Advanced search
Publication Cover
Epigenomics Volume 3, 2011 - Issue 2
Submit an article Journal homepage
417
Views
0
CrossRef citations to date
0
Altmetric
Review

Epigenetic Mechanisms in Memory and Synaptic Function

Faraz A Sultan1 University of Alabama at Birmingham, Department of Neurobiology, Evelyn F McKnight Brain Institute, 1007 Shelby Building, 1825 University Boulevard Birmingham, AL35294-2182, USAView further author information
&
Jeremy J Day1 University of Alabama at Birmingham, Department of Neurobiology, Evelyn F McKnight Brain Institute, 1007 Shelby Building, 1825 University Boulevard Birmingham, AL35294-2182, USACorrespondence[email protected]
View further author information
Pages 157-181 | Published online: 20 Apr 2011

Bibliography

  • Sweatt JD : Mechanisms of Memory. Elsevier, Burlington, MA, USA (2010).
  • Abel T , LattalKM: Molecular mechanisms of memory acquisition, consolidation and retrieval.Curr. Opin. Neurobiol.11(2) , 180–187 (2001).
  • Alberini CM : Transcription factors in long-term memory and synaptic plasticity.Physiol. Rev.89(1) , 121–145 (2009).
  • Stevens CF : CREB and memory consolidation.Neuron13(4) , 769–770 (1994).
  • Bailey CH , KandelER, SiK: The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth.Neuron44(1) , 49–57 (2004).
  • Roberson ED , SweattJD: A biochemical blueprint for long-term memory.Learn Mem.6(4) , 381–388 (1999).
  • Price JC , GuanS, BurlingameA, PrusinerSB, GhaemmaghamiS: Analysis of proteome dynamics in the mouse brain.Proc. Natl Acad. Sci. USA107(32) , 14508–14513 (2010).
  • Archibald K , PerryMJ, MolnarE, HenleyJM: Surface expression and metabolic half-life of AMPA receptors in cultured rat cerebellar granule cells.Neuropharmacology37(10–11) , 1345–1353 (1998).
  • Silva AJ , StevensCF, TonegawaS, WangY: Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice.Science257(5067) , 201–206 (1992).
  • Berger SL , KouzaridesT, ShiekhattarR, ShilatifardA: An operational definition of epigenetics.Genes Dev.23(7) , 781–783 (2009).
  • Price TD , QvarnstromA, IrwinDE: The role of phenotypic plasticity in driving genetic evolution.Proc. Biol. Sci.270(1523) , 1433–1440 (2003).
  • Bird A : Perceptions of epigenetics.Nature447(7143) , 396–398 (2007).
  • Kouzarides T : Chromatin modifications and their function.Cell128(4) , 693–705 (2007).
  • Brownell JE , ZhouJ, RanalliTet al.: Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation.Cell84(6) , 843–851 (1996).
  • Taunton J , HassigCA, SchreiberSL: A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p.Science272(5260) , 408–411 (1996).
  • Allis CD , ReinbergD: Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, USA (2007).
  • Nowak SJ , CorcesVG: Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation.Trends Genet.20(4) , 214–220 (2004).
  • Peters AH , SchubelerD: Methylation of histones: playing memory with DNA.Curr. Opin. Cell Biol.17(2) , 230–238 (2005).
  • Shilatifard A : Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation.Curr. Opin. Cell Biol.20(3) , 341–348 (2008).
  • Shiio Y , EisenmanRN: Histone sumoylation is associated with transcriptional repression.Proc. Natl Acad. Sci. USA100(23) , 13225–13230 (2003).
  • Graff J , MansuyIM: Epigenetic codes in cognition and behaviour.Behav. Brain Res.192(1) , 70–87 (2008).
  • Jaenisch R , BirdA: Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals.Nat. Genet.33Suppl , 245–254 (2003).
  • Chahrour M , JungSY, ShawCet al.: MeCP2, a key contributor to neurological disease, activates and represses transcription.Science320(5880) , 1224–1229 (2008).
