Role of BDNF epigenetics in activity-dependent neuronal plasticity

Neuropharmacology

Volumn 76, Issue PART C, 2014, Pages 709-718

  Karpova, Nina N ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

BDNF exons; BDNF promoter; DNA methylation; Epigenetics; Histone modifications; MicroRNAs; Neuronal activity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DNA BINDING PROTEIN; MESSENGER RNA; MICRORNA;

3' UNTRANSLATED REGION; BDNF GENE; DNA METHYLATION; DRUG TARGETING; EPIGENETICS; EXON; GENE EXPRESSION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; MENTAL DISEASE; NERVE CELL PLASTICITY; NEUROLOGIC DISEASE; NEUROPSYCHIATRIC DISORDER; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA TRANSPORT;

BDNF EXONS; BDNF PROMOTER; DNA METHYLATION; EPIGENETICS; HISTONE MODIFICATIONS; MICRORNAS; NEURONAL ACTIVITY;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DNA METHYLATION; EPIGENESIS, GENETIC; MICRORNAS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; RNA, MESSENGER; SYNAPSES;

EID: 84890441146     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.04.002     Document Type: Review

References (125)

1. I. Abidin, T. Kohler, E. Weiler, G. Zoidl, U.T. Eysel, V. Lessmann, and T. Mittmann Reduced presynaptic efficiency of excitatory synaptic transmission impairs LTP in the visual cortex of BDNF-heterozygous mice Eur. J. Neurosci. 24 2006 3519 3531
2. I. Abidin, U.T. Eysel, V. Lessmann, and T. Mittmann Impaired GABAergic inhibition in the visual cortex of brain-derived neurotrophic factor heterozygous knockout mice J. Physiol. 586 2008 1885 1901
3. L. Abuhatzira, K. Makedonski, Y. Kaufman, A. Razin, and R. Shemer MeCP2 deficiency in the brain decreases BDNF levels by REST/CoREST-mediated repression and increases TRKB production Epigenetics 2 2007 214 222
4. T. Aid, A. Kazantseva, M. Piirsoo, K. Palm, and T. Timmusk Mouse and rat BDNF gene structure and expression revisited J. Neurosci. Res. 85 2007 525 535
5. J.M. Alarcon, G. Malleret, K. Touzani, S. Vronskaya, S. Ishii, E.R. Kandel, and A. Barco Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration Neuron 42 2004 947 959
6. R.E. Amir, I.B. Van den Veyver, M. Wan, C.Q. Tran, U. Francke, and H.Y. Zoghbi Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2 Nat. Genet. 23 1999 185 188
7. J.J. An, K. Gharami, G.Y. Liao, N.H. Woo, A.G. Lau, F. Vanevski, E.R. Torre, K.R. Jones, Y. Feng, B. Lu, and B. Xu Distinct role of long 3′ UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons Cell 134 2008 175 187
8. A.E. Autry, and L.M. Monteggia Brain-derived neurotrophic factor and neuropsychiatric disorders Pharmacol. Rev. 64 2012 238 258
9. N. Ballas, D.T. Lioy, C. Grunseich, and G. Mandel Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology Nat. Neurosci. 12 2009 311 317
10. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
11. S.K. Bhattacharya, S. Ramchandani, N. Cervoni, and M. Szyf A mammalian protein with specific demethylase activity for mCpG DNA Nature 397 1999 579 583
12. A. Bird DNA methylation patterns and epigenetic memory Genes Dev. 16 2002 6 21
13. A. Bird Perceptions of epigenetics Nature 447 2007 396 398
14. A. Bird, M. Taggart, M. Frommer, O.J. Miller, and D. Macleod A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA Cell 40 1985 91 99
15. F. Boulle, D.L. van den Hove, S.B. Jakob, B.P. Rutten, M. Hamon, J. van Os, K.P. Lesch, L. Lanfumey, H.W. Steinbusch, and G. Kenis Epigenetic regulation of the BDNF gene: implications for psychiatric disorders Mol. Psychiatry 17 2012 584 596
