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Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways

Nature Neuroscience volume 13, pages 1330–1337 (2010)Cite this article

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Abstract

The development and function of neurons require the regulated expression of large numbers of very specific gene sets. Epigenetic modifications of both DNA and histone proteins are now emerging as fundamental mechanisms by which neurons adapt their transcriptional response to developmental and environmental cues. In the nervous system, the mechanisms by which extracellular signals regulate the activity of chromatin-modifying enzymes have just begun to be characterized. In this Review, I discuss how extracellular cues, including synaptic activity and neurotrophic factors, influence epigenetic modifications and regulate the neuronal transcriptional response. I also summarize additional mechanisms that induce chromatin remodeling events by combinatorial assembly of multiprotein complexes on neuronal gene promoters.

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Figure 1: Activity-dependent epigenetic regulation.
Figure 2: Epigenetic regulation by neurotrophins.
Figure 3: Composition of BAF complexes at different stages of neuronal differentiation.

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References

  1. Berger, S.L., Kouzarides, T., Shiekhattar, R. & Shilatifard, A. An operational definition of epigenetics. Genes Dev. 23, 781–783 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Berger, S.L. The complex language of chromatin regulation during transcription. Nature 447, 407–412 (2007).

    Article  CAS  PubMed  Google Scholar 

  3. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693–705 (2007).

    Article  CAS  PubMed  Google Scholar 

  4. Borrelli, E., Nestler, E.J., Allis, C.D. & Sassone-Corsi, P. Decoding the epigenetic language of neuronal plasticity. Neuron 60, 961–974 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Dulac, C. Brain function and chromatin plasticity. Nature 465, 728–735 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Yoo, A.S. & Crabtree, G.R. ATP-dependent chromatin remodeling in neural development. Curr. Opin. Neurobiol. 19, 120–126 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Turner, B.M. Defining an epigenetic code. Nat. Cell Biol. 9, 2–6 (2007).

    Article  CAS  PubMed  Google Scholar 

  8. Cuthbert, G.L. et al. Histone deimination antagonizes arginine methylation. Cell 118, 545–553 (2004).

    Article  CAS  PubMed  Google Scholar 

  9. Wang, Y. et al. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306, 279–283 (2004).

    Article  CAS  PubMed  Google Scholar 

  10. Turner, B.M. Epigenetic responses to environmental change and their evolutionary implications. Phil. Trans. R. Soc. Lond. B 364, 3403–3418 (2009).

    Article  CAS  Google Scholar 

  11. Sterner, D.E. & Berger, S.L. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64, 435–459 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hassan, A.H., Neely, K.E. & Workman, J.L. Histone acetyltransferase complexes stabilize swi/snf binding to promoter nucleosomes. Cell 104, 817–827 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Boeger, H., Griesenbeck, J., Strattan, J.S. & Kornberg, R.D. Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell 11, 1587–1598 (2003).

    Article  CAS  PubMed  Google Scholar 

  14. Reinke, H. & Horz, W. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell 11, 1599–1607 (2003).

    Article  CAS  PubMed  Google Scholar 

  15. Shahbazian, M.D. & Grunstein, M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76, 75–100 (2007).

    Article  CAS  PubMed  Google Scholar 

  16. Goodman, R.H. & Smolik, S. CBP/p300 in cell growth, transformation, and development. Genes Dev. 14, 1553–1577 (2000).

    CAS  PubMed  Google Scholar 

  17. Vo, N. & Goodman, R.H. CREB-binding protein and p300 in transcriptional regulation. J. Biol. Chem. 276, 13505–13508 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Partanen, A., Motoyama, J. & Hui, C.C. Developmentally regulated expression of the transcriptional cofactors/histone acetyltransferases CBP and p300 during mouse embryogenesis. Int. J. Dev. Biol. 43, 487–494 (1999).

    CAS  PubMed  Google Scholar 

  19. Tanaka, Y. et al. Abnormal skeletal patterning in embryos lacking a single Cbp allele: a partial similarity with Rubinstein-Taybi syndrome. Proc. Natl. Acad. Sci. USA 94, 10215–10220 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Petrij, F. et al. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature 376, 348–351 (1995).