  • Wu SC , ZhangY: Active DNA demethylation: many roads lead to Rome.Nat. Rev. Mol. Cell Biol.11(9) , 607–620 (2010).
  • Jones PL , VeenstraGJ, WadePAet al.: Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription.Nat. Genet.19(2) , 187–191 (1998).
  • Guan JS , HaggartySJ, GiacomettiEet al.: HDAC2 negatively regulates memory formation and synaptic plasticity.Nature459(7243) , 55–60 (2009).
  • Morris MJ , KarraAS, MonteggiaLM: Histone deacetylases govern cellular mechanisms underlying behavioral and synaptic plasticity in the developing and adult brain.Behav. Pharmacol.21(5–6) , 409–419 (2010).
  • Janssen C , SchmalbachS, BoeseltS, SarletteA, DenglerR, PetriS: Differential histone deacetylase mRNA expression patterns in amyotrophic lateral sclerosis.J. Neuropathol. Exp. Neurol.69(6) , 573–581 (2010).
  • Riccio A : Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways.Nat. Neurosci.13(11) , 1330–1337 (2010).
  • MacDonald JL , RoskamsAJ: Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development.Dev. Dyn.237(8) , 2256–2267 (2008).
  • Schaefer A , SampathSC, IntratorAet al.: Control of cognition and adaptive behavior by the GLP/G9a epigenetic suppressor complex.Neuron64(5) , 678–691 (2009).
  • Feng J , ChangH, LiE, FanG: Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system.J. Neurosci. Res.79(6) , 734–746 (2005).
  • Thompson RF , AtzmonG, GheorgheCet al.: Tissue-specific dysregulation of DNA methylation in aging.Aging Cell9(4) , 506–518
  • Penner MR , RothTL, BarnesCA, SweattJD: An epigenetic hypothesis of aging-related cognitive dysfunction.Front. Aging Neurosci.2 , 9 (2010).
  • Penner MR , RothTL, ChawlaMKet al.: Age-related changes in Arc transcription and DNA methylation within the hippocampus.Neurobiol. Aging (2010) (Epub ahead of print).
  • Noh JS , SharmaRP, VeldicMet al.: DNA methyltransferase 1 regulates reelin mRNA expression in mouse primary cortical cultures.Proc. Natl Acad. Sci. USA102(5) , 1749–1754 (2005).
  • Sharma RP , GavinDP, GraysonDR: CpG methylation in neurons: message, memory, or mask?Neuropsychopharmacology35(10) , 2009–2020 (2010).
  • Levenson JM : DNA (cytosine-5) methyltransferase inhibitors: a potential therapeutic agent for schizophrenia.Mol. Pharmacol.71(3) , 635–637 (2007).
  • Barreto G , SchaferA, MarholdJet al.: Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation.Nature445(7128) , 671–675 (2007).
  • Ma DK , JangMH, GuoJUet al.: Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis.Science323(5917) , 1074–1077 (2009).
  • Kandel JHS , Jessell TM: Principles of Neural Science (4th Edition). McGraw-Hill Medical (2000).
  • Nelson ED , KavalaliET, MonteggiaLM: Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation.J. Neurosci.28(2) , 395–406 (2008).
  • Monteggia LM , KavalaliET: Rett syndrome and the impact of MeCP2 associated transcriptional mechanisms on neurotransmission.Biol. Psychiatry65(3) , 204–210 (2009).
  • Asaka Y , JugloffDG, ZhangL, EubanksJH, FitzsimondsRM: Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome.Neurobiol. Dis.21(1) , 217–227 (2006).
  • Collins AL , LevensonJM, VilaythongAPet al.: Mild overexpression of MeCP2 causes a progressive neurological disorder in mice.Hum. Mol. Genet.13(21) , 2679–2689 (2004).
  • Belichenko PV , OldforsA, HagbergB, DahlstromA: Rett syndrome: 3-D confocal microscopy of cortical pyramidal dendrites and afferents.Neuroreport5(12) , 1509–1513 (1994).
