Epigenetic control on cell fate choice in neural stem cells
Epigenetic control on cell fate choice in neural stem cells
Xiao-Ling Hu1, Yuping Wang2, Qin Shen1()
1. Center for Stem Cell Biology and Regenerative Medicine, School of Medicine, Tsinghua Center for Life Sciences, Tsinghua University, Beijing 100084, China; 2. Department of Pharmacy, Tianjin Children’s Hospital, Tianjin 300074, China
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.
Allis, C.D., Berger, S.L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R., . (2007). New nomenclature for chromatin-modifying enzymes. Cell 131, 633-636 . doi: 10.1016/j.cell.2007.10.039
2
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 . doi: 10.1093/nar/gki830
3
Ambros, V. (2003). MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell 113, 673-676 . doi: 10.1016/S0092-8674(03)00428-8
4
Ambros, V. (2004). The functions of animal microRNAs. Nature 431, 350-355 . doi: 10.1038/nature02871
5
Azuara, V., Perry, P., Sauer, S., Spivakov, M., J?rgensen, H.F., John, R.M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M., . (2006). Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8, 532-538 . doi: 10.1038/ncb1403
6
Balazs, R., Vernon, J., and Hardy, J. (2011). Epigenetic mechanisms in Alzheimer’s disease: progress but much to do. Neurobiol Aging 32, 1181-1187 . doi: 10.1016/j.neurobiolaging.2011.02.024
7
Bannister, A.J., and Kouzarides, T. (2005). Reversing histone methylation. Nature 436, 1103-1106 . doi: 10.1038/nature04048
8
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 . doi: 10.1074/jbc.M500796200
Bernstein, B.E., Meissner, A., and Lander, E.S. (2007). The mammalian epigenome. Cell 128, 669-681 . doi: 10.1016/j.cell.2007.01.033
12
Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., . (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 . doi: 10.1016/j.cell.2006.02.041
13
Bernstein, E., and Allis, C.D. (2005). RNA meets chromatin. Genes Dev 19, 1635-1655 . doi: 10.1101/gad.1324305
14
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 . doi: 10.1038/nature08752
15
Bhutani, N., Burns, D.M., and Blau, H.M. (2011). DNA demethylation dynamics. Cell 146, 866-872 . doi: 10.1016/j.cell.2011.08.042
16
Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev 16, 6-21 . doi: 10.1101/gad.947102
17
Bird, A. (2007). Perceptions of epigenetics. Nature 447, 396-398 . doi: 10.1038/nature05913
18
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. doi: 10.1371/journal.pone.0003034
19
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 . doi: 10.1126/science.1076997
20
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 . doi: 10.1146/annurev.neuro.29.051605.112839
21
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 . doi: 10.1016/j.ydbio.2007.12.016
22
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 . doi: 10.1038/nn.2294
23
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 . doi: 10.1038/nature08315
24
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 . doi: 10.1038/nature04837
25
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 . doi: 10.1073/pnas.0511041103
26
Coolen, M., and Bally-Cuif, L. (2009). MicroRNAs in brain development and physiology. Curr Opin Neurobiol 19, 461-470 . doi: 10.1016/j.conb.2009.09.006
27
Cortellino, S., Xu, J., Sannai, M., Moore, R., Caretti, E., Cigliano, A., Le Coz, M., Devarajan, K., Wessels, A., Soprano, D., . (2011). Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79 . doi: 10.1016/j.cell.2011.06.020
28
De Carvalho, D.D., You, J.S., and Jones, P.A. (2010). DNA methylation and cellular reprogramming. Trends Cell Biol 20, 609-617 . doi: 10.1016/j.tcb.2010.08.003
29
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 . doi: 10.1038/nrg1882
30
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 . doi: 10.1242/dev.025080
31
Deaton, A.M., and Bird, A. (2011). CpG islands and the regulation of transcription. Genes Dev 25, 1010-1022 . doi: 10.1101/gad.2037511
32
Eden, S., Hashimshony, T., Keshet, I., Cedar, H., and Thorne, A.W. (1998). DNA methylation models histone acetylation. Nature 394, 842. doi: 10.1038/29680
33
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 . doi: 10.1038/sj.emboj.7601967
34
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 . doi: 10.1016/j.stem.2008.09.002
35
Fan, G., Martinowich, K., Chin, M.H., He, F., Fouse, S.D., Hutnick, L., Hattori, D., Ge, W., Shen, Y., Wu, H., . (2005). DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132, 3345-3356 . doi: 10.1242/dev.01912
36
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 . doi: 10.1002/jnr.20404
37
Ferrón, S.R., Charalambous, M., Radford, E., McEwen, K., Wildner, H., Hind, E., Morante-Redolat, J.M., Laborda, J., Guillemot, F., Bauer, S.R., . (2011). Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 475, 381-385 . doi: 10.1038/nature10229
38
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 . doi: 10.1038/nature10008
39
Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S.N., . (2008). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357 . doi: 10.1038/nature07287
40
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 . doi: 10.4161/epi.5.5.11999
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 .