    Article  CAS  PubMed  Google Scholar 

  21. Doi, M., Hirayama, J. & Sassone-Corsi, P. Circadian regulator CLOCK is a histone acetyltransferase. Cell 125, 497–508 (2006).

    Article  CAS  PubMed  Google Scholar 

  22. Nakahata, Y., Grimaldi, B., Sahar, S., Hirayama, J. & Sassone-Corsi, P. Signaling to the circadian clock: plasticity by chromatin remodeling. Curr. Opin. Cell Biol. 19, 230–237 (2007).

    Article  CAS  PubMed  Google Scholar 

  23. Nishihara, E. et al. SRC-1 null mice exhibit moderate motor dysfunction and delayed development of cerebellar Purkinje cells. J. Neurosci. 23, 213–222 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gregoretti, I.V., Lee, Y.M. & Goodson, H.V. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338, 17–31 (2004).

    Article  CAS  PubMed  Google Scholar 

  25. Yang, X.J. & Seto, E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9, 206–218 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kazantsev, A.G. & Thompson, L.M. Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat. Rev. Drug Discov. 7, 854–868 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. Haberland, M., Montgomery, R.L. & Olson, E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10, 32–42 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Michan, S. & Sinclair, D. Sirtuins in mammals: insights into their biological function. Biochem. J. 404, 1–13 (2007).

    Article  CAS  PubMed  Google Scholar 

  29. Broide, R.S. et al. Distribution of histone deacetylases 1–11 in the rat brain. J. Mol. Neurosci. 31, 47–58 (2007).

    Article  CAS  PubMed  Google Scholar 

  30. MacDonald, J.L. & Roskams, A.J. Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Dev. Dyn. 237, 2256–2267 (2008).

    Article  PubMed  Google Scholar 

  31. Lagger, G. et al. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J. 21, 2672–2681 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Guan, J.S. et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459, 55–60 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wang, Z. et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138, 1019–1031 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Bernstein, B.E. et al. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. USA 99, 8695–8700 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lonze, B.E. & Ginty, D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605–623 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. Impey, S. et al. Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron 34, 235–244 (2002).

    Article  CAS  PubMed  Google Scholar 

  37. Hardingham, G.E., Chawla, S., Cruzalegui, F.H. & Bading, H. Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron 22, 789–798 (1999).

    Article  CAS  PubMed  Google Scholar 

  38. Merienne, K., Pannetier, S., Harel-Bellan, A. & Sassone-Corsi, P. Mitogen-regulated RSK2-CBP interaction controls their kinase and acetylase activities. Mol. Cell. Biol. 21, 7089–7096 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Liu, Y.Z., Chrivia, J.C. & Latchman, D.S. Nerve growth factor up-regulates the transcriptional activity of CBP through activation of the p42/p44(MAPK) cascade. J. Biol. Chem. 273, 32400–32407 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Liu, Y.Z., Thomas, N.S. & Latchman, D.S. CBP associates with the p42/p44 MAPK enzymes and is phosphorylated following NGF treatment. Neuroreport 10, 1239–1243 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Hu, S.C., Chrivia, J. & Ghosh, A. Regulation of CBP-mediated signatures transcription by neuronal calcium signaling. Neuron 22, 799–808 (1999).

    Article  CAS  PubMed  Google Scholar 

  42. Heintzman, N.D. et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39, 311–318 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854–858 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Kim, T.K. et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182–187 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Riccio, A. et al. A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol. Cell 21, 283–294 (2006).

    Article  CAS  PubMed  Google Scholar 

  46. Nott, A., Watson, P.M., Robinson, J.D., Crepaldi, L. & Riccio, A. S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455, 411–415 (2008).

    Article  CAS  PubMed  Google Scholar 

  47. Chawla, S., Vanhoutte, P., Arnold, F.J., Huang, C.L. & Bading, H. Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J. Neurochem. 85, 151–159 (2003).

    Article  CAS  PubMed  Google Scholar 

  48. Sassone-Corsi, P. et al. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science 285, 886–891 (1999).

    Article  CAS  PubMed  Google Scholar 

  49. Crosio, C., Cermakian, N., Allis, C.D. & Sassone-Corsi, P. Light induces chromatin modification in cells of the mammalian circadian clock. Nat. Neurosci. 3, 1241–1247 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Crosio, C., Heitz, E., Allis, C.D., Borrelli, E. & Sassone-Corsi, P. Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J. Cell Sci. 116, 4905–4914 (2003).

