Epigenetic control on cell fate choice in neural stem cells
- 751 Downloads
- 17 Citations
Abstract
Derived from neural stem cells (NSCs) and progenitor cells originated from the neuroectoderm, the nervous system presents an unprecedented degree of cellular diversity, interwoven to ensure correct connections for propagating information and responding to environmental cues. NSCs and progenitor cells must integrate cell-intrinsic programs and environmental cues to achieve production of appropriate types of neurons and glia at appropriate times and places during development. These developmental dynamics are reflected in changes in gene expression, which is regulated by transcription factors and at the epigenetic level. From early commitment of neural lineage to functional plasticity in terminal differentiated neurons, epigenetic regulation is involved in every step of neural development. Here we focus on the recent advance in our understanding of epigenetic regulation on orderly generation of diverse neural cell types in the mammalian nervous system, an important aspect of neural development and regenerative medicine.
Keywords
neural stem cells (NSCs) epigenetic regulation neurogenesis gliogenesis radial glial cell cerebral cortex subventricular zone (SVZ) DNA methylation histone modificationReferences
- Allis, C.D., Berger, S.L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R., et al. (2007). New nomenclature for chromatin-modifying enzymes. Cell 131, 633–636.Google Scholar
- Alvarez-Venegas, R., and Avramova, Z. (2005). Methylation patterns of histone H3 Lys 4, Lys 9 and Lys 27 in transcriptionally active and inactive Arabidopsis genes and in atx1 mutants. Nucleic Acids Res 33, 5199–5207.PubMedCentralGoogle Scholar
- Ambros, V. (2003). MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell 113, 673–676.Google Scholar
- Ambros, V. (2004). The functions of animal microRNAs. Nature 431, 350–355.Google Scholar
- Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jørgensen, H.F., John, R.M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M., et al. (2006). Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8, 532–538.Google Scholar
- Balazs, R., Vernon, J., and Hardy, J. (2011). Epigenetic mechanisms in Alzheimer’s disease: progress but much to do. Neurobiol Aging 32, 1181–1187.Google Scholar
- Bannister, A.J., and Kouzarides, T. (2005). Reversing histone methylation. Nature 436, 1103–1106.Google Scholar
- Bannister, A.J., Schneider, R., Myers, F.A., Thorne, A.W., Crane-Robinson, C., and Kouzarides, T. (2005). Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J Biol Chem 280, 17732–17736.Google Scholar
- Bartel, D.P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.Google Scholar
- Bartel, D.P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.PubMedCentralGoogle Scholar
- Bernstein, B.E., Meissner, A., and Lander, E.S. (2007). The mammalian epigenome. Cell 128, 669–681.Google Scholar
- Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326.Google Scholar
- Bernstein, E., and Allis, C.D. (2005). RNA meets chromatin. Genes Dev 19, 1635–1655.Google Scholar
- Bhutani, N., Brady, J.J., Damian, M., Sacco, A., Corbel, S.Y., and Blau, H.M. (2010). Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463, 1042–1047.PubMedCentralGoogle Scholar
- Bhutani, N., Burns, D.M., and Blau, H.M. (2011). DNA demethylation dynamics. Cell 146, 866–872.PubMedCentralGoogle Scholar
- Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev 16, 6–21.Google Scholar
- Bird, A. (2007). Perceptions of epigenetics. Nature 447, 396–398.Google Scholar
- Burgold, T., Spreafico, F., De Santa, F., Totaro, M.G., Prosperini, E., Natoli, G., and Testa, G. (2008). The histone H3 lysine 27-specific demethylase Jmjd3 is required for neural commitment. PLoS One 3, e3034.PubMedCentralGoogle Scholar
- Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S., and Zhang, Y. (2002). Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039–1043.Google Scholar
- Cao, X., Yeo, G., Muotri, A.R., Kuwabara, T., and Gage, F.H. (2006). Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci 29, 77–103.Google Scholar