  • Kaufmann WE , MacDonaldSM, AltamuraCR: Dendritic cytoskeletal protein expression in mental retardation: an immunohistochemical study of the neocortex in Rett syndrome.Cereb. Cortex10(10) , 992–1004 (2000).
  • Dani VS , ChangQ, MaffeiA, TurrigianoGG, JaenischR, NelsonSB: 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. USA102(35) , 12560–12565 (2005).
  • Suzuki M , YamadaT, Kihara-NegishiF, SakuraiT, OikawaT: Direct association between PU.1 and MeCP2 that recruits mSin3A-HDAC complex for PU.1-mediated transcriptional repression.Oncogene22(54) , 8688–8698 (2003).
  • Nelson ED , KavalaliET, MonteggiaLM: MeCP2-dependent transcriptional repression regulates excitatory neurotransmission.Curr. Biol.16(7) , 710–716 (2006).
  • Akhtar MW , RaingoJ, NelsonEDet al.: Histone deacetylases 1 and 2 form a developmental switch that controls excitatory synapse maturation and function.J. Neurosci.29(25) , 8288–8297 (2009).
  • Guan Z , GiustettoM, LomvardasSet al.: Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure.Cell111(4) , 483–493 (2002).
  • Levenson JM , O‘RiordanKJ, BrownKD, TrinhMA, MolfeseDL, SweattJD: Regulation of histone acetylation during memory formation in the hippocampus.J. Biol. Chem.279(39) , 40545–40559 (2004).
  • Vecsey CG , HawkJD, LattalKMet al.: Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation.J. Neurosci.27(23) , 6128–6140 (2007).
  • Alarcon JM , MalleretG, TouzaniKet al.: Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration.Neuron42(6) , 947–959 (2004).
  • Wood MA , KaplanMP, ParkAet al.: Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage.Learn Mem.12(2) , 111–119 (2005).
  • Kim SY , LevensonJM, KorsmeyerS, SweattJD, SchumacherA: Developmental regulation of Eed complex composition governs a switch in global histone modification in brain.J. Biol. Chem.282(13) , 9962–9972 (2007).
  • Fontan-Lozano A , Suarez-PereiraI, HorrilloA, del-Pozo-MartinY, HmadchaA, CarrionAM: Histone H1 poly[ADP]-ribosylation regulates the chromatin alterations required for learning consolidation.J. Neurosci.30(40) , 13305–13313 (2010).
  • Yeh SH , LinCH, GeanPW: Acetylation of nuclear factor-κB in rat amygdala improves long-term but not short-term retention of fear memory.Mol. Pharmacol.65(5) , 1286–1292 (2004).
  • Putignano E , LonettiG, CanceddaLet al.: Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity.Neuron53(5) , 747–759 (2007).
  • Levenson JM , RothTL, LubinFDet al.: Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus.J. Biol. Chem.281(23) , 15763–15773 (2006).
  • Miller CA , CampbellSL, SweattJD: DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity.Neurobiol. Learn Mem.89(4) , 599–603 (2008).
  • Feng J , ZhouY, CampbellSLet al.: Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons.Nat. Neurosci.13(4) , 423–430 (2010).
  • Zhao X , UebaT, ChristieBRet al.: Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function.Proc. Natl Acad. Sci. USA100(11) , 6777–6782 (2003).
  • Moretti P , LevensonJM, BattagliaFet al.: Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome.J. Neurosci.26(1) , 319–327 (2006).
  • Tsankova N , RenthalW, KumarA, NestlerEJ: Epigenetic regulation in psychiatric disorders.Nat. Rev. Neurosci.8(5) , 355–367 (2007).
  • Tsankova NM , BertonO, RenthalW, KumarA, NeveRL, NestlerEJ: Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action.Nat. Neurosci.9(4) , 519–525 (2006).
  • Weaver IC , CervoniN, ChampagneFAet al.: Epigenetic programming by maternal behavior.Nat. Neurosci.7(8) , 847–854 (2004).