43
Goldberg, A.D., Allis, C.D., and Bernstein, E. (2007). Epigenetics: a landscape takes shape. Cell 128, 635-638 . doi: 10.1016/j.cell.2007.02.006
44
Golebiewska, A., Atkinson, S.P., Lako, M., and Armstrong, L. (2009). Epigenetic landscaping during hESC differentiation to neural cells. Stem Cells 27, 1298-1308 . doi: 10.1002/stem.59
Goll, M.G., and Halpern, M.E. (2011). DNA methylation in zebrafish. Prog Mol Biol Transl Sci 101, 193-218 . doi: 10.1016/B978-0-12-387685-0.00005-6
47
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 . doi: 10.1093/nar/gkm952
48
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 . doi: 10.1016/j.molcel.2007.06.017
49
Groth, A., Rocha, W., Verreault, A., and Almouzni, G. (2007). Chromatin challenges during DNA replication and repair. Cell 128, 721-733 . doi: 10.1016/j.cell.2007.01.030
50
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 . doi: 10.1016/j.cell.2011.03.022
51
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 . doi: 10.1007/s10142-011-0246-z
52
Hargreaves, D.C., and Crabtree, G.R. (2011). ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 21, 396-420 . doi: 10.1038/cr.2011.32
53
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 . doi: 10.1038/ng1158
54
He, L., and Hannon, G.J. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5, 522-531 . doi: 10.1038/nrg1379
He, Y.F., Li, B.Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L., . (2011b). Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307 . doi: 10.1126/science.1210944
57
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 . doi: 10.1159/000072263
58
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 . doi: 10.1101/gad.975202
59
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 . doi: 10.1038/nn.2875
60
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 . doi: 10.1101/gad.1208404
61
Holliday, R. (2006). Epigenetics: a historical overview. Epigenetics 1, 76-80 . doi: 10.4161/epi.1.2.2762
62
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 . doi: 10.1073/pnas.0407643101
63
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 . doi: 10.1074/jbc.M703897200
64
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 .
65
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 . doi: 10.1002/glia.21141
66
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 . doi: 10.1016/j.cell.2007.02.017
67
Jacobson, M. (1991). Developmental neurobiology, 3rd edn. New York: Plenum Press.