16. C.R. Bramham, and D.G. Wells Dendritic mRNA: transport, translation and function Nat. Rev. Neurosci. 8 2007 776 789
17. T.W. Bredy, and M. Barad The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear Learn. Mem. 15 2008 39 45
18. T.W. Bredy, H. Wu, C. Crego, J. Zellhoefer, Y.E. Sun, and M. Barad Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear Learn. Mem. 14 2007 268 276
19. A.W. Bruce, I.J. Donaldson, I.C. Wood, S.A. Yerbury, M.I. Sadowski, M. Chapman, B. Gottgens, and N.J. Buckley Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes Proc. Natl. Acad. Sci. U. S. A. 101 2004 10458 10463
20. V. Caputo, L. Sinibaldi, A. Fiorentino, C. Parisi, C. Catalanotto, A. Pasini, C. Cogoni, and A. Pizzuti Brain derived neurotrophic factor (BDNF) expression is regulated by microRNAs miR-26a and miR-26b allele-specific binding PLoS One 6 2011 e28656
21. J. Chang, B. Zhang, H. Heath, N. Galjart, X. Wang, and J. Milbrandt Nicotinamide adenine dinucleotide (NAD)-regulated DNA methylation alters CCCTC-binding factor (CTCF)/cohesin binding and transcription at the BDNF locus Proc. Natl. Acad. Sci. U. S. A. 107 2010 21836 21841
22. Q. Chang, G. Khare, V. Dani, S. Nelson, and R. Jaenisch The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression Neuron 49 2006 341 348
23. K.A. Chase, and R.P. Sharma Nicotine induces chromatin remodelling through decreases in the methyltransferases GLP, G9a, Setdb1 and levels of H3K9me2 Int. J. Neuropsychopharmacol. 2012 1 10
24. R.Z. Chen, S. Akbarian, M. Tudor, and R. Jaenisch Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice Nat. Genet. 27 2001 327 331
25. W.G. Chen, Q. Chang, Y. Lin, A. Meissner, A.E. West, E.C. Griffith, R. Jaenisch, and M.E. Greenberg Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2 Science 302 2003 885 889
26. Z.Y. Chen, A. Ieraci, H. Teng, H. Dall, C.X. Meng, D.G. Herrera, A. Nykjaer, B.L. Hempstead, and F.S. Lee Sortilin controls intracellular sorting of brain-derived neurotrophic factor to the regulated secretory pathway J. Neurosci. 25 2005 6156 6166
27. Z.Y. Chen, D. Jing, K.G. Bath, A. Ieraci, T. Khan, C.J. Siao, D.G. Herrera, M. Toth, C. Yang, and B.S. McEwen Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior Science 314 2006 140 143
28. C. Chiaruttini, M. Sonego, G. Baj, M. Simonato, and E. Tongiorgi BDNF mRNA splice variants display activity-dependent targeting to distinct hippocampal laminae Mol. Cell. Neurosci. 37 2008 11 19
29. C. Chiaruttini, A. Vicario, Z. Li, G. Baj, P. Braiuca, Y. Wu, F.S. Lee, L. Gardossi, J.M. Baraban, and E. Tongiorgi Dendritic trafficking of BDNF mRNA is mediated by translin and blocked by the G196A (Val66Met) mutation Proc. Natl. Acad. Sci. U. S. A. 106 2009 16481 16486
30. P.J. Conn, C.W. Lindsley, and C.K. Jones Activation of metabotropic glutamate receptors as a novel approach for the treatment of schizophrenia Trends Pharmacol. Sci. 30 2009 25 31
31. H.E. Covington 3rd, I. Maze, H. Sun, H.M. Bomze, K.D. DeMaio, E.Y. Wu, D.M. Dietz, M.K. Lobo, S. Ghose, and E. Mouzon A role for repressive histone methylation in cocaine-induced vulnerability to stress Neuron 71 2011 656 670
32. V.S. Dani, Q. Chang, A. Maffei, G.G. Turrigiano, R. Jaenisch, and S.B. Nelson Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome Proc. Natl. Acad. Sci. U. S. A. 102 2005 12560 12565