  • Weaver IC , DiorioJ, SecklJR, SzyfM, MeaneyMJ: Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites.Ann. NY Acad. Sci.1024 , 182–212 (2004).
  • Roth TL , LubinFD, FunkAJ, SweattJD: Lasting epigenetic influence of early-life adversity on the BDNF gene.Biol. Psychiatry65(9) , 760–769 (2009).
  • Day JJ , SweattJD: DNA methylation and memory formation.Nat. Neurosci.13(11) , 1319–1323 (2010).
  • Levenson JM , SweattJD: Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation.Cell Mol. Life Sci.63(9) , 1009–1016 (2006).
  • Federman N , FustinanaMS, RomanoA: Histone acetylation is recruited in consolidation as a molecular feature of stronger memories.Learn Mem.16(10) , 600–606 (2009).
  • Stefanko DP , BarrettRM, LyAR, ReolonGK, WoodMA: Modulation of long-term memory for object recognition via HDAC inhibition.Proc. Natl Acad. Sci. USA106(23) , 9447–9452 (2009).
  • Korzus E , RosenfeldMG, MayfordM: CBP histone acetyltransferase activity is a critical component of memory consolidation.Neuron42(6) , 961–972 (2004).
  • Josselyn SA , NguyenPV: CREB, synapses and memory disorders: past progress and future challenges.Curr. Drug Targets CNS Neurol. Disord.4(5) , 481–497 (2005).
  • Chen G , ZouX, WatanabeH, van Deursen JM, Shen J: CREB binding protein is required for both short-term and long-term memory formation. J. Neurosci.30(39) , 13066–13077 (2010).
  • Oliveira AM , WoodMA, McDonoughCB, AbelT: Transgenic mice expressing an inhibitory truncated form of p300 exhibit long-term memory deficits.Learn Mem.14(9) , 564–572 (2007).
  • Kalkhoven E : CBP and p300: HATs for different occasions.Biochem. Pharmacol.68(6) , 1145–1155 (2004).
  • Ramos YF , HestandMS, VerlaanMet al.: Genome-wide assessment of differential roles for p300 and CBP in transcription regulation.Nucleic Acids Res.38(16) , 5396–5408
  • Oliveira AM , AbelT, BrindlePK, WoodMA: Differential role for CBP and p300 CREB-binding domain in motor skill learning.Behav. Neurosci.120(3) , 724–729 (2006).
  • Burke SN , BarnesCA: Neural plasticity in the ageing brain.Nat. Rev. Neurosci.7(1) , 30–40 (2006).
  • Kilgore M , MillerCA, FassDMet al.: Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer‘s disease.Neuropsychopharmacology35(4) , 870–880 (2010).
  • Peleg S , SananbenesiF, ZovoilisAet al.: Altered histone acetylation is associated with age-dependent memory impairment in mice.Science328(5979) , 753–756 (2010).
  • Graff J , MansuyIM: Epigenetic dysregulation in cognitive disorders.Eur. J. Neurosci.30(1) , 1–8 (2009).
  • Fischer A , SananbenesiF, MungenastA, TsaiLH: Targeting the correct HDAC(s) to treat cognitive disorders.Trends Pharmacol. Sci.31(12) , 605–617 (2010).
  • Selvi BR , CasselJC, KunduTK, BoutillierAL: Tuning acetylation levels with HAT activators: Therapeutic strategy in neurodegenerative diseases.Biochim. Biophys. Acta1799(10-12) , 840–853 (2010).
  • D‘Mello SR : Histone deacetylases as targets for the treatment of human neurodegenerative diseases.Drug News Perspect.22(9) , 513–524 (2009).
  • Chuang DM , LengY, MarinovaZ, KimHJ, ChiuCT: Multiple roles of HDAC inhibition in neurodegenerative conditions.Trends Neurosci.32(11) , 591–601 (2009).
  • Mai A , RotiliD, ValenteS, KazantsevAG: Histone deacetylase inhibitors and neurodegenerative disorders: holding the promise.Curr. Pharm. Des.15(34) , 3940–3957 (2009).