68
Jaenisch, R., and Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33, 245-254 . doi: 10.1038/ng1089
69
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 . doi: 10.1002/bies.200900189
70
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 . doi: 10.1016/j.cell.2011.01.020
71
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 . doi: 10.1016/j.gep.2008.10.001
72
Juliandi, B., Abematsu, M., and Nakashima, K. (2010a). Chromatin remodeling in neural stem cell differentiation. Curr Opin Neurobiol 20, 408-415 . doi: 10.1016/j.conb.2010.04.001
73
Juliandi, B., Abematsu, M., and Nakashima, K. (2010b). Epigenetic regulation in neural stem cell differentiation. Dev Growth Differ 52, 493-504 . doi: 10.1111/j.1440-169X.2010.01175.x
74
Kapoor, A., Agius, F., and Zhu, J.K. (2005). Preventing transcriptional gene silencing by active DNA demethylation. FEBS Lett 579, 5889-5898 . doi: 10.1016/j.febslet.2005.08.039
75
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. doi: 10.1186/gb-2007-8-8-r173
76
Kawaguchi, A., Miyata, T., Sawamoto, K., Takashita, N., Murayama, A., Akamatsu, W., Ogawa, M., Okabe, M., Tano, Y., Goldman, S.A., . (2001). Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17, 259-273 . doi: 10.1006/mcne.2000.0925
77
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 . doi: 10.1242/jcs.059659
78
Kennison, J.A. (1995). The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu Rev Genet 29, 289-303 . doi: 10.1146/annurev.ge.29.120195.001445
79
Kohyama, J., Kojima, T., Takatsuka, E., Yamashita, T., Namiki, J., Hsieh, J., Gage, F.H., Namihira, M., Okano, H., Sawamoto, K., . (2008). Epigenetic regulation of neural cell differentiation plasticity in the adult mammalian brain. Proc Natl Acad Sci U S A 105, 18012-18017 . doi: 10.1073/pnas.0808417105
80
Kornberg, R.D. (1974). Chromatin structure: a repeating unit of histones and DNA. Science 184, 868-871 . doi: 10.1126/science.184.4139.868
81
Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705 . doi: 10.1016/j.cell.2007.02.005
82
Ku, M., Koche, R.P., Rheinbay, E., Mendenhall, E.M., Endoh, M., Mikkelsen, T.S., Presser, A., Nusbaum, C., Xie, X., Chi, A.S., . (2008). Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4, e1000242. doi: 10.1371/journal.pgen.1000242
Lan, F., Bayliss, P.E., Rinn, J.L., Whetstine, J.R., Wang, J.K., Chen, S., Iwase, S., Alpatov, R., Issaeva, I., Canaani, E., . (2007). A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449, 689-694 . doi: 10.1038/nature06192
85
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 . doi: 10.1016/j.cell.2007.02.004
86
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 . doi: 10.1126/science.1149042
87
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 . doi: 10.1016/S0092-8674(04)00261-2
88
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 . doi: 10.1016/j.neuron.2007.06.019
89
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 . doi: 10.1038/nn.2115
90
Li, E., Bestor, T.H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926 . doi: 10.1016/0092-8674(92)90611-F
91
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., . (2007). Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol Cell Biol 27, 8748-8759 . doi: 10.1128/MCB.01380-07
92
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 . doi: 10.1074/jbc.M804899200
93
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 . doi: 10.1016/j.stem.2010.02.017
94
Lunyak, V.V., and Rosenfeld, M.G. (2005). No rest for REST: REST/NRSF regulation of neurogenesis. Cell 121, 499-501 . doi: 10.1016/j.cell.2005.05.003
95
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 . doi: 10.1038/75546
96
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 . doi: 10.1126/science.1166859
97
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 . doi: 10.1038/nn.2672
98
Martens, J.A., and Winston, F. (2003). Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr Opin Genet Dev 13, 136-142 . doi: 10.1016/S0959-437X(03)00022-4
99
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 . doi: 10.1016/j.neurobiolaging.2010.08.017
100
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 . doi: 10.1016/j.ydbio.2005.10.044
101
Mattick, J.S., and Makunin, I.V. (2005). Small regulatory RNAs in mammals. Hum Mol Genet 14, R121-R132 . doi: 10.1093/hmg/ddi101
Mehler, M.F. (2008). Epigenetic principles and mechanisms underlying nervous system functions in health and disease. Prog Neurobiol 86, 305-341 . doi: 10.1016/j.pneurobio.2008.10.001
104
Mehler, M.F., and Mattick, J.S. (2006). Non-coding RNAs in the nervous system. J Physiol 575, 333-341 . doi: 10.1113/jphysiol.2006.113191
105
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 . doi: 10.1152/physrev.00036.2006
106
Meissner, A., Mikkelsen, T.S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B.E., Nusbaum, C., Jaffe, D.B., . (2008). Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770 .