- Cartagena, J.A., Matsunaga, S., Seki, M., Kurihara, D., Yokoyama, M., Shinozaki, K., Fujimoto, S., Azumi, Y., Uchiyama, S., and Fukui, K. (2008). The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev Biol 315, 355–368.Google Scholar
- Cheng, L.C., Pastrana, E., Tavazoie, M., and Doetsch, F. (2009). miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12, 399–408.PubMedCentralGoogle Scholar
- Ciccone, D.N., Su, H., Hevi, S., Gay, F., Lei, H., Bajko, J., Xu, G., Li, E., and Chen, T. (2009). KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461, 415–418.Google Scholar
- Cloos, P.A., Christensen, J., Agger, K., Maiolica, A., Rappsilber, J., Antal, T., Hansen, K.H., and Helin, K. (2006). The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 442, 307–311.Google Scholar
- Conaco, C., Otto, S., Han, J.J., and Mandel, G. (2006). Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci U S A 103, 2422–2427.PubMedCentralGoogle Scholar
- Coolen, M., and Bally-Cuif, L. (2009). MicroRNAs in brain development and physiology. Curr Opin Neurobiol 19, 461–470.Google Scholar
- Cortellino, S., Xu, J., Sannai, M., Moore, R., Caretti, E., Cigliano, A., Le Coz, M., Devarajan, K., Wessels, A., Soprano, D., et al. (2011). Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67–79.PubMedCentralGoogle Scholar
- De Carvalho, D.D., You, J.S., and Jones, P.A. (2010). DNA methylation and cellular reprogramming. Trends Cell Biol 20, 609–617.PubMedCentralGoogle Scholar
- de la Serna, I.L., Ohkawa, Y., and Imbalzano, A.N.(2006). Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet 7, 461–473.Google Scholar
- De Pietri Tonelli, D., Pulvers, J.N., Haffner, C., Murchison, E.P., Hannon, G.J., and Huttner, W.B. (2008). miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development 135, 3911–3921.PubMedCentralGoogle Scholar
- Deaton, A.M., and Bird, A. (2011). CpG islands and the regulation of transcription. Genes Dev 25, 1010–1022.PubMedCentralGoogle Scholar
- Eden, S., Hashimshony, T., Keshet, I., Cedar, H., and Thorne, A.W. (1998). DNA methylation models histone acetylation. Nature 394, 842.Google Scholar
- Edmunds, J.W., Mahadevan, L.C., and Clayton, A.L. (2008). Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J 27, 406–420.PubMedCentralGoogle Scholar
- Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., and Sasai, Y. (2008). Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519–532.Google Scholar
- Fan, G., Martinowich, K., Chin, M.H., He, F., Fouse, S.D., Hutnick, L., Hattori, D., Ge, W., Shen, Y., Wu, H., et al. (2005). DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132, 3345–3356.Google Scholar
- Feng, J., Chang, H., Li, E., and Fan, G. (2005). Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J Neurosci Res 79, 734–746.Google Scholar
- Ferrón, S.R., Charalambous, M., Radford, E., McEwen, K., Wildner, H., Hind, E., Morante-Redolat, J.M., Laborda, J., Guillemot, F., Bauer, S.R., et al. (2011). Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 475, 381–385.PubMedCentralGoogle Scholar
- Ficz, G., Branco, M.R., Seisenberger, S., Santos, F., Krueger, F., Hore, T.A., Marques, C.J., Andrews, S., and Reik, W. (2011). Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398–402.Google Scholar
- Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S.N., et al. (2008). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351–357.Google Scholar
- Gatto, S., Della Ragione, F., Cimmino, A., Strazzullo, M., Fabbri, M., Mutarelli, M., Ferraro, L., Weisz, A., D’Esposito, M., and Matarazzo, M.R. (2010). Epigenetic alteration of microRNAs in DNMT3B-mutated patients of ICF syndrome. Epigenetics 5, 427–443.Google Scholar
- Giraldez, A.J., Cinalli, R.M., Glasner, M.E., Enright, A.J., Thomson, J.M., Baskerville, S., Hammond, S.M., Bartel, D.P., and Schier, A.F. (2005). MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833–838.Google Scholar
- Gjerset, R.A., and Martin, D.W. Jr. (1982). Presence of a DNA demethylating activity in the nucleus of murine erythroleukemic cells. J Biol Chem 257, 8581–8583.Google Scholar
- Goldberg, A.D., Allis, C.D., and Bernstein, E. (2007). Epigenetics: a landscape takes shape. Cell 128, 635–638.Google Scholar