  • Duclot F , JacquetC, GongoraC, MauriceT: Alteration of working memory but not in anxiety or stress response in p300/CBP associated factor (PCAF) histone acetylase knockout mice bred on a C57BL/6 background.Neurosci. Lett.475(3) , 179–183 (2010).
  • Maurice T , DuclotF, MeunierJet al.: Altered memory capacities and response to stress in p300/CBP-associated factor (PCAF) histone acetylase knockout mice.Neuropsychopharmacology33(7) , 1584–1602 (2008).
  • Roozendaal B , HernandezA, CabreraSMet al.: Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification.J. Neurosci.30(14) , 5037–5046 (2010).
  • Swank MW , SweattJD: Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning.J. Neurosci.21(10) , 3383–3391 (2001).
  • Silingardi D , ScaliM, BelluominiG, PizzorussoT: Epigenetic treatments of adult rats promote recovery from visual acuity deficits induced by long-term monocular deprivation.Eur. J. Neurosci.31(12) , 2185–2192 (2010).
  • Chwang WB , ArthurJS, SchumacherA, SweattJD: The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation.J. Neurosci.27(46) , 12732–12742 (2007).
  • Chandramohan Y , DrosteSK, ArthurJS, ReulJM: The forced swimming-induced behavioural immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-D-aspartate/extracellular signal-regulated kinase/mitogen- and stress-activated kinase signalling pathway.Eur. J. Neurosci.27(10) , 2701–2713 (2008).
  • Reul JM , HeskethSA, CollinsA, MecinasMG: Epigenetic mechanisms in the dentate gyrus act as a molecular switch in hippocampus-associated memory formation.Epigenetics4(7) , 434–439 (2009).
  • Lubin FD , SweattJD: The IκB kinase regulates chromatin structure during reconsolidation of conditioned fear memories.Neuron55(6) , 942–957 (2007).
  • Merlo E , FreudenthalR, RomanoA: The IκB kinase inhibitor sulfasalazine impairs long-term memory in the crab Chasmagnathus.Neuroscience112(1) , 161–172 (2002).
  • Zocchi L , Sassone-CorsiP: Joining the dots: from chromatin remodeling to neuronal plasticity.Curr. Opin. Neurobiol.20(4) , 432–440 (2010).
  • Koshibu K , GraffJ, BeullensMet al.: Protein phosphatase 1 regulates the histone code for long-term memory.J. Neurosci.29(41) , 13079–13089 (2009).
  • Cohen-Armon M , VisochekL, KatzoffAet al.: Long-term memory requires polyADP-ribosylation.Science304(5678) , 1820–1822 (2004).
  • Goldberg S , VisochekL, GiladiE, GozesI, Cohen-ArmonM: PolyADP-ribosylation is required for long-term memory formation in mammals.J. Neurochem.111(1) , 72–79 (2009).
  • Lubin FD , RothTL, SweattJD: Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory.J. Neurosci.28(42) , 10576–10586 (2008).
  • Miller CA , SweattJD: Covalent modification of DNA regulates memory formation.Neuron53(6) , 857–869 (2007).
  • Juttermann R , LiE, JaenischR: Toxicity of 5-aza-2´-deoxycytidine to mammalian cells is mediated primarily by covalent trapping of DNA methyltransferase rather than DNA demethylation.Proc. Natl Acad. Sci. USA91(25) , 11797–11801 (1994).
  • Frankland PW , BontempiB, TaltonLE, KaczmarekL, SilvaAJ: The involvement of the anterior cingulate cortex in remote contextual fear memory.Science304(5672) , 881–883 (2004).
  • Miller CA , GavinCF, WhiteJAet al.: Cortical DNA methylation maintains remote memory.Nat. Neurosci.13(6) , 664–666 (2010).