33. S. Diaz de Leon-Guerrero, G. Pedraza-Alva, and L. Perez-Martinez In sickness and in health: the role of methyl-CpG binding protein 2 in the central nervous system Eur. J. Neurosci. 33 2011 1563 1574
34. D. Dorsett Cohesin, gene expression and development: lessons from Drosophila Chromosome Res. 17 2009 185 200
35. K.I. Erickson, D.L. Miller, and K.A. Roecklein The aging hippocampus: interactions between exercise, depression, and BDNF Neuroscientist 18 2012 82 97
36. H. Frielingsdorf, K.G. Bath, F. Soliman, J. Difede, B.J. Casey, and F.S. Lee Variant brain-derived neurotrophic factor Val66Met endophenotypes: implications for posttraumatic stress disorder Ann. N. Y. Acad. Sci. 1208 2012 150 157
37. M. Fuchikami, S. Morinobu, M. Segawa, Y. Okamoto, S. Yamawaki, N. Ozaki, T. Inoue, I. Kusumi, T. Koyama, K. Tsuchiyama, and T. Terao DNA methylation profiles of the brain-derived neurotrophic factor (BDNF) gene as a potent diagnostic biomarker in major depression PLoS One 6 2011 e23881
38. D.P. Gavin, R.P. Sharma, K.A. Chase, F. Matrisciano, E. Dong, and A. Guidotti Growth arrest and DNA-damage-inducible, beta (GADD45b)-mediated DNA demethylation in major psychosis Neuropsychopharmacology 37 2012 531 542
39. J.C. Gewirtz, and G.J. Marek Behavioral evidence for interactions between a hallucinogenic drug and group II metabotropic glutamate receptors Neuropsychopharmacology 23 2000 569 576
40. F. Gomez-Pinilla, Y. Zhuang, J. Feng, Z. Ying, and G. Fan Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation Eur. J. Neurosci. 33 2011 383 390
41. M.M. Gonzalez, and G. Aston-Jones Light deprivation damages monoamine neurons and produces a depressive behavioral phenotype in rats Proc. Natl. Acad. Sci. U. S. A. 105 2008 4898 4903
42. J.U. Guo, Y. Su, C. Zhong, G.L. Ming, and H. Song Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain Cell 145 2011 423 434
43. S. Gupta-Agarwal, A.V. Franklin, T. Deramus, M. Wheelock, R.L. Davis, L.L. McMahon, and F.D. Lubin G9a/GLP histone lysine dimethyltransferase complex activity in the hippocampus and the entorhinal cortex is required for gene activation and silencing during memory consolidation J. Neurosci. 32 2012 5440 5453
44. S. Gupta, S.Y. Kim, S. Artis, D.L. Molfese, A. Schumacher, J.D. Sweatt, R.E. Paylor, and F.D. Lubin Histone methylation regulates memory formation J. Neurosci. 30 2010 3589 3599
45. J. Guy, B. Hendrich, M. Holmes, J.E. Martin, and A. Bird A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome Nat. Genet. 27 2001 322 326
46. B. Hagberg, J. Aicardi, K. Dias, and O. Ramos A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: report of 35 cases Ann. Neurol. 14 1983 471 479
47. J. Hall, K.L. Thomas, and B.J. Everitt Rapid and selective induction of BDNF expression in the hippocampus during contextual learning Nat. Neurosci. 3 2000 533 535
48. D. Hara, M. Fukuchi, T. Miyashita, A. Tabuchi, I. Takasaki, Y. Naruse, N. Mori, T. Kondo, and M. Tsuda Remote control of activity-dependent BDNF gene promoter-I transcription mediated by REST/NRSF Biochem. Biophys. Res. Commun. 384 2009 506 511
49. I. Heo, and V.N. Kim Regulating the regulators: posttranslational modifications of RNA silencing factors Cell 139 2009 28 31
50. E.J. Hong, A.E. McCord, and M.E. Greenberg A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition Neuron 60 2008 610 624
51. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080
