Genetics and epigenetics in adult neurogenesis

Cold Spring Harbor Perspectives in Biology

Volumn 8, Issue 6, 2016, Pages

  Hsieh, Jenny ^a   Zhao, Xinyu ^b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UNTRANSLATED RNA;

ANIMAL; BRAIN; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; GENETIC EPIGENESIS; HUMAN; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHYSIOLOGY;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EPIGENESIS, GENETIC; HUMANS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; RNA, UNTRANSLATED;

EID: 84973161212     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a018911     Document Type: Article

References (133)

1. Ajamian F, Suuronen T, Salminen A, Reeben M. 2003. Upregulation of class II histone deacetylases mRNA during neural differentiation of cultured rat hippocampal progenitor cells. Neurosci Lett 346: 57-60.
2. Albert M, Helin K. 2010. Histone methyltransferases in cancer. Semin Cell Dev Biol 21: 209-220.
3. Allan AM, Liang X, Luo Y, Pak C, Li X, Szulwach KE, Chen D, Jin P, Zhao X. 2008. The loss of methyl-CpG binding protein 1 leads to autism-like behavioral deficits. Hum Mol Genet 17: 2047-2057.
4. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23: 185-188.
5. Ananiev G, Williams EC, Li H, Chang Q. 2011. Isogenic pairs of wild type and mutant induced pluripotent stem cell (iPSC) lines from Rett syndrome patients as in vitro disease model. PLoS ONE 6: e25255.
6. Ballas N, Battaglioli E, Atouf F, Andres ME, Chenoweth J, Anderson ME, Burger C, Moniwa M, Davie JR, Bowers WJ, et al. 2001. Regulation of neuronal traits by a novel transcriptional complex. Neuron 31: 353-365.
7. Barry G, Briggs JA, Vanichkina DP, Poth EM, Beveridge NJ, Ratnu VS, Nayler SP, Nones K, Hu J, Bredy TW, et al. 2013. The long non-coding RNA Gomafu is acutely regulated in response to neuronal activation and involved in schizophrenia-associated alternative splicing. Mol Psychiatry 19: 486-494.
8. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
9. Becker PB, Horz W. 2002. ATP-dependent nucleosome remodeling. Annu Rev Biochem 71: 247-273.
10. Bernstein BE, Meissner A, Lander ES. 2007. Themammalian epigenome. Cell 128: 669-681.
11. Biacsi R, Kumari D, Usdin K. 2008. SIRT2 inhibition alleviates gene silencing in Fragile X mental retardation syndrome. PLoS Genet 4: e1000017.
12. Bruce AW, Donaldson IJ, Wood IC, Yerbury SA, Sadowski MI, Chapman M, Gottgens B, Buckley NJ. 2004. Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes. Proc Natl Acad Sci 101: 10458-10463.
13. Cao X, Yeo G, Muotri AR, Kuwabara T, Gage FH. 2006. Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci 29: 77-103.
14. Chen ZX, Riggs AD. 2011. DNA methylation and demethylation in mammals. J Biol Chem 286: 18347-18353.
15. Cheng L, Pastrana E, Tavazoie M, Doetsch F. 2009. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12: 399-408.
16. Chiurazzi P, Pomponi MG, Willemsen R, Oostra BA, Neri G. 1998. In vitro reactivation of the FMR1 gene involved in fragile X syndrome. Hum Mol Genet 7: 109-113.
17. Chiurazzi P, Pomponi MG, Pietrobono R, Bakker CE, Neri G, Oostra BA. 1999. Synergistic effect of histone hyperacetylation andDNAdemethylation in the reactivation of the FMR1 gene. Hum Mol Genet 8: 2317-2323.
18. Coffee B, Zhang F, Warren ST, Reines D. 1999. Acetylated histones are associated with FMR1 in normal but not fragile X-syndrome cells. Nat Genet 22: 98-101.
19. Chong JA, Tapia-Ramirez J, Kim S, Toledo-Aral JJ, Zheng Y, Boutros MC, Altshuller YM, Frohman MA, Kraner SD, Mandel G. 1995. REST: A mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80: 949-957.