- Golebiewska, A., Atkinson, S.P., Lako, M., and Armstrong, L. (2009). Epigenetic landscaping during hESC differentiation to neural cells. Stem Cells 27, 1298–1308.Google Scholar
- Goll, M.G., and Bestor, T.H. (2005). Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74, 481–514.Google Scholar
- Goll, M.G., and Halpern, M.E. (2011). DNA methylation in zebrafish. Prog Mol Biol Transl Sci 101, 193–218.Google Scholar
- Griffiths-Jones, S., Saini, H.K., van Dongen, S., and Enright, A.J. (2008). miRBase: tools for microRNA genomics. Nucleic Acids Res 36, D154–D158.PubMedCentralGoogle Scholar
- Grimson, A., Farh, K.K., Johnston, W.K., Garrett-Engele, P., Lim, L.P., and Bartel, D.P. (2007). MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27, 91–105.PubMedCentralGoogle Scholar
- Groth, A., Rocha, W., Verreault, A., and Almouzni, G. (2007). Chromatin challenges during DNA replication and repair. Cell 128, 721–733.Google Scholar
- Guo, J.U., Su, Y., Zhong, C., Ming, G.L., and Song, H. (2011). Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145, 423–434.PubMedCentralGoogle Scholar
- Habibi, E., Masoudi-Nejad, A., Abdolmaleky, H.M., and Haggarty, S.J. (2011). Emerging roles of epigenetic mechanisms in Parkinson’s disease. Funct Integr Genomics 11, 523–537.Google Scholar
- Hargreaves, D.C., and Crabtree, G.R. (2011). ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 21, 396–420.PubMedCentralGoogle Scholar
- Hashimshony, T., Zhang, J., Keshet, I., Bustin, M., and Cedar, H. (2003). The role of DNA methylation in setting up chromatin structure during development. Nat Genet 34, 187–192.Google Scholar
- He, L., and Hannon, G.J. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5, 522–531.Google Scholar
- He, X.B., Yi, S.H., Rhee, Y.H., Kim, H., Han, Y.M., Lee, S.H., Lee, H., Park, C.H., Lee, Y.S., Richardson, E., et al. (2011a). Prolonged membrane depolarization enhances midbrain dopamine neuron differentiation via epigenetic histone modifications. Stem Cells 29, 1861–1873.Google Scholar
- He, Y.F., Li, B.Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L., et al. (2011b). Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303–1307.PubMedCentralGoogle Scholar
- Hevner, R.F., Daza, R.A., Rubenstein, J.L., Stunnenberg, H., Olavarria, J.F., and Englund, C. (2003). Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 25, 139–151.Google Scholar
- Hitoshi, S., Alexson, T., Tropepe, V., Donoviel, D., Elia, A.J., Nye, J.S., Conlon, R.A., Mak, T.W., Bernstein, A., and van der Kooy, D. (2002). Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16, 846–858.PubMedCentralGoogle Scholar
- Hitoshi, S., Ishino, Y., Kumar, A., Jasmine, S., Tanaka, K.F., Kondo, T., Kato, S., Hosoya, T., Hotta, Y., and Ikenaka, K. (2011). Mammalian Gcm genes induce Hes5 expression by active DNA demethylation and induce neural stem cells. Nat Neurosci 14, 957–964.Google Scholar
- Hitoshi, S., Seaberg, R.M., Koscik, C., Alexson, T., Kusunoki, S., Kanazawa, I., Tsuji, S., and van der Kooy, D. (2004). Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling. Genes Dev 18, 1806–1811.PubMedCentralGoogle Scholar
- Holliday, R. (2006). Epigenetics: a historical overview. Epigenetics 1, 76–80.Google Scholar
- Hsieh, J., Nakashima, K., Kuwabara, T., Mejia, E., and Gage, F.H. (2004). Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 101, 16659–16664.PubMedCentralGoogle Scholar
- Huarte, M., Lan, F., Kim, T., Vaughn, M.W., Zaratiegui, M., Martienssen, R.A., Buratowski, S., and Shi, Y. (2007). The fission yeast Jmj2 reverses histone H3 Lysine 4 trimethylation. J Biol Chem 282, 21662–21670.Google Scholar
- Iorio, M.V., Piovan, C., and Croce, C.M. (2010). Interplay between microRNAs and the epigenetic machinery: an intricate network. Biochim Biophys Acta 1799, 694–701.Google Scholar
- Irmady, K., Zechel, S., and Unsicker, K. (2011). Fibroblast growth factor 2 regulates astrocyte differentiation in a region-specific manner in the hindbrain. Glia 59, 708–719.Google Scholar