    Article  CAS  PubMed  Google Scholar 

  51. Wittmann, M. et al. Synaptic activity induces dramatic changes in the geometry of the cell nucleus: interplay between nuclear structure, histone H3 phosphorylation, and nuclear calcium signaling. J. Neurosci. 29, 14687–14700 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Segal, R.A. Selectivity in neurotrophin signaling: theme and variations. Annu. Rev. Neurosci. 26, 299–330 (2003).

    Article  CAS  PubMed  Google Scholar 

  53. Nakajima, T. et al. The signal-dependent coactivator CBP is a nuclear target for pp90RSK. Cell 86, 465–474 (1996).

    Article  CAS  PubMed  Google Scholar 

  54. Wong, K. et al. Nerve growth factor receptor signaling induces histone acetyltransferase domain-dependent nuclear translocation of p300/CREB-binding protein-associated factor and hGCN5 acetyltransferases. J. Biol. Chem. 279, 55667–55674 (2004).

    Article  CAS  PubMed  Google Scholar 

  55. Bredt, D.S. & Snyder, S.H. Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron 13, 301–313 (1994).

    Article  CAS  PubMed  Google Scholar 

  56. Contestabile, A. Regulation of transcription factors by nitric oxide in neurons and in neural-derived tumor cells. Prog. Neurobiol. 84, 317–328 (2008).

    Article  CAS  PubMed  Google Scholar 

  57. Shahani, N. & Sawa, A. Nitric oxide signaling and nitrosative stress in neurons: role for S-nitrosylation. Antioxid. Redox Signal. published online, doi:10.1089/ars.2010.3580 (2 September 2010).

  58. Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E. & Stamler, J.S. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150–166 (2005).

    Article  CAS  PubMed  Google Scholar 

  59. Dhakshinamoorthy, S. et al. Protein/DNA arrays identify nitric oxide-regulated cis-element and trans-factor activities some of which govern neuroblastoma cell viability. Nucleic Acids Res. 35, 5439–5451 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Colussi, C. et al. HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc. Natl. Acad. Sci. USA 105, 19183–19187 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Miller, C.A. & Sweatt, J.D. Covalent modification of DNA regulates memory formation. Neuron 53, 857–869 (2007).

    Article  CAS  PubMed  Google Scholar 

  62. Herz, J. & Chen, Y. Reelin, lipoprotein receptors and synaptic plasticity. Nat. Rev. Neurosci. 7, 850–859 (2006).

    Article  CAS  PubMed  Google Scholar 

  63. Wu, H. et al. Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329, 444–448 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Morey, L. & Helin, K. Polycomb group protein-mediated repression of transcription. Trends Biochem. Sci. 35, 323–332 (2010).

    Article  CAS  PubMed  Google Scholar 

  65. Ma, D.K. et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074–1077 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929–930 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Valinluck, V. et al. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res. 32, 4100–4108 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Jones, P.L. et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19, 187–191 (1998).

    Article  CAS  PubMed  Google Scholar 

  69. Bienvenu, T. & Chelly, J. Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat. Rev. Genet. 7, 415–426 (2006).

    Article  CAS  PubMed  Google Scholar 

  70. Chahrour, M. et al. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224–1229 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Chen, W.G. et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302, 885–889 (2003).

    Article  CAS  PubMed  Google Scholar 

  72. Martinowich, K. et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302, 890–893 (2003).

    Article  CAS  PubMed  Google Scholar 

  73. Zhou, Z. et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255–269 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Skene, P.J. et al. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 37, 457–468 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Yasui, D.H. et al. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl. Acad. Sci. USA 104, 19416–19421 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Chong, J.A. et al. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80, 949–957 (1995).

    Article  CAS  PubMed  Google Scholar 

  77. Schoenherr, C.J. & Anderson, D.J. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267, 1360–1363 (1995).

    Article  CAS  PubMed  Google Scholar 

  78. Ooi, L. & Wood, I.C. Chromatin crosstalk in development and disease: lessons from REST. Nat. Rev. Genet. 8, 544–554 (2007).