52. K.R. Jones, I. Farinas, C. Backus, and L.F. Reichardt Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development Cell 76 1994 989 999
53. N.N. Karpova, T. Rantamaki, A. Di Lieto, L. Lindemann, M.C. Hoener, and E. Castren Darkness reduces BDNF expression in the visual cortex and induces repressive chromatin remodeling at the BDNF gene in both hippocampus and visual cortex Cell. Mol. Neurobiol. 30 2010 1117 1123
54. S. Keller, M. Sarchiapone, F. Zarrilli, A. Videtic, A. Ferraro, V. Carli, S. Sacchetti, F. Lembo, A. Angiolillo, and N. Jovanovic Increased BDNF promoter methylation in the Wernicke area of suicide subjects Arch. Gen. Psychiatry 67 2010 258 267
55. N. Kishi, and J.D. Macklis MECP2 is progressively expressed in post-migratory neurons and is involved in neuronal maturation rather than cell fate decisions Mol. Cell. Neurosci. 27 2004 306 321
56. R.J. Klose, and A.P. Bird Genomic DNA methylation: the mark and its mediators Trends Biochem. Sci. 31 2006 89 97
57. W. Konopka, A. Kiryk, M. Novak, M. Herwerth, J.R. Parkitna, M. Wawrzyniak, A. Kowarsch, P. Michaluk, J. Dzwonek, and T. Arnsperger MicroRNA loss enhances learning and memory in mice J. Neurosci. 30 2010 14835 14842
58. T. Kouzarides Chromatin modifications and their function Cell 128 2007 693 705
59. V. Krishnan, M.H. Han, D.L. Graham, O. Berton, W. Renthal, S.J. Russo, Q. Laplant, A. Graham, M. Lutter, and D.C. Lagace Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions Cell 131 2007 391 404
60. A. Kumar, K.H. Choi, W. Renthal, N.M. Tsankova, D.E. Theobald, H.T. Truong, S.J. Russo, Q. Laplant, T.S. Sasaki, and K.N. Whistler Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum Neuron 48 2005 303 314
61. N. Kuzumaki, D. Ikegami, R. Tamura, N. Hareyama, S. Imai, M. Narita, K. Torigoe, K. Niikura, H. Takeshima, and T. Ando Hippocampal epigenetic modification at the brain-derived neurotrophic factor gene induced by an enriched environment Hippocampus 21 2011 127 132
62. J.L. Larimore, C.A. Chapleau, S. Kudo, A. Theibert, A.K. Percy, and L. Pozzo-Miller Bdnf overexpression in hippocampal neurons prevents dendritic atrophy caused by Rett-associated MECP2 mutations Neurobiol. Dis. 34 2009 199 211
63. A.G. Lau, H.A. Irier, J. Gu, D. Tian, L. Ku, G. Liu, M. Xia, B. Fritsch, J.Q. Zheng, and R. Dingledine Distinct 3'UTRs differentially regulate activity-dependent translation of brain-derived neurotrophic factor (BDNF) Proc. Natl. Acad. Sci. U. S. A. 107 2010 15945 15950
64. K.K. Lee, and J.L. Workman Histone acetyltransferase complexes: one size doesn't fit all Nat. Rev. Mol. Cell. Biol. 8 2007 284 295
65. S.T. Lee, K. Chu, K.H. Jung, J.H. Kim, J.Y. Huh, H. Yoon, D.K. Park, J.Y. Lim, J.M. Kim, and D. Jeon miR-206 regulates brain-derived neurotrophic factor in Alzheimer disease model Ann. Neurol. 72 2012 269 277
66. J.M. Levenson, T.L. Roth, F.D. Lubin, C.A. Miller, I.C. Huang, P. Desai, L.M. Malone, and J.D. Sweatt Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus J. Biol. Chem. 281 2006 15763 15773
67. B. Li, M. Carey, and J.L. Workman The role of chromatin during transcription Cell 128 2007 707 719
68. H. Li, X. Zhong, K.F. Chau, E.C. Williams, and Q. Chang Loss of activity-induced phosphorylation of MeCP2 enhances synaptogenesis, LTP and spatial memory Nat. Neurosci. 14 2011 1001 1008
69. G.Y. Liao, J.J. An, K. Gharami, E.G. Waterhouse, F. Vanevski, K.R. Jones, and B. Xu Dendritically targeted Bdnf mRNA is essential for energy balance and response to leptin Nat. Med. 18 2012 564 571