- Iwase, S., Lan, F., Bayliss, P., de la Torre-Ubieta, L., Huarte, M., Qi, H.H., Whetstine, J.R., Bonni, A., Roberts, T.M., and Shi, Y. (2007). The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128, 1077–1088.Google Scholar
- Jacobson, M. (1991). Developmental neurobiology, 3rd edn. New York: Plenum Press.Google Scholar
- Jaenisch, R., and Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33, 245–254.Google Scholar
- Jamniczky, H.A., Boughner, J.C., Rolian, C., Gonzalez, P.N., Powell, C.D., Schmidt, E.J., Parsons, T.E., Bookstein, F.L., and Hallgrímsson, B. (2010). Rediscovering Waddington in the post-genomic age: Operationalising Waddington’s epigenetics reveals new ways to investigate the generation and modulation of phenotypic variation. Bioessays 32, 553–558.Google Scholar
- Jiang, H., Shukla, A., Wang, X., Chen, W.Y., Bernstein, B.E., and Roeder, R.G. (2011). Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell 144, 513–525.PubMedCentralGoogle Scholar
- Joglekar, M.V., Joglekar, V.M., and Hardikar, A.A. (2009). Expression of islet-specific microRNAs during human pancreatic development. Gene Expr Patterns 9, 109–113.Google Scholar
- Juliandi, B., Abematsu, M., and Nakashima, K. (2010a). Chromatin remodeling in neural stem cell differentiation. Curr Opin Neurobiol 20, 408–415.Google Scholar
- Juliandi, B., Abematsu, M., and Nakashima, K. (2010b). Epigenetic regulation in neural stem cell differentiation. Dev Growth Differ 52, 493–504.Google Scholar
- Kapoor, A., Agius, F., and Zhu, J.K. (2005). Preventing transcriptional gene silencing by active DNA demethylation. FEBS Lett 579, 5889–5898.Google Scholar
- Kapsimali, M., Kloosterman, W.P., de Bruijn, E., Rosa, F., Plasterk, R.H., and Wilson, S.W. (2007). MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol 8, R173.PubMedCentralGoogle Scholar
- Kawaguchi, A., Miyata, T., Sawamoto, K., Takashita, N., Murayama, A., Akamatsu, W., Ogawa, M., Okabe, M., Tano, Y., Goldman, S.A., et al. (2001). Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17, 259–273.Google Scholar
- Kawase-Koga, Y., Low, R., Otaegi, G., Pollock, A., Deng, H., Eisenhaber, F., Maurer-Stroh, S., and Sun, T. (2010). RNAase-III enzyme Dicer maintains signaling pathways for differentiation and survival in mouse cortical neural stem cells. J Cell Sci 123, 586–594.PubMedCentralGoogle Scholar
- Kennison, J.A. (1995). The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu Rev Genet 29, 289–303.Google Scholar
- Kohyama, J., Kojima, T., Takatsuka, E., Yamashita, T., Namiki, J., Hsieh, J., Gage, F.H., Namihira, M., Okano, H., Sawamoto, K., et al. (2008). Epigenetic regulation of neural cell differentiation plasticity in the adult mammalian brain. Proc Natl Acad Sci U S A 105, 18012–18017.PubMedCentralGoogle Scholar
- Kornberg, R.D. (1974). Chromatin structure: a repeating unit of histones and DNA. Science 184, 868–871.Google Scholar
- Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693–705.Google Scholar
- Ku, M., Koche, R.P., Rheinbay, E., Mendenhall, E.M., Endoh, M., Mikkelsen, T.S., Presser, A., Nusbaum, C., Xie, X., Chi, A.S., et al. (2008). Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4, e1000242.PubMedCentralGoogle Scholar
- Kuo, M.H., and Allis, C.D. (1998). Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20, 615–626.Google Scholar
- Lan, F., Bayliss, P.E., Rinn, J.L., Whetstine, J.R., Wang, J.K., Chen, S., Iwase, S., Alpatov, R., Issaeva, I., Canaani, E., et al. (2007). A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449, 689–694.Google Scholar
- Lee, M.G., Norman, J., Shilatifard, A., and Shiekhattar, R. (2007a). Physical and functional association of a trimethyl H3K4 demethylase and Ring6a/MBLR, a polycomb-like protein. Cell 128, 877–887.Google Scholar
- Lee, M.G., Villa, R., Trojer, P., Norman, J., Yan, K.P., Reinberg, D., Di Croce, L., and Shiekhattar, R. (2007b). Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318, 447–450.Google Scholar
- Lee, Y.S., Nakahara, K., Pham, J.W., Kim, K., He, Z., Sontheimer, E.J., and Carthew, R.W. (2004). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69–81.Google Scholar