20. Conaco C, Otto S, Han JJ, Mandel G. 2006. Reciprocal actions of RESTand a microRNA promote neuronal identity. Proc Natl Acad Sci 103: 2422-2427.
21. Cui H, Ma J, Ding J, Li T, Alam G, Ding HF. 2006. Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentration-dependent manner. J Biol Chem 281: 34696-34704.
22. Cukier HN, Rabionet R, Konidari I, Rayner-Evans MY, Baltos ML, Wright HH, Abramson RK, Martin ER, Cuccaro ML, Pericak-Vance MA, et al. 2010. Novel variants identified in methyl-CpG-binding domain genes in autistic individuals. Neurogenetics 11: 291-303.
23. Defossez PA, Stancheva I. 2011. Biological functions of methyl-CpG-binding proteins. Prog Mol Biol Transl Sci 101: 377-398.
24. De Pietri Tonelli D, Pulvers JN, Haffner C, Murchison EP, Hannon GJ, Huttner WB. 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.
25. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB. 2003. Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem J 370: 737-749.
26. Fan G, Beard C, Chen RZ, Csankovszki G, Sun Y, Siniaia M, Biniszkiewicz D, Bates B, Lee PP, Kuhn R, et al. 2001. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J Neurosci 21: 788-797.
27. Fan G, Martinowich K, Chin MH, He F, Fouse SD, 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.
28. Farra N, Zhang WB, Pasceri P, Eubanks JH, Salter MW, Ellis J. 2012. Rett syndrome induced pluripotent stem cellderived neurons reveal novel neurophysiological alterations. Mol Psychiatry 17: 1261-1271.
29. Feenstra I, Vissers LE, Orsel M, van Kessel AG, Brunner HG, Veltman JA, van Ravenswaaij-Arts CM. 2007. Genotype-phenotype mapping of chromosome 18q deletions by high-resolution array CGH: An update of the phenotypic map. Am J Med Genet A 143A: 1858-1867.
30. Feng J, Chang H, Li E, Fan G. 2005. Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. JNeurosci Res 79: 734-746.
31. Feng J, Zhou Y, Campbell SL, Le T, Li E, Sweatt JD, Silva AJ, Fan G. 2010. Dnmt1 and Dnmt3a maintain DNA meth-ylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 13: 423-430.
32. Gage FH. 2000. Mammalian neural stem cells. Science 287: 1433-1438.
33. Gao Z, Ure K, Ding P, Nashaat M, Yuan L, Ma J, Hammer RE, Hsieh J. 2011. The master negative regulator REST/ NRSF controls adult neurogenesis by restraining the neurogenic program in quiescent stem cells. J Neurosci 31: 9772-9786.
34. Garriga-Canut M, Schoenike B, Qazi R, Bergendahl K, Daley TJ, Pfender RM, Morrison JF, Ockuly J, Stafstrom C, Sutula T. 2006. 2-Deoxy-D-glucose reduces epilepsy progression by NRSF-CtBP-dependent metabolic regulation of chromatin structure. Nat Neurosci 9: 1382-1387.
35. Greenway DJ, Street M, Jeffries A, Buckley NJ. 2006. REST maintains a repressive chromatin environment in embryonic hippocampal neural stem cells. Stem Cells 25: 354-363.
36. Grozinger CM, Schreiber SL. 2002. Deacetylase enzymes: Biological functions and the use of small-molecule inhibitors. Chem Biol 9: 3-16.
37. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J, Nieland TJ, Zhou Y, Wang X, Mazitschek R, et al. 2009. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459: 55-60.
38. Guillemot F. 2005. Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol 17: 639-647.
39. Guo JU, Ma DK, Mo H, Ball MP, Jang MH, Bonaguidi MA, Balazer JA, Eaves HL, Xie B, Ford E, et al. 2011a.Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat Neurosci 14: 1345-1351.
40. Guo JU, Su Y, Zhong C, Ming GL, Song H. 2011b. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145: 423-434.
41. Guo W, Allan AM, Zong R, Zhang L, Johnson EB, Schaller EG, Murthy AC, Goggin SL, Eisch AJ, Oostra BA, et al. 2011c. Ablation of Fmrp in adult neural stem cells disrupts hippocampus-dependent learning. Nat Med 17: 559-565.