  • Fuso A , NicoliaV, CavallaroRAet al.: B-vitamin deprivation induces hyperhomocysteinemia and brain S-adenosylhomocysteine, depletes brain S-adenosylmethionine, and enhances PS1 and BACE expression and amyloid-β deposition in mice.Mol. Cell Neurosci.37(4) , 731–746 (2008).
  • Fuso A , SeminaraL, CavallaroRA, D‘AnselmiF, ScarpaS: S-adenosylmethionine/homocysteine cycle alterations modify DNA methylation status with consequent deregulation of PS1 and BACE and β-amyloid production.Mol. Cell Neurosci.28(1) , 195–204 (2005).
  • Scarpa S , FusoA, D‘AnselmiF, CavallaroRA: Presenilin 1 gene silencing by S-adenosylmethionine: a treatment for Alzheimer disease?FEBS Lett.541(1–3) , 145–148 (2003).
  • Chen TF , HuangRF, LinSE, LuJF, TangMC, ChiuMJ: Folic Acid potentiates the effect of memantine on spatial learning and neuronal protection in an Alzheimer‘s disease transgenic model.J. Alzheimers Dis.20(2) , 607–615 (2010).
  • Mastroeni D , GroverA, DelvauxE, WhitesideC, ColemanPD, RogersJ: Epigenetic changes in Alzheimer‘s disease: decrements in DNA methylation.Neurobiol. Aging31(12) , 2025–2037 (2010).
  • Silva PN , GigekCO, LealMFet al.: Promoter methylation analysis of SIRT3, SMARCA5, HTERT and CDH1 genes in aging and Alzheimer‘s disease.J. Alzheimers Dis.13(2) , 173–176 (2008).
  • Wang SC , OelzeB, SchumacherA: Age-specific epigenetic drift in late-onset Alzheimer‘s disease.PLoS One3(7) , e2698 (2008).
  • Scarpa S , CavallaroRA, D‘AnselmiF, FusoA: Gene silencing through methylation: an epigenetic intervention on Alzheimer disease.J. Alzheimers Dis.9(4) , 407–414 (2006).
  • Robinson TE , KolbB: Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine.J. Neurosci.17(21) , 8491–8497 (1997).
  • LaPlant Q , VialouV, CovingtonHE, 3rd et al.: Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat. Neurosci.13(9) , 1137–1143 (2010).
  • Nestler EJ : Molecular basis of long-term plasticity underlying addiction.Nat. Rev. Neurosci.2(2) , 119–128 (2001).
  • Kumar A , ChoiKH, RenthalWet al.: Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum.Neuron48(2) , 303–314 (2005).
  • Sanchis-Segura C , Lopez-AtalayaJP, BarcoA: Selective boosting of transcriptional and behavioral responses to drugs of abuse by histone deacetylase inhibition.Neuropsychopharmacology34(13) , 2642–2654 (2009).
  • Renthal W , MazeI, KrishnanVet al.: Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli.Neuron56(3) , 517–529 (2007).
  • Wang L , LvZ, HuZet al.: Chronic cocaine-induced H3 acetylation and transcriptional activation of CaMKIIα in the nucleus accumbens is critical for motivation for drug reinforcement.Neuropsychopharmacology35(4) , 913–928 (2010).
  • Renthal W , KumarA, XiaoGet al.: Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins.Neuron62(3) , 335–348 (2009).
  • Maze I , CovingtonHE, 3rd, Dietz DM et al.: Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science327(5962) , 213–216 (2010).
  • Stipanovich A , ValjentE, MatamalesMet al.: A phosphatase cascade by which rewarding stimuli control nucleosomal response.Nature453(7197) , 879–884 (2008).
  • Im HI , HollanderJA, BaliP, KennyPJ: MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA.Nat. Neurosci.13(9) , 1120–1127 (2010).
  • Deng W , AimoneJB, GageFH: New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?Nat. Rev. Neurosci.11(5) , 339–350 (2010).
  • Anier K , MalinovskajaK, Aonurm-HelmA, ZharkovskyA, KaldaA: DNA methylation regulates cocaine-induced behavioral sensitization in mice.Neuropsychopharmacology35(12) , 2450–2461 (2010).