107
Métivier, R., Gallais, R., Tiffoche, C., Le Péron, C., Jurkowska, R.Z., Carmouche, R.P., Ibberson, D., Barath, P., Demay, F., Reid, G., . (2008). Cyclical DNA methylation of a transcriptionally active promoter. Nature 452, 45-50 . doi: 10.1038/nature06544
108
Moazed, D. (2009). Small RNAs in transcriptional gene silencing and genome defence. Nature 457, 413-420 . doi: 10.1038/nature07756
109
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 . doi: 10.1016/j.molcel.2008.05.007
110
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 . doi: 10.1073/pnas.0902750106
111
Morange, M. (2002). The relations between genetics and epigenetics: a historical point of view. Ann N Y Acad Sci 981, 50-60 . doi: 10.1111/j.1749-6632.2002.tb04911.x
112
Mosammaparast, N., and Shi, Y. (2010). Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79, 155-179 . doi: 10.1146/annurev.biochem.78.070907.103946
113
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 .
114
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 . doi: 10.1098/rstb.2008.2262
115
Nekrasov, M., Wild, B., and Müller, J. (2005). Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep 6, 348-353 . doi: 10.1038/sj.embor.7400376
116
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 . doi: 10.1002/dvdy.21176
117
Niehrs, C. (2009). Active DNA demethylation and DNA repair. Differentiation 77, 1-11 . doi: 10.1016/j.diff.2008.09.004
118
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 . doi: 10.1016/S0092-8674(00)81656-6
119
Ooi, S.K., and Bestor, T.H. (2008a). The colorful history of active DNA demethylation. Cell 133, 1145-1148 . doi: 10.1016/j.cell.2008.06.009
Pastor, W.A., Pape, U.J., Huang, Y., Henderson, H.R., Lister, R., Ko, M., McLoughlin, E.M., Brudno, Y., Mahapatra, S., Kapranov, P., . (2011). Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473, 394-397 . doi: 10.1038/nature10102
122
Pazin, M.J., and Kadonaga, J.T. (1997). What’s up and down with histone deacetylation and transcription? Cell 89, 325-328 . doi: 10.1016/S0092-8674(00)80211-1
123
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 .
124
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 . doi: 10.1016/S0896-6273(00)00086-6
125
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 . doi: 10.1016/j.cell.2008.11.042
126
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 . doi: 10.1006/dbio.1994.1023
127
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 . doi: 10.1016/j.stem.2008.09.012
128
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 . doi: 10.1126/science.1553558
129
Ringrose, L., and Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38, 413-443 . doi: 10.1146/annurev.genet.38.072902.091907
130
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 . doi: 10.1038/77124
131
Robertson, K.D., and Wolffe, A.P. (2000). DNA methylation in health and disease. Nat Rev Genet 1, 11-19 . doi: 10.1038/35049533
132
Roth, S.Y., and Allis, C.D. (1996). Histone acetylation and chromatin assembly: a single escort, multiple dances? Cell 87, 5-8 . doi: 10.1016/S0092-8674(00)81316-1
133
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 . doi: 10.1128/MCB.24.12.5475-5484.2004
134
Sato, S., Yagi, S., Arai, Y., Hirabayashi, K., Hattori, N., Iwatani, M., Okita, K., Ohgane, J., Tanaka, S., Wakayama, T., . (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 . doi: 10.1111/j.1365-2443.2010.01404.x
135
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 . doi: 10.1038/emboj.2011.383
136
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 . doi: 10.1002/jnr.21001
137
Shen, Q., and Temple, S. (2009). Fine control: microRNA regulation of adult neurogenesis. Nat Neurosci 12, 369-370 . doi: 10.1038/nn0409-369
138
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 . doi: 10.1038/nn1694
139
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 . doi: 10.1016/j.cell.2004.12.012
140
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 . doi: 10.1523/JNEUROSCI.3219-08.2008
141
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 . doi: 10.1128/MCB.25.14.5880-5892.2005
142
Smith, J.L., and Schoenwolf, G.C. (1997). Neurulation: coming to closure. Trends Neurosci 20, 510-517 . doi: 10.1016/S0166-2236(97)01121-1
143
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. doi: 10.1371/journal.pone.0019503
144
Song, C.X., Szulwach, K.E., Fu, Y., Dai, Q., Yi, C., Li, X., Li, Y., Chen, C.H., Zhang, W., Jian, X., . (2011). Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcyt-osine. Nat Biotechnol 29, 68-72 . doi: 10.1038/nbt.1732