42. Guo W, Murthy AC, Zhang L, Johnson EB, Schaller EG, Allan AM, Zhao X. 2012. Inhibition of GSK3b improves hippocampus-dependent learning and rescues neurogenesis in a mouse model of fragile X syndrome. Hum Mol Genet 21: 681-691.
43. Guo W, Polich ED, Juan Su J, Gao Y, Christopher DM, Allan AM, Wang M, Wang F, Wang G, Zhao X. 2015. Fragile X proteins FMRP and FXR2P control synaptic GluA1 expression and neuronal maturation via distinct mechanisms. Cell Rep 11: 1651-1666.
44. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. 2001. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27: 322-326.
45. Haberland M, Carrer M, Mokalled MH, Montgomery RL, Olson EN. 2010. Redundant control of adipogenesis by histone deacetylases 1 and 2. J Biol Chem 285: 14663-14670.
46. Hao Y, Creson T, Zhang L, Li P, Du F, Yuan P, Gould T, Manji H, Chen G. 2004. Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. J Neurosci 24: 6590-6599.
47. Harikrishnan KN, Chow MZ, Baker EK, Pal S, Bassal S, Brasacchio D, Wang L, Craig JM, Jones PL, Sif S, et al. 2005. Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing. Nat Genet 37: 254-264.
48. Hodge RD, Kahoud RJ, Hevner RF. 2012. Transcriptional control of glutamatergic differentiation during adult neurogenesis. Cell Mol Life Sci 69: 2125-2134.
49. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, Ge K. 2007. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci 104: 18439-18444.
50. Hsieh J. 2012. Orchestrating transcriptional control of adult neurogenesis. Genes Dev 26: 1010-1021.
51. Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH. 2004. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci 101: 16659-16664.
52. Issaeva I, Zonis Y, Rozovskaia T, Orlovsky K, Croce CM, Nakamura T, Mazo A, Eisenbach L, Canaani E. 2007. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol Cell Biol 27: 1889-1903.
53. Jaenisch R, Bird A. 2003. Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nat Genet 33: 245-254.
54. Jawerka M, Colak D, Dimou L, Spiller C, Lagger S, Montgomery RL, Olson EN, Wurst W, Gottlicher M, Gotz M. 2010. The specific role of histone deacetylase 2 in adult neurogenesis. Neuron Glia Biol 6: 93-107.
55. Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293: 1074-1080.
56. Jepsen K, Hermanson O, Onami TM, Gleiberman AS, Lunyak V, McEvilly RJ, Kurokawa R, Kumar V, Liu F, Seto E, et al. 2000. Combinatorial roles of the nuclear receptor corepressor in transcription and development. Cell 102: 753-763.
57. Jiang Y, Hsieh J. 2014. HDAC3 controls gap 2/mitosis progression in adult neural stem/progenitor cells by regulating CDK1 levels. Proc Natl Acad Sci 111: 13541-13546.
58. Jobe EM, McQuate AL, Zhao X. 2012. Crosstalk among epigenetic pathways regulates neurogenesis. Front Neurosci 6: 59.
59. Jung BP, Jugloff DG, Zhang G, Logan R, Brown S, Eubanks JH. 2003. The expression of methyl CpG binding factor MeCP2 correlates with cellular differentiation in the developing rat brain and in cultured cells. J Neurobiol 55: 86-96.
60. Kato Z, Morimoto W, Kimura T, Matsushima A, Kondo N. 2010. Interstitial deletion of 18q: Comparative genomic hybridization array analysis of 46, XX, del(18) (q21.2.q21.33). Birth Defects Res A Clin Mol Teratol 88: 132-135.
61. Kim JE, O’Sullivan ML, Sanchez CA, Hwang M, Israel MA, Brennand K, Deerinck TJ, Goldstein LS, Gage FH, Ellisman MH, et al. 2011. Investigating synapse formation and function using human pluripotent stem cell-derived neurons. Proc Natl Acad Sci 108: 3005-3010.