  • Shiflett MW , MartiniRP, MaunaJC, FosterRL, PeetE, ThielsE: Cue-elicited reward-seeking requires extracellular signal-regulated kinase activation in the nucleus accumbens.J. Neurosci.28(6) , 1434–1443 (2008).
  • Shiflett MW , MaunaJC, ChipmanAM, PeetE, ThielsE: Appetitive Pavlovian conditioned stimuli increase CREB phosphorylation in the nucleus accumbens.Neurobiol. Learn Mem.92(3) , 451–454 (2009).
  • Danilova AB , KharchenkoOA, ShevchenkoKG, GrinkevichLN: Histone H3 acetylation is asymmetrically induced upon learning in identified neurons of the food aversion network in the mollusk Helix lucorum.Front. Behav. Neurosci.4 , 180 (2010).
  • Cohen-Armon M , VisochekL, RozensalDet al.: DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation.Mol. Cell25(2) , 297–308 (2007).
  • Tsankova NM , KumarA, NestlerEJ: Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures.J. Neurosci.24(24) , 5603–5610 (2004).
  • Huang Y , DohertyJJ, DingledineR: Altered histone acetylation at glutamate receptor 2 and brain-derived neurotrophic factor genes is an early event triggered by status epilepticus.J. Neurosci.22(19) , 8422–8428 (2002).
  • Sng JC , TaniuraH, YonedaY: Histone modifications in kainate-induced status epilepticus.Eur. J. Neurosci.23(5) , 1269–1282 (2006).
  • Malkani S , WallaceKJ, DonleyMP, RosenJB: An egr-1 (zif268) antisense oligodeoxynucleotide infused into the amygdala disrupts fear conditioning.Learn Mem.11(5) , 617–624 (2004).
  • Baumgartel K , GenouxD, WelzlHet al.: Control of the establishment of aversive memory by calcineurin and Zif.Nat. Neurosci.11(5) , 572–578 (2008).
  • Monfils MH , CowansageKK, LeDouxJE: Brain-derived neurotrophic factor: linking fear learning to memory consolidation.Mol. Pharmacol.72(2) , 235–237 (2007).
  • Sacktor TC : PKMzeta, LTP maintenance, and the dynamic molecular biology of memory storage.Prog. Brain Res.169 , 27–40 (2008).
  • Fuchikami M , MorinobuS, KurataA, YamamotoS, YamawakiS: Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus.Int. J. Neuropsychopharmacol.12(1) , 73–82 (2009).
  • Chwang WB , O‘RiordanKJ, LevensonJM, SweattJD: ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning.Learn Mem.13(3) , 322–328 (2006).
  • Crosio C , HeitzE, AllisCD, BorrelliE, Sassone-CorsiP: Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons.J. Cell Sci.116(Pt 24) , 4905–4914 (2003).
  • Gupta S , KimSY, ArtisSet al.: Histone methylation regulates memory formation.J. Neurosci.30(10) , 3589–3599 (2010).
  • An W : Histone acetylation and methylation: combinatorial players for transcriptional regulation.Subcell Biochem.41 , 351–369 (2007).
  • Oliver SS , DenuJM: Dynamic interplay between histone H3 modifications and protein interpreters: emerging evidence for a ‘histone language‘.Chembiochem12(2) , 299–307 (2010).
  • Meaney MJ , Ferguson-SmithAC: Epigenetic regulation of the neural transcriptome: the meaning of the marks.Nat. Neurosci.13(11) , 1313–1318 (2010).
  • Martinowich K , HattoriD, WuHet al.: DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation.Science302(5646) , 890–893 (2003).
  • Rai K , HugginsIJ, JamesSR, KarpfAR, JonesDA, CairnsBR: DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45.Cell135(7) , 1201–1212 (2008).
  • Kangaspeska S , StrideB, MetivierRet al.: Transient cyclical methylation of promoter DNA.Nature452(7183) , 112–115 (2008).