70. R. Lister, and J.R. Ecker Finding the fifth base: genome-wide sequencing of cytosine methylation Genome Res. 19 2009 959 966
71. Q.R. Liu, D. Walther, T. Drgon, O. Polesskaya, T.G. Lesnick, K.J. Strain, M. de Andrade, J.H. Bower, D.M. Maraganore, and G.R. Uhl Human brain derived neurotrophic factor (BDNF) genes, splicing patterns, and assessments of associations with substance abuse and Parkinson's Disease Am. J. Med. Genet. B Neuropsychiatr. Genet. 134B 2005 93 103
72. F.D. Lubin, T.L. Roth, and J.D. Sweatt Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory J. Neurosci. 28 2008 10576 10586
73. S. Luikenhuis, E. Giacometti, C.F. Beard, and R. Jaenisch Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice Proc. Natl. Acad. Sci. U. S. A. 101 2004 6033 6038
74. B. Ma, B.P. Culver, G. Baj, E. Tongiorgi, M.V. Chao, and N. Tanese Localization of BDNF mRNA with the Huntington's disease protein in rat brain Mol. Neurodegener. 5 2010 22
75. D.K. Ma, M.H. Jang, J.U. Guo, Y. Kitabatake, M.L. Chang, N. Pow-Anpongkul, R.A. Flavell, B. Lu, G.L. Ming, and H. Song Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis Science 323 2009 1074 1077
76. I. Maezawa, S. Swanberg, D. Harvey, J.M. LaSalle, and L.W. Jin Rett syndrome astrocytes are abnormal and spread MeCP2 deficiency through gap junctions J. Neurosci. 29 2009 5051 5061
77. A.L. Mahan, and K.J. Ressler Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder Trends Neurosci. 35 2012 24 35
78. K. Martinowich, D. Hattori, H. Wu, S. Fouse, F. He, Y. Hu, G. Fan, and Y.E. Sun DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation Science 302 2003 890 893
79. F. Matrisciano, E. Dong, D.P. Gavin, F. Nicoletti, and A. Guidotti Activation of group II metabotropic glutamate receptors promotes DNA demethylation in the mouse brain Mol. Pharmacol. 80 2011 174 182
80. J.F. Maya Vetencourt, E. Tiraboschi, M. Spolidoro, E. Castren, and L. Maffei Serotonin triggers a transient epigenetic mechanism that reinstates adult visual cortex plasticity in rats Eur. J. Neurosci. 33 2011 49 57
81. I. Maze, H.E. Covington 3rd, D.M. Dietz, Q. LaPlant, W. Renthal, S.J. Russo, M. Mechanic, E. Mouzon, R.L. Neve, and S.J. Haggarty Essential role of the histone methyltransferase G9a in cocaine-induced plasticity Science 327 2010 213 216
82. P. Miura, A. Amirouche, C. Clow, G. Belanger, and B.J. Jasmin Brain-derived neurotrophic factor expression is repressed during myogenic differentiation by miR-206 J. Neurochem. 120 2012 230 238
83. P. Moretti, and H.Y. Zoghbi MeCP2 dysfunction in Rett syndrome and related disorders Curr. Opin. Genet. Dev. 16 2006 276 281
84. X. Nan, F.J. Campoy, and A. Bird MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin Cell 88 1997 471 481
85. E.D. Nelson, E.T. Kavalali, and L.M. Monteggia Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation J. Neurosci. 28 2008 395 406
86. H.H. Ng, P. Jeppesen, and A. Bird Active repression of methylated genes by the chromosomal protein MBD1 Mol. Cell. Biol. 20 2000 1394 1406
87. H.H. Ng, Y. Zhang, B. Hendrich, C.A. Johnson, B.M. Turner, H. Erdjument-Bromage, P. Tempst, D. Reinberg, and A. Bird MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex Nat. Genet. 23 1999 58 61
88. S. Oe, and Y. Yoneda Cytoplasmic polyadenylation element-like sequences are involved in dendritic targeting of BDNF mRNA in hippocampal neurons FEBS Lett. 584 2010 3424 3430