- Lessard, J., Wu, J.I., Ranish, J.A., Wan, M., Winslow, M.M., Staahl, B.T., Wu, H., Aebersold, R., Graef, I.A., and Crabtree, G.R. (2007). An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201–215.PubMedCentralGoogle Scholar
- Leucht, C., Stigloher, C., Wizenmann, A., Klafke, R., Folchert, A., and Bally-Cuif, L. (2008). MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci 11, 641–648.Google Scholar
- Li, E., Bestor, T.H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915–926.Google Scholar
- Li, J.Y., Pu, M.T., Hirasawa, R., Li, B.Z., Huang, Y.N., Zeng, R., Jing, N.H., Chen, T., Li, E., Sasaki, H., et al. (2007). Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol Cell Biol 27, 8748–8759.PubMedCentralGoogle Scholar
- Li, X., Barkho, B.Z., Luo, Y., Smrt, R.D., Santistevan, N.J., Liu, C., Kuwabara, T., Gage, F.H., and Zhao, X. (2008). Epigenetic regulation of the stem cell mitogen Fgf-2 by Mbd1 in adult neural stem/progenitor cells. J Biol Chem 283, 27644–27652.PubMedCentralGoogle Scholar
- Liu, C., Teng, Z.Q., Santistevan, N.J., Szulwach, K.E., Guo, W., Jin, P., and Zhao, X. (2010). Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell 6, 433–444.PubMedCentralGoogle Scholar
- Lunyak, V.V., and Rosenfeld, M.G. (2005). No rest for REST: REST/NRSF regulation of neurogenesis. Cell 121, 499–501.Google Scholar
- Lyle, R., Watanabe, D., te Vruchte, D., Lerchner, W., Smrzka, O.W., Wutz, A., Schageman, J., Hahner, L., Davies, C., and Barlow, D.P. (2000). The imprinted antisense RNA at the Igf2r locus overlaps but does not imprint Mas1. Nat Genet 25, 19–21.Google Scholar
- Ma, D.K., Jang, M.H., Guo, J.U., Kitabatake, Y., Chang, M.L., Pow-Anpongkul, N., Flavell, R.A., Lu, B., Ming, G.L., and Song, H. (2009). Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074–1077.PubMedCentralGoogle Scholar
- Ma, D.K., Marchetto, M.C., Guo, J.U., Ming, G.L., Gage, F.H., and Song, H. (2010). Epigenetic choreographers of neurogenesis in the adult mammalian brain. Nat Neurosci 13, 1338–1344.PubMedCentralGoogle Scholar
- Martens, J.A., and Winston, F. (2003). Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr Opin Genet Dev 13, 136–142.Google Scholar
- Mastroeni, D., Grover, A., Delvaux, E., Whiteside, C., Coleman, P.D., and Rogers, J. (2011). Epigenetic mechanisms in Alzheimer’s disease. Neurobiol Aging 32, 1161–1180.PubMedCentralGoogle Scholar
- Matsumoto, S., Banine, F., Struve, J., Xing, R., Adams, C., Liu, Y., Metzger, D., Chambon, P., Rao, M.S., and Sherman, L.S. (2006). Brg1 is required for murine neural stem cell maintenance and gliogenesis. Dev Biol 289, 372–383.Google Scholar
- Mattick, J.S., and Makunin, I.V. (2005). Small regulatory RNAs in mammals. Hum Mol Genet 14, R121–R132.Google Scholar
- Mattick, J.S., and Makunin, I.V. (2006). Non-coding RNA. Hum Mol Genet 15, R17–R29.Google Scholar
- Mehler, M.F. (2008). Epigenetic principles and mechanisms underlying nervous system functions in health and disease. Prog Neurobiol 86, 305–341.PubMedCentralGoogle Scholar
- Mehler, M.F., and Mattick, J.S. (2006). Non-coding RNAs in the nervous system. J Physiol 575, 333–341.PubMedCentralGoogle Scholar
- Mehler, M.F., and Mattick, J.S. (2007). Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiol Rev 87, 799–823.Google Scholar
- Meissner, A., Mikkelsen, T.S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B.E., Nusbaum, C., Jaffe, D.B., et al. (2008). Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766–770.PubMedCentralGoogle Scholar
- Métivier, R., Gallais, R., Tiffoche, C., Le Péron, C., Jurkowska, R.Z., Carmouche, R.P., Ibberson, D., Barath, P., Demay, F., Reid, G., et al. (2008). Cyclical DNA methylation of a transcriptionally active promoter. Nature 452, 45–50.Google Scholar
- Moazed, D. (2009). Small RNAs in transcriptional gene silencing and genome defence. Nature 457, 413–420.PubMedCentralGoogle Scholar
- Mohn, F., Weber, M., Rebhan, M., Roloff, T.C., Richter, J., Stadler, M.B., Bibel, M., and Schübeler, D. (2008). Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30, 755–766.Google Scholar
- Montgomery, R.L., Hsieh, J., Barbosa, A.C., Richardson, J.A., and Olson, E.N. (2009). Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci U S A 106, 7876–7881.PubMedCentralGoogle Scholar