62. Knuckles P, Vogt MA, Lugert S, Milo M, Chong MM, Hautbergue GM, Wilson SA, Littman DR, Taylor V. 2012. Drosha regulates neurogenesis by controlling neurogenin 2 expression independent of microRNAs. Nat Neurosci 15: 962-969.
63. Koh KP, Rao A. 2013. DNA methylation and methylcytosine oxidation in cell fate decisions. Curr Opin Cell Biol 25: 152-161.
64. Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11: 597-610.
65. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, et al. 2006. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
66. Lessard J, Wu JI, Ranish JA, Wan M, Winslow MM, Staahl BT, Wu H, Aebersold R, Graef IA, Crabtree GR. 2007. An essential switch in subunit composition of a chromatin remodeling complex during neural development.Neuron 55: 201-215.
67. Levenson JM, Roth TL, Lubin FD, Miller CA, Huang IC, Desai P, Malone LM, Sweatt JD. 2006. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 281: 15763-15773.
68. Li X, Zhao X. 2008. Epigenetic regulation of mammalian stem cells. Stem Cells Dev 17: 1043-1052.
69. Li H, Yamagata T, Mori M, Yasuhara A, Momoi MY. 2005. Mutation analysis of methyl-CpG binding protein family genes in autistic patients. Brain Dev 27: 321-325.
70. Li X, Barkho B, Luo Y, Smrt R, Santistevan N, Liu C, Kuwabara T, Gage F, 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.
71. Lim DA, Huang YC, Swigut T, Mirick AL, Garcia-Verdugo JM, Wysocka J, Ernst P, Alvarez-Buylla A. 2009. Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458: 529-533.
72. Liu C, Teng ZQ, Santistevan NJ, Szulwach KE, Guo W, Jin P, Zhao X. 2010. Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell 6: 433-444.
73. Liu XS, Chopp M, Zhang RL, Tao T, Wang XL, Kassis H, Hozeska-Solgot A, Zhang L, Chen C, Zhang ZG. 2011. MicroRNA profiling in subventricular zone after stroke: MiR-124a regulates proliferation of neural progenitor cells through Notch signaling pathway. PLoS ONE 6: e23461.
74. Liu C, Teng ZQ, McQuate AL, Jobe EM, Christ CC, von Hoyningen-Huene SJ, Reyes MD, Polich ED, Xing Y, Li Y, et al. 2013. An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation. PLoS ONE 8: e51436.
75. Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein JL. 2007. Dlx-dependent and-independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27: 3230-3243.
76. Luger K, Richmond TJ. 1998. The histone tails of the nucleosome. Curr Opin Genet Dev 8: 140-146.
77. Luo Y, Shan G, Guo W, Smrt RD, Johnson EB, Li X, Pfeiffer RL, Szulwach KE, Duan R, Barkho BZ, et al. 2010. Fragile X mental retardation protein regulates proliferation and differentiation of adult neural stem/progenitor cells. PLoS Genet 6: e1000898.
78. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N, Flavell RA, Lu B, Ming GL, Song H. 2009. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323: 1074-1077.
79. MacDonald JL, Roskams AJ. 2008. Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Dev Dyn 237: 2256-2267.
80. Makeyev E, Zhang J, Carrasco M, Maniatis T. 2007. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27: 435-448.
81. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, Chen G, Gage FH, Muotri AR. 2010. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143: 527-539.
82. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. 2008. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci 105: 716-721.
83. Ming GL, Song H. 2005. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223-250.
84. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schubeler D. 2008. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30: 755-766.
85. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. 2003. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425: 962-967.
86. Montgomery RL, Hsieh J, Barbosa AC, Richardson JA, Olson EN. 2009. Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci 106: 7876-7881.
87. Mosammaparast N, Shi Y. 2010. Reversal of histone methylation: Biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79: 155-179.
88. Namihira M, Nakashima K, Taga T. 2004. Developmental stage dependent regulation of DNA methylation and chromatin modification in an immature astrocyte specific gene promoter. FEBS Lett 572: 184-188.
89. Naruse Y, Aoki T, Kojima T, Mori N. 1999. Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuron-specific target genes. Proc Natl Acad Sci 96: 13691-13696.