  • Metivier R , GallaisR, TiffocheCet al.: Cyclical DNA methylation of a transcriptionally active promoter.Nature452(7183) , 45–50 (2008).
  • Sharma RP , TunN, GraysonDR: Depolarization induces downregulation of DNMT1 and DNMT3a in primary cortical cultures.Epigenetics3(2) , 74–80 (2008).
  • Marutha Ravindran CR , TickuMK: Effect of 5-azacytidine on the methylation aspects of NMDA receptor NR2B gene in the cultured cortical neurons of mice.Neurochem. Res.34(2) , 342–350 (2009).
  • Marutha Ravindran CR , TickuMK: Changes in methylation pattern of NMDA receptor NR2B gene in cortical neurons after chronic ethanol treatment in mice.Brain Res. Mol. Brain Res.121(1–2) , 19–27 (2004).
  • Marutha RCR , TickuMK: Role of CpG islands in the up-regulation of NMDA receptor NR2B gene expression following chronic ethanol treatment of cultured cortical neurons of mice.Neurochem. Int.46(4) , 313–327 (2005).
  • Qiang M , DennyA, ChenJ, TickuMK, YanB, HendersonG: The site specific demethylation in the 5´-regulatory area of NMDA receptor 2B subunit gene associated with CIE-induced up-regulation of transcription.PLoS One5(1) , e8798 (2010).
  • Lee S , KimW, HamBJ, ChenW, BearMF, YoonBJ: Activity-dependent NR2B expression is mediated by MeCP2-dependent epigenetic regulation.Biochem. Biophys. Res. Commun.377(3) , 930–934 (2008).
  • Tian F , HuXZ, WuXet al.: Dynamic chromatin remodeling events in hippocampal neurons are associated with NMDA receptor-mediated activation of Bdnf gene promoter 1.J. Neurochem.109(5) , 1375–1388 (2009).
  • Levenson JM , QiuS, WeeberEJ: The role of reelin in adult synaptic function and the genetic and epigenetic regulation of the reelin gene.Biochim. Biophys. Acta1779(8) , 422–431 (2008).
  • Koshibu K , GraffJ, MansuyIM: Nuclear protein phosphatase-1: an epigenetic regulator of fear memory and amygdala long-term potentiation.Neuroscience173 , 30–36 (2011).
  • Abel T , MartinKC, BartschD, KandelER: Memory suppressor genes: inhibitory constraints on the storage of long-term memory.Science279(5349) , 338–341 (1998).
  • Costa E , DongE, GraysonDR, GuidottiA, RuzickaW, VeldicM: Reviewing the role of DNA (cytosine-5) methyltransferase overexpression in the cortical GABAergic dysfunction associated with psychosis vulnerability.Epigenetics2(1) , 29–36 (2007).
  • Jiang Y , LangleyB, LubinFDet al.: Epigenetics in the nervous system.J. Neurosci.28(46) , 11753–11759 (2008).
  • Kim TK , HembergM, GrayJMet al.: Widespread transcription at neuronal activity-regulated enhancers.Nature465(7295) , 182–187 (2010).
  • Smalheiser NR , LugliG, ThimmapuramJ, CookEH, LarsonJ: Endogenous siRNAs and noncoding RNA-derived small RNAs are expressed in adult mouse hippocampus and are up-regulated in olfactory discrimination training.RNA17(1) , 166–181 (2011).
  • Edbauer D , NeilsonJR, FosterKAet al.: Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR.Neuron65(3) , 373–384 (2010).
  • Rajasethupathy P , FiumaraF, SheridanRet al.: Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB.Neuron63(6) , 803–817 (2009).
  • Gao J , WangWY, MaoYWet al.: A novel pathway regulates memory and plasticity via SIRT1 and miR.Nature466(7310) , 1105–1109 (2010).
  • Ma DK , MarchettoMC, GuoJU, MingGL, GageFH, SongH: Epigenetic choreographers of neurogenesis in the adult mammalian brain.Nat. Neurosci.13(11) , 1338–1344 (2010).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.