- Morange, M. (2002). The relations between genetics and epigenetics: a historical point of view. Ann N Y Acad Sci 981, 50–60.Google Scholar
- Mosammaparast, N., and Shi, Y. (2010). Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79, 155–179.Google Scholar
- Nakamura, Y., Sakakibara, S., Miyata, T., Ogawa, M., Shimazaki, T., Weiss, S., Kageyama, R., and Okano, H. (2000). The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci 20, 283–293.Google Scholar
- Namihira, M., Kohyama, J., Abematsu, M., and Nakashima, K. (2008). Epigenetic mechanisms regulating fate specification of neural stem cells. Philos Trans R Soc Lond B Biol Sci 363, 2099–2109.PubMedCentralGoogle Scholar
- Nekrasov, M., Wild, B., and Müller, J. (2005). Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep 6, 348–353.PubMedCentralGoogle Scholar
- Nguyen, S., Meletis, K., Fu, D., Jhaveri, S., and Jaenisch, R. (2007). Ablation of de novo DNA methyltransferase Dnmt3a in the nervous system leads to neuromuscular defects and shortened lifespan. Dev Dyn 236, 1663–1676.Google Scholar
- Niehrs, C. (2009). Active DNA demethylation and DNA repair. Differentiation 77, 1–11.Google Scholar
- Okano, M., Bell, D.W., Haber, D.A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–257.Google Scholar
- Ooi, S.K., and Bestor, T.H. (2008a). The colorful history of active DNA demethylation. Cell 133, 1145–1148.Google Scholar
- Ooi, S.K., and Bestor, T.H. (2008b). Cytosine methylation: remaining faithful. Curr Biol 18, R174–R176.Google Scholar
- Pastor, W.A., Pape, U.J., Huang, Y., Henderson, H.R., Lister, R., Ko, M., McLoughlin, E.M., Brudno, Y., Mahapatra, S., Kapranov, P., et al. (2011). Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473, 394–397.PubMedCentralGoogle Scholar
- Pazin, M.J., and Kadonaga, J.T. (1997). What’s up and down with histone deacetylation and transcription? Cell 89, 325–328.Google Scholar
- Qian, X., Goderie, S.K., Shen, Q., Stern, J.H., and Temple, S. (1998). Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125, 3143–3152.Google Scholar
- Qian, X., Shen, Q., Goderie, S.K., He, W., Capela, A., Davis, A.A., and Temple, S. (2000). Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28, 69–80.Google Scholar
- Rai, K., Huggins, I.J., James, S.R., Karpf, A.R., Jones, D.A., and Cairns, B.R. (2008). DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135, 1201–1212.PubMedCentralGoogle Scholar
- Randazzo, F.M., Khavari, P., Crabtree, G., Tamkun, J., and Rossant, J. (1994). brg1: a putative murine homologue of the Drosophila brahma gene, a homeotic gene regulator. Dev Biol 161, 229–242.Google Scholar
- Ravin, R., Hoeppner, D.J., Munno, D.M., Carmel, L., Sullivan, J., Levitt, D.L., Miller, J.L., Athaide, C., Panchision, D.M., and McKay, R.D. (2008). Potency and fate specification in CNS stem cell populations in vitro. Cell Stem Cell 3, 670–680.Google Scholar
- Reynolds, B.A., and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707–1710.Google Scholar
- Ringrose, L., and Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38, 413–443.Google Scholar
- Robertson, K.D., Ait-Si-Ali, S., Yokochi, T., Wade, P.A., Jones, P.L., and Wolffe, A.P. (2000). DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet 25, 338–342.Google Scholar
- Robertson, K.D., and Wolffe, A.P. (2000). DNA methylation in health and disease. Nat Rev Genet 1, 11–19.Google Scholar
- Roth, S.Y., and Allis, C.D. (1996). Histone acetylation and chromatin assembly: a single escort, multiple dances? Cell 87, 5–8.Google Scholar
- Rougeulle, C., Chaumeil, J., Sarma, K., Allis, C.D., Reinberg, D., Avner, P., and Heard, E. (2004). Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 24, 5475–5484.PubMedCentralGoogle Scholar
- Sato, S., Yagi, S., Arai, Y., Hirabayashi, K., Hattori, N., Iwatani, M., Okita, K., Ohgane, J., Tanaka, S., Wakayama, T., et al. (2010). Genome-wide DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) residing in mouse pluripotent stem cells. Genes Cells 15, 607–618.Google Scholar