90. Neul JL, Fang P, Barrish J, Lane J, Caeg EB, Smith EO, Zoghbi H, Percy A, Glaze DG. 2008. Specific mutations in methyl-CpG-binding protein 2 confer different severity in Rett syndrome. Neurology 70: 1313-1321.
91. Ng SY, Bogu GK, Soh BS, Stanton LW. 2013a. The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. Mol Cell 51: 349-359.
92. Ng SY, Lin L, Soh BS, Stanton LW. 2013b. Long noncoding RNAs in development and disease of the central nervous system. Trends Genet 29: 461-468.
93. Nimura K, Ura K, Kaneda Y. 2010. Histone methyltransferases: Regulation of transcription and contribution to human disease. J Mol Med 88: 1213-1220.
94. Ninkovic J, Steiner-Mezzadri A, Jawerka M, Akinci U, Masserdotti G, Petricca S, Fischer J, von Holst A, Beckers J, Lie CD, et al. 2013. The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic crossregulatory transcriptional network. Cell Stem Cell 13: 403-418.
95. Novina CD, Sharp PA. 2004. The RNAi revolution. Nature 430: 161-164.
96. Ooi SK, O’Donnell AH, Bestor TH. 2009. Mammalian cytosine methylation at a glance. J Cell Sci 122: 2787-2791.
97. Ouchi Y, Banno Y, Shimizu Y, Ando S, Hasegawa H, Adachi K, Iwamoto T. 2013. Reduced adult hippocampal neurogenesis and working memory deficits in the Dgcr8-deficient mouse model of 22q11.2 deletion-associated schizophrenia can be rescued by IGF2. J Neurosci 33: 9408-9419.
98. Park CY, Choi YS, McManus MT. 2010. Analysis of micro-RNA knockouts in mice. Hum Mol Genet 19: R169-R175.
99. Pedersen MT, Helin K. 2010. Histone demethylases in development and disease. Trends Cell Biol 20: 662-671.
100. Powell WT, Coulson RL, Crary FK, Wong SS, Ach RA, Tsang P, Alice Yamada N, Yasui DH, Lasalle JM. 2013.A Prader-Willi locus lncRNA cloud modulates diurnal genes and energy expenditure. Hum Mol Genet 22: 4318-4328.
101. Qureshi IA, Mehler MF. 2013. Long non-coding RNAs: Novel targets for nervous system disease diagnosis and therapy. Neurotherapeutics 10: 632-646.
102. Ramos AD, Diaz A, Nellore A, Delgado RN, Park KY, Gonzales-Roybal G, Oldham MC, Song JS, Lim DA. 2013. Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 12: 616-628.
103. Rett A. 1966. On a unusual brain atrophy syndrome in hyperammonemia in childhood. Wien Med Wochenschr 116: 723-726.
104. Ross SE, Greenberg ME, Stiles CD. 2003. Basic helix-loop-helix factors in cortical development. Neuron 39: 13-25.
105. Schneider JW, Gao Z, Li S, Farooqi M, Tang TS, Bezprozvanny I, Frantz DE, Hsieh J. 2008. Small-molecule activation of neuronal cell fate. Nat Chem Biol 4: 408-410.
106. Schoenherr CJ, Anderson DJ. 1995. The neuron-restrictive silencer factor (NRSF): A coordinate repressor of multiple neuron-specific genes. Science 267: 1360-1363.
107. Shen L, Zhang Y. 2013 5-Hydroxymethylcytosine: Generation, fate, and genomic distribution. Curr Opin Cell Biol 25: 289-296.
108. Shi Y, Chichung Lie D, Taupin P, Nakashima K, Ray J, Yu RT, Gage FH, Evans RM. 2004a. Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427: 78-83.
109. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA. 2004b. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941-953.
110. Smrt R, Eaves-Egenes J, Barkho B, Santistevan N, Zhao C, Aimone J, Gage F, Zhao X. 2007. Mecp2 deficiency leads to delayed maturation and altered gene expression in hippocampal neurons. Neurobiol Dis 27: 77-89.