145
Song, M.R., and Ghosh, A. (2004). FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nat Neurosci 7, 229-235 . doi: 10.1038/nn1192
146
Sterner, D.E., and Berger, S.L. (2000). Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 64, 435-459 . doi: 10.1128/MMBR.64.2.435-459.2000
147
Storz, G. (2002). An expanding universe of noncoding RNAs. Science 296, 1260-1263 . doi: 10.1126/science.1072249
148
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. doi: 10.1155/2011/835968
149
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 . doi: 10.1073/pnas.0704089104
150
Surani, M.A., Hayashi, K., and Hajkova, P. (2007). Genetic and epigenetic regulators of pluripotency. Cell 128, 747-762 . doi: 10.1016/j.cell.2007.02.010
151
Suzuki, M.M., and Bird, A. (2008). DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9, 465-476 . doi: 10.1038/nrg2341
152
Temple, S. (2001). The development of neural stem cells. Nature 414, 112-117 . doi: 10.1038/35102174
153
Testa, G. (2011). The time of timing: how Polycomb proteins regulate neurogenesis. Bioessays 33, 519-528 . doi: 10.1002/bies.201100021
154
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 . doi: 10.1006/dbio.1998.9192
155
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 . doi: 10.1016/j.expneurol.2009.05.001
156
Viré, E., Brenner, C., Deplus, R., Blanchon, L., Fraga, M., Didelot, C., Morey, L., Van Eynde, A., Bernard, D., Vanderwinden, J.M., . (2006). The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871-874 . doi: 10.1038/nature04431
157
Wade, P.A., Pruss, D., and Wolffe, A.P. (1997). Histone acetylation: chromatin in action. Trends Biochem Sci 22, 128-132 . doi: 10.1016/S0968-0004(97)01016-5
158
Walsh, C.P., and Bestor, T.H. (1999). Cytosine methylation and mammalian development. Genes Dev 13, 26-34 . doi: 10.1101/gad.13.1.26
159
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 . doi: 10.1038/nature02985
160
Weiss, A., and Cedar, H. (1997). The role of DNA demethylation during development. Genes Cells 2, 481-486 . doi: 10.1046/j.1365-2443.1997.1390337.x
161
Whetstine, J.R., Nottke, A., Lan, F., Huarte, M., Smolikov, S., Chen, Z., Spooner, E., Li, E., Zhang, G., Colaiacovo, M., . (2006). Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125, 467-481 . doi: 10.1016/j.cell.2006.03.028
162
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 . doi: 10.1093/nar/12.2.1163
163
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 . doi: 10.1016/S0925-4773(99)00116-1
164
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 . doi: 10.1126/science.1190485
165
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-hydroxymet-hylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 25, 679-684 . doi: 10.1101/gad.2036011
166
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 . doi: 10.1038/nature09934
167
Wu, H., and Sun, Y.E. (2009). Reversing DNA methylation: new insights from neuronal activity-induced Gadd45b in adult neurogenesis. Sci Signal 2, pe17. doi: 10.1126/scisignal.264pe17
168
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 . doi: 10.1073/pnas.1005595107
169
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. doi: 10.1186/gb-2006-7-9-r85
170
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 . doi: 10.1016/j.neuron.2007.08.021
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 . doi: 10.1016/j.cell.2006.03.027
173
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., . (2009). HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12, 829-838 . doi: 10.1038/nn.2333
174
Yoder, J.A., Walsh, C.P., and Bestor, T.H. (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13, 335-340 . doi: 10.1016/S0168-9525(97)01181-5
175
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 .
176
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 . doi: 10.1038/nature10323
177
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 . doi: 10.1016/j.neuropharm.2008.09.019
178
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 . doi: 10.1073/pnas.1018510108
179
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 . doi: 10.1101/gad.927301
180
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 . doi: 10.1038/nsmb.1576
181
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., . (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 . doi: 10.1073/pnas.1131928100
182
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 . doi: 10.1038/ncb1329