- Schmitz, S.U., Albert, M., Malatesta, M., Morey, L., Johansen, J.V., Bak, M., Tommerup, N., Abarrategui, I., and Helin, K. (2011). Jarid1b targets genes regulating development and is involved in neural differentiation. EMBO J 30, 4586–4600.PubMedCentralGoogle Scholar
- Setoguchi, H., Namihira, M., Kohyama, J., Asano, H., Sanosaka, T., and Nakashima, K. (2006). Methyl-CpG binding proteins are involved in restricting differentiation plasticity in neurons. J Neurosci Res 84, 969–979.Google Scholar
- Shen, Q., and Temple, S. (2009). Fine control: microRNA regulation of adult neurogenesis. Nat Neurosci 12, 369–370.Google Scholar
- 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.Google Scholar
- Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A., Casero, R.A., and Shi, Y. (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941–953.Google Scholar
- Shibata, M., Kurokawa, D., Nakao, H., Ohmura, T., and Aizawa, S. (2008). MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J Neurosci 28, 10415–10421.Google Scholar
- Smith, C.L., and Peterson, C.L. (2005). A conserved Swi2/Snf2 ATPase motif couples ATP hydrolysis to chromatin remodeling. Mol Cell Biol 25, 5880–5892.PubMedCentralGoogle Scholar
- Smith, J.L., and Schoenwolf, G.C. (1997). Neurulation: coming to closure. Trends Neurosci 20, 510–517.Google Scholar
- So, A.Y., Jung, J.W., Lee, S., Kim, H.S., and Kang, K.S. (2011). DNA methyltransferase controls stem cell aging by regulating BMI1 and EZH2 through microRNAs. PLoS One 6, e19503.PubMedCentralGoogle Scholar
- Song, C.X., Szulwach, K.E., Fu, Y., Dai, Q., Yi, C., Li, X., Li, Y., Chen, C.H., Zhang, W., Jian, X., et al. (2011). Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol 29, 68–72.PubMedCentralGoogle Scholar
- Song, M.R., and Ghosh, A. (2004). FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nat Neurosci 7, 229–235.Google Scholar
- Sterner, D.E., and Berger, S.L. (2000). Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 64, 435–459.PubMedCentralGoogle Scholar
- Storz, G. (2002). An expanding universe of noncoding RNAs. Science 296, 1260–1263.Google Scholar
- Sun, G., Fu, C., Shen, C., and Shi, Y. (2011). Histone deacetylases in neural stem cells and induced pluripotent stem cells. J Biomed Biotechnol 2011, 835968.Google Scholar
- Sun, G., Yu, R.T., Evans, R.M., and Shi, Y. (2007). Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc Natl Acad Sci U S A 104, 15282–15287.PubMedCentralGoogle Scholar
- Surani, M.A., Hayashi, K., and Hajkova, P. (2007). Genetic and epigenetic regulators of pluripotency. Cell 128, 747–762.Google Scholar
- Suzuki, M.M., and Bird, A. (2008). DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9, 465–476.Google Scholar
- Temple, S. (2001). The development of neural stem cells. Nature 414, 112–117.Google Scholar
- Testa, G. (2011). The time of timing: how Polycomb proteins regulate neurogenesis. Bioessays 33, 519–528.Google Scholar
- Tropepe, V., Sibilia, M., Ciruna, B.G., Rossant, J., Wagner, E.F., and van der Kooy, D. (1999). Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208, 166–188.Google Scholar
- Tsujimura, K., Abematsu, M., Kohyama, J., Namihira, M., and Nakashima, K. (2009). Neuronal differentiation of neural precursor cells is promoted by the methyl-CpG-binding protein MeCP2. Exp Neurol 219, 104–111.Google Scholar
- Viré, E., Brenner, C., Deplus, R., Blanchon, L., Fraga, M., Didelot, C., Morey, L., Van Eynde, A., Bernard, D., Vanderwinden, J.M., et al. (2006). The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871–874.Google Scholar
- Wade, P.A., Pruss, D., and Wolffe, A.P. (1997). Histone acetylation: chromatin in action. Trends Biochem Sci 22, 128–132.Google Scholar
- Walsh, C.P., and Bestor, T.H. (1999). Cytosine methylation and mammalian development. Genes Dev 13, 26–34.PubMedCentralGoogle Scholar
- Wang, H., Wang, L., Erdjument-Bromage, H., Vidal, M., Tempst, P., Jones, R.S., and Zhang, Y. (2004). Role of histone H2A ubiquitination in Polycomb silencing. Nature 431, 873–878.Google Scholar
- Weiss, A., and Cedar, H. (1997). The role of DNA demethylation during development. Genes Cells 2, 481–486.Google Scholar