89. N. Onishchenko, N. Karpova, F. Sabri, E. Castren, and S. Ceccatelli Long-lasting depression-like behavior and epigenetic changes of BDNF gene expression induced by perinatal exposure to methylmercury J. Neurochem. 106 2008 1378 1387
90. B. Papp, and J. Muller Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins Genes Dev. 20 2006 2041 2054
91. A. Prokhortchouk, B. Hendrich, H. Jorgensen, A. Ruzov, M. Wilm, G. Georgiev, A. Bird, and E. Prokhortchouk The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor Genes Dev. 15 2001 1613 1618
92. P. Pruunsild, A. Kazantseva, T. Aid, K. Palm, and T. Timmusk Dissecting the human BDNF locus: bidirectional transcription, complex splicing, and multiple promoters Genomics 90 2007 397 406
93. P. Pruunsild, M. Sepp, E. Orav, I. Koppel, and T. Timmusk Identification of cis-elements and transcription factors regulating neuronal activity-dependent transcription of human BDNF gene J. Neurosci. 31 2011 3295 3308
94. S.M. Reamon-Buettner, and J. Borlak A new paradigm in toxicology and teratology: altering gene activity in the absence of DNA sequence variation Reprod. Toxicol. 24 2007 20 30
95. K.D. Robertson, and A.P. Wolffe DNA methylation in health and disease Nat. Rev. Genet. 1 2000 11 19
96. T.L. Roth, and J.D. Sweatt Epigenetic marking of the BDNF gene by early-life adverse experiences Horm. Behav. 59 2010 315 320
97. T.L. Roth, P.R. Zoladz, J.D. Sweatt, and D.M. Diamond Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder J. Psychiatr. Res. 45 2011 919 926
98. G. Sadri-Vakili, V. Kumaresan, H.D. Schmidt, K.R. Famous, P. Chawla, F.M. Vassoler, R.P. Overland, E. Xia, C.E. Bass, and E.F. Terwilliger Cocaine-induced chromatin remodeling increases brain-derived neurotrophic factor transcription in the rat medial prefrontal cortex, which alters the reinforcing efficacy of cocaine J. Neurosci. 30 2010 11735 11744
99. A.J. Sales, C. Biojone, M.S. Terceti, F.S. Guimaraes, M.V. Gomes, and S.R. Joca Antidepressant-like effect induced by systemic and intra-hippocampal administration of DNA methylation inhibitors Br. J. Pharmacol. 164 2011 1711 1721
100. F. Santos, A.H. Peters, A.P. Otte, W. Reik, and W. Dean Dynamic chromatin modifications characterise the first cell cycle in mouse embryos Dev. Biol. 280 2005 225 236
101. H.D. Schmidt, G.R. Sangrey, S.B. Darnell, R.L. Schassburger, J.H. Cha, R.C. Pierce, and G. Sadri-Vakili Increased brain-derived neurotrophic factor, BDNF expression in the ventral tegmental area during cocaine abstinence is associated with increased histone acetylation at BDNF exon I-containing promoters J. Neurochem. 120 2012 202 209
102. B. Schuettengruber, D. Chourrout, M. Vervoort, B. Leblanc, and G. Cavalli Genome regulation by polycomb and trithorax proteins Cell 128 2007 735 745
103. P.M. Schwartz, P.R. Borghesani, R.L. Levy, S.L. Pomeroy, and R.A. Segal Abnormal cerebellar development and foliation in BDNF-/- mice reveals a role for neurotrophins in CNS patterning Neuron 19 1997 269 281
104. P.J. Skene, R.S. Illingworth, S. Webb, A.R. Kerr, K.D. James, D.J. Turner, R. Andrews, and A.P. Bird Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state Mol. Cell. 37 2010 457 468
105. F. Soliman, C.E. Glatt, K.G. Bath, L. Levita, R.M. Jones, S.S. Pattwell, D. Jing, N. Tottenham, D. Amso, and L.H. Somerville A genetic variant BDNF polymorphism alters extinction learning in both mouse and human Science 327 2010 863 866