    Article  CAS  PubMed  Google Scholar 

  79. Ballas, N. & Mandel, G. The many faces of REST oversee epigenetic programming of neuronal genes. Curr. Opin. Neurobiol. 15, 500–506 (2005).

    Article  CAS  PubMed  Google Scholar 

  80. Chen, Z.F., Paquette, A.J. & Anderson, D.J. NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nat. Genet. 20, 136–142 (1998).

    Article  CAS  PubMed  Google Scholar 

  81. Battaglioli, E. et al. REST repression of neuronal genes requires components of the hSWI.SNF complex. J. Biol. Chem. 277, 41038–41045 (2002).

    Article  CAS  PubMed  Google Scholar 

  82. Shi, Y. et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941–953 (2004).

    Article  CAS  PubMed  Google Scholar 

  83. Shi, Y. et al. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422, 735–738 (2003).

    Article  CAS  PubMed  Google Scholar 

  84. Garriga-Canut, M. et al. 2-Deoxy-D-glucose reduces epilepsy progression by NRSF-CtBP-dependent metabolic regulation of chromatin structure. Nat. Neurosci. 9, 1382–1387 (2006).

    Article  CAS  PubMed  Google Scholar 

  85. Ballas, N., Grunseich, C., Lu, D.D., Speh, J.C. & Mandel, G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121, 645–657 (2005).

    Article  CAS  PubMed  Google Scholar 

  86. Yeo, M. et al. Small CTD phosphatases function in silencing neuronal gene expression. Science 307, 596–600 (2005).

    Article  CAS  PubMed  Google Scholar 

  87. Lunyak, V.V. et al. Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science 298, 1747–1752 (2002).

    Article  CAS  PubMed  Google Scholar 

  88. Bai, S. et al. DNA methyltransferase 3b regulates nerve growth factor-induced differentiation of PC12 cells by recruiting histone deacetylase 2. Mol. Cell. Biol. 25, 751–766 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Bowman, G.D. Mechanisms of ATP-dependent nucleosome sliding. Curr. Opin. Struct. Biol. 20, 73–81 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Muchardt, C. & Yaniv, M. ATP-dependent chromatin remodelling: SWI/SNF and Co. are on the job. J. Mol. Biol. 293, 187–198 (1999).

    Article  CAS  PubMed  Google Scholar 

  91. Wu, J.I., Lessard, J. & Crabtree, G.R. Understanding the words of chromatin regulation. Cell 136, 200–206 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Ho, L. & Crabtree, G.R. Chromatin remodelling during development. Nature 463, 474–484 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Bultman, S. et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287–1295 (2000).

    Article  CAS  PubMed  Google Scholar 

  94. Lessard, J. et al. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201–215 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Wu, J.I. et al. Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56, 94–108 (2007).

    Article  CAS  PubMed  Google Scholar 

  96. Qiu, Z. & Ghosh, A. A calcium-dependent switch in a CREST-BRG1 complex regulates activity-dependent gene expression. Neuron 60, 775–787 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Brandl, A., Heinzel, T. & Kramer, O.H. Histone deacetylases: salesmen and customers in the post-translational modification market. Biol. Cell 101, 193–205 (2009).

    Article  CAS  PubMed  Google Scholar 

  98. Hait, N.C. et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325, 1254–1257 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Fraser, P. & Bickmore, W. Nuclear organization of the genome and the potential for gene regulation. Nature 447, 413–417 (2007).

    Article  CAS  PubMed  Google Scholar 

  100. Manuelidis, L. Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences. Proc. Natl. Acad. Sci. USA 81, 3123–3127 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The author is grateful to L. Crepaldi and A. Nott for reading the manuscript. A.R. is the recipient of an MRC Senior Non Clinical Fellowship.

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  1. Medical Research Council Laboratory for Molecular and Cell Biology and Department of Neuroscience, Physiology and Pharmacology, University College London, London, UK

    Antonella Riccio

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Riccio, A. Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways. Nat Neurosci 13, 1330–1337 (2010). https://doi.org/10.1038/nn.2671

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