, 37, 76-81. https://doi.org/10.1016/j.gde.2015.12.003
Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., … Wu, J. Q. (2014). An RNA-sequencing Transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. The Journal of Neuroscience, 34(36), 11929-11947. https://doi.org/10.1523/jneurosci.1860-14.2014
Zhao, C., Dong, C., Frah, M., Deng, Y., Marie, C., Zhang, F., … Lu, Q. R. (2018). Dual requirement of CHD8 for chromatin landscape establishment and histone Methyltransferase recruitment to promote CNS myelination and repair. Developmental Cell, 45(6), 753-768.e758. https://doi.org/10.1016/j.devcel.2018.05.022
Zhou, Q., & Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell, 109(1), 61-73.
Zhou, Q., Wang, S., & Anderson, D. J. (2000). Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron, 25(2), 331-343.