106. M.M. Suzuki, and A. Bird DNA methylation landscapes: provocative insights from epigenomics Nat. Rev. Genet. 9 2008 465 476
107. M. Szyf The dynamic epigenome and its implications in toxicology Toxicol. Sci. 100 2007 7 23
108. M. Tahiliani, K.P. Koh, Y. Shen, W.A. Pastor, H. Bandukwala, Y. Brudno, S. Agarwal, L.M. Iyer, D.R. Liu, L. Aravind, and A. Rao Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 Science 324 2009 930 935
109. S. Takei, S. Morinobu, S. Yamamoto, M. Fuchikami, T. Matsumoto, and S. Yamawaki Enhanced hippocampal BDNF/TrkB signaling in response to fear conditioning in an animal model of posttraumatic stress disorder J. Psychiatr. Res. 45 2011 460 468
110. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism Neuron 20 1998 709 726
111. F. Tian, X.Z. Hu, X. Wu, H. Jiang, H. Pan, A.M. Marini, and R.H. Lipsky Dynamic chromatin remodeling events in hippocampal neurons are associated with NMDA receptor-mediated activation of Bdnf gene promoter 1 J. Neurochem. 109 2009 1375 1388
112. E. Tongiorgi, M. Righi, and A. Cattaneo Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons J. Neurosci. 17 1997 9492 9505
113. N.M. Tsankova, O. Berton, W. Renthal, A. Kumar, R.L. Neve, and E.J. Nestler Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action Nat. Neurosci. 9 2006 519 525
114. N.M. Tsankova, A. Kumar, and E.J. Nestler Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures J. Neurosci. 24 2004 5603 5610
115. F.M. Vassoler, S.L. White, H.D. Schmidt, G. Sadri-Vakili, and R.C. Pierce Epigenetic inheritance of a cocaine-resistance phenotype Nat. Neurosci. 16 2013 42 47
116. P.A. Wade, A. Gegonne, P.L. Jones, E. Ballestar, F. Aubry, and A.P. Wolffe Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation Nat. Genet. 23 1999 62 66
117. W.S. Wang, S. Kang, W.T. Liu, M. Li, Y. Liu, C. Yu, J. Chen, Z.Q. Chi, L. He, and J.G. Liu Extinction of aversive memories associated with morphine withdrawal requires ERK-mediated epigenetic regulation of brain-derived neurotrophic factor transcription in the rat ventromedial prefrontal cortex J. Neurosci. 32 2012 13763 13775
118. M. Weber, I. Hellmann, M.B. Stadler, L. Ramos, S. Paabo, M. Rebhan, and D. Schubeler Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome Nat. Genet. 39 2007 457 466
119. H. Wu, J. Tao, P.J. Chen, A. Shahab, W. Ge, R.P. Hart, X. Ruan, Y. Ruan, and Y.E. Sun 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 2010 18161 18166
120. H.G. Yoon, D.W. Chan, A.B. Reynolds, J. Qin, and J. Wong N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso Mol. Cell. 12 2003 723 734
121. M. Yossifoff, T. Kisliouk, and N. Meiri Dynamic changes in DNA methylation during thermal control establishment affect CREB binding to the brain-derived neurotrophic factor promoter Eur. J. Neurosci. 28 2008 2267 2277
122. Y. Zeng, M. Tan, J. Kohyama, M. Sneddon, J.B. Watson, Y.E. Sun, and C.W. Xie Epigenetic enhancement of BDNF signaling rescues synaptic plasticity in aging J. Neurosci. 31 2011 17800 17810
123. Y. Zhang, H.H. Ng, H. Erdjument-Bromage, P. Tempst, A. Bird, and D. Reinberg Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation Genes Dev. 13 1999 1924 1935
124. Z. Zhou, E.J. Hong, S. Cohen, W.N. Zhao, H.Y. Ho, L. Schmidt, W.G. Chen, Y. Lin, E. Savner, and E.C. Griffith Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation Neuron 52 2006 255 269
125. J.K. Zhu Active DNA demethylation mediated by DNA glycosylases Annu. Rev. Genet. 43 2009 143 166