111. Smrt RD, Szulwach KE, Pfeiffer RL, Li X, Guo W, Pathania M, Teng ZQ, Luo Y, Peng J, Bordey A, et al. 2010. Micro-RNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 28: 1060-1070.
112. Smrt RD, Pfeiffer RL, Zhao X. 2011. Age-dependent expression of MeCP2 in a heterozygous mosaic mouse model. Hum Mol Genet 20: 1834-1843.
113. Sun YM, Greenway DJ, Johnson R, Street M, Belyaev ND, Deuchars J, Bee T, Wilde S, Buckley NJ. 2005. Distinct profiles of REST interactions with its target genes at different stages of neuronal development. Mol Biol Cell 16: 5630-5638.
114. Sun G, Yu RT, Evans RM, Shi Y. 2007. Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc Natl Acad Sci 104: 15282-15287.
115. Sun G, Alzayady K, Stewart R, Ye P, Yang S, Li W, Shi Y. 2010. Histone demethylase LSD1 regulates neural stem cell proliferation. Mol Cell Biol 30: 1997-2005.
116. Szulwach KE, Li X, Smrt RD, Li Y, Luo Y, Lin L, Santistevan NJ, Li W, Zhao X, Jin P. 2010. Cross talk between micro-RNA and epigenetic regulation in adult neurogenesis. J Cell Biol 189: 127-141.
117. Szulwach KE, Li X, Li Y, Song CX, Wu H, Dai Q, Irier H, Upadhyay AK, Gearing M, Levey AI, et al. 2011. 5-hmCmediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 14: 1607-1616.
118. Tabolacci E, Pietrobono R, Moscato U, Oostra BA, Chiurazzi P, Neri G. 2005. Differential epigenetic modifications in the FMR1 gene of the fragile X syndrome after reactivating pharmacological treatments. Eur J Hum Genet 13: 641-648.
119. Tabolacci E, De Pascalis I, Accadia M, Terracciano A, Moscato U, Chiurazzi P, Neri G. 2008. Modest reactivation of the mutant FMR1 gene by valproic acid is accompanied by histone modifications but not DNA demethylation. Pharmacogenet Genomics 18: 738-741.
120. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T. 2001. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1: 749-758.
121. Temple S. 2001. The development of neural stem cells. Nature 414: 112-117.
122. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M. 2007. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445: 214-218.
123. Visvanathan J, Lee S, Lee B, Lee J, Lee S. 2007. The micro-RNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21: 744-749.
124. Wang KC, Chang HY. 2011. Molecular mechanisms of long noncoding RNAs. Mol Cell 43: 904-914.
125. Wang T, Pan Q, Lin L, Szulwach KE, Song CX, He C, Wu H, Warren ST, Jin P, Duan R, et al. 2012. Genome-wide DNA hydroxymethylation changes are associated with neuro-developmental genes in the developing human cerebellum. Hum Mol Genet 21: 5500-5510.
126. Wapinski O, Chang HY. 2011. Long noncoding RNAs and human disease. Trends Cell Biol 21: 354-361.
127. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, et al. 2009. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the b-catenin-TCF interaction. Nat Neurosci 12: 829-838.
128. Yoo AS, Staahl BT, Chen L, Crabtree GR. 2009. MicroRNAmediated switching of chromatin-remodelling complexes in neural development. Nature 460: 642-646.
129. Zhang CL, Zou Y, He W, Gage FH, Evans RM. 2008. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451: 1004-1007.
130. Zhang RR, Cui QY, Murai K, Lim YC, Smith ZD, Jin S, Ye P, Rosa L, Lee YK, Wu HP, et al. 2013. Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 13: 237-245.
131. Zhao X, Ueba T, Christie BR, Barkho B, McConnell MJ, Nakashima K, Lein ES, Eadie BD, Willhoite AR, Muotri A, et al. 2003. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc Natl Acad Sci 100: 6777-6782.
132. Ziats MN, Rennert OM. 2013. Aberrant expression of long noncoding RNAs in autistic brain. J Mol Neurosci 49: 589-593.
133. Zoghbi HY. 2003. Postnatal neurodevelopmental disorders: Meeting at the synapse? Science 302: 826-830.