- Whetstine, J.R., Nottke, A., Lan, F., Huarte, M., Smolikov, S., Chen, Z., Spooner, E., Li, E., Zhang, G., Colaiacovo, M., et al. (2006). Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125, 467–481.Google Scholar
- Wilks, A., Seldran, M., and Jost, J.P. (1984). An estrogen-dependent demethylation at the 5′ end of the chicken vitellogenin gene is independent of DNA synthesis. Nucleic Acids Res 12, 1163–1177.PubMedCentralGoogle Scholar
- Wood, H.B., and Episkopou, V. (1999). Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86, 197–201.Google Scholar
- Wu, H., Coskun, V., Tao, J., Xie, W., Ge, W., Yoshikawa, K., Li, E., Zhang, Y., and Sun, Y.E. (2010a). Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329, 444–448.PubMedCentralGoogle Scholar
- Wu, H., D’Alessio, A.C., Ito, S., Wang, Z., Cui, K., Zhao, K., Sun, Y.E., and Zhang, Y. (2011a). Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 25, 679–684.PubMedCentralGoogle Scholar
- Wu, H., D’Alessio, A.C., Ito, S., Xia, K., Wang, Z., Cui, K., Zhao, K., Sun, Y.E., and Zhang, Y. (2011b). Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473, 389–393.PubMedCentralGoogle Scholar
- Wu, H., and Sun, Y.E. (2009). Reversing DNA methylation: new insights from neuronal activity-induced Gadd45b in adult neurogenesis. Sci Signal 2, pe17.Google Scholar
- Wu, H., Tao, J., Chen, P.J., Shahab, A., Ge, W., Hart, R.P., Ruan, X., Ruan, Y., and Sun, Y.E. (2010b). Genome-wide analysis reveals methyl-CpG-binding protein 2-dependent regulation of microRNAs in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A 107, 18161–18166.PubMedCentralGoogle Scholar
- Wu, J., and Xie, X. (2006). Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression. Genome Biol 7, R85.PubMedCentralGoogle Scholar
- Wu, J.I., Lessard, J., Olave, I.A., Qiu, Z., Ghosh, A., Graef, I.A., and Crabtree, G.R. (2007). Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56, 94–108.Google Scholar
- Xu, Y., Wu, F., Tan, L., Kong, L., Xiong, L., Deng, J., Barbera, A.J., Zheng, L., Zhang, H., Huang, S., et al. (2011). Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42, 451–464.PubMedCentralGoogle Scholar
- Yamane, K., Toumazou, C., Tsukada, Y., Erdjument-Bromage, H., Tempst, P., Wong, J., and Zhang, Y. (2006). JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125, 483–495.Google Scholar
- Ye, F., Chen, Y., Hoang, T., Montgomery, R.L., Zhao, X.H., Bu, H., Hu, T., Taketo, M.M., van Es, J.H., Clevers, H., et al. (2009). HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12, 829–838.PubMedCentralGoogle Scholar
- Yoder, J.A., Walsh, C.P., and Bestor, T.H. (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13, 335–340.Google Scholar
- Yoo, A.S., Staahl, B.T., Chen, L., and Crabtree, G.R. (2009). MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460, 642–646.PubMedCentralGoogle Scholar
- Yoo, A.S., Sun, A.X., Li, L., Shcheglovitov, A., Portmann, T., Li, Y., Lee-Messer, C., Dolmetsch, R.E., Tsien, R.W., and Crabtree, G.R. (2011). MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476, 228–231.PubMedCentralGoogle Scholar
- Yu, I.T., Park, J.Y., Kim, S.H., Lee, J.S., Kim, Y.S., and Son, H. (2009). Valproic acid promotes neuronal differentiation by induction of proneural factors in association with H4 acetylation. Neuropharmacology 56, 473–480.Google Scholar
- Zhan, X., Shi, X., Zhang, Z., Chen, Y., and Wu, J.I. (2011). Dual role of Brg chromatin remodeling factor in Sonic hedgehog signaling during neural development. Proc Natl Acad Sci U S A 108, 12758–12763.PubMedCentralGoogle Scholar
- Zhang, Y., and Reinberg, D. (2001). Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 15, 2343–2360.Google Scholar
- Zhao, C., Sun, G., Li, S., and Shi, Y. (2009). A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 16, 365–371.PubMedCentralGoogle Scholar
- Zhao, X., Ueba, T., Christie, B.R., Barkho, B., McConnell, M.J., Nakashima, K., Lein, E.S., Eadie, B.D., Willhoite, A.R., Muotri, A.R., et al. (2003). Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc Natl Acad Sci U S A 100, 6777–6782.PubMedCentralGoogle Scholar
- Zhao, Z., Yu, Y., Meyer, D., Wu, C., and Shen, W.H. (2005). Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat Cell Biol 7, 1256–1260.Google Scholar