Advanced search
Publication Cover
Epigenomics Volume 1, 2009 - Issue 1
Submit an article Journal homepage
159
Views
1
CrossRef citations to date
0
Altmetric
Review

Environmental Regulation Of The Neural Epigenome

Judy Sng1 Integrative Neuroscience Program, Singapore Institute for Clinical Sciences, 30 Medial Drive, 117609Singapore. View further author information
&
Michael J Meaney1 Integrative Neuroscience Program, Singapore Institute for Clinical Sciences, 30 Medial Drive, 117609Singapore. ;2 Sackler Program for Epigenetics and Psychobiology of McGill University, Douglas Mental Health University Institute, Quebec, CanadaCorrespondence[email protected]
View further author information
Pages 131-151 | Published online: 01 Oct 2009

Bibliography

  • Rutter M : Gene–environment interdependence.Dev. Sci.10 , 12–18 (2007).
  • Ebstein RP : The molecular genetic architecture of human personality: beyond self-report questionnaires.Mol. Psychiatry11 , 427–445 (2006).
  • Meyer-Lindenberg A , WeinbergerDR: Intermediate phenotypes and genetic mechanisms of psychiatric disorders.Nat. Rev. Neurosci.7 , 818–827 (2006).
  • Petronis A : Epigenetics and twins: three variations on the theme.Trends Genet.22, , 347–350 (2006).
  • Fraga MF , BallestarE, PazMF et al.: Epigenetic differences arise during the lifetime of monozygotic twins.Proc. Natl Acad. Sci. USA102 , 10604–10609 (2005).
  • Weksberg R , ShumanC, CaluseriuO et al.: Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith–Wiedemann syndrome.Hum. Mol. Genet.11 , 1317–1325 (2002).
  • Meaney MJ , SzyfM: Maternal effects as a model for environmentally-dependent chromatin plasticity.Trends Neurosci.28 , 456–463 (2005).
  • Meaney MJ , SzyfM, SecklJR: Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health.Trends Mol. Med.13 , 269–277 (2007).
  • Jirtle RL , SkinnerMK: Environmental epigenomics and disease susceptibility.Nat. Rev. Genet.8 , 253–262 (2007).
  • Tsankova N , RenthalW, KumarA, NestlerEJ: Epigenetic regulation in psychiatric disorders.Nat. Rev. Neurosci.8 , 355–367 (2007).
  • Sweatt JD : Experience-dependent epigenetic modifications in the central nervous system.Biol. Psychiatry65 , 191–197 (2009).
  • Ooi SKT , BestorTH: The colorful history of active demethylation.Cell133 , 1145–1148 (2008).
  • Bateson P , BarkerD, Clutton-BrockT et al.: Developmental plasticity and human health.Nature430 , 419–421 (2004).
  • Gluckman PD , HansonMA: Developmental plasticity and human disease: research directions.J. Int. Med.261 , 461–471 (2007).
  • Seckl JR , HolmesMC: Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming‘ of adult pathophysiology.Nat. Clin. Prac. Endocrinol. Metab.3 , 479–488 (2007).
  • Paulsen M , Ferguson-SmithAC: DNA methylation in genomic imprinting, development, and disease.J. Pathol.195 , 97–110 (2001).
  • Miller F , GauthierAS: Timing is everything: making neurons versus glia in the developing cortex.Neuron54 , 357–369 (2007).
  • Sun Y , Nadal-VicensM, MisonoS et al.: Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms.Cell104 , 365–376 (2001).
  • Meissner A . Mikkelsen TS. Gu H et al.: Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature454 , 766–770 (2008).
  • Hatada I , MoritaS, KimuraM, HoriiT, YamashitaR, NakaiK: Genome-wide demethylation during neural differentiation of P19 embryonic carcinoma cells.J. Hum. Genet.53 , 185–191 (2008).
  • Heintzman ND , StuartRK, HonG et al.: Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome.Nat. Genet.39 , 311–318 (2007).
  • Shen Q , WangY, DimosJT et al.: The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells.Nat. Neurosci.6 , 743–751 (2006).
  • Namihira M , NakashimaK, Taga,T: Developmental stage dependent regulation of DNA methylation and chromatin modification in a immature astrocyte specific gene promoter. FEBS Lett.572 , 184–188 (2004).
  • Barnabé-Heider F , WasylnkaJA, FernandesKJ et al.: Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1.Neuron48 , 253–265 (2005).
  • Bonni A , SunY, Nadal-VicensM et al.: Regulation of gliogenesis in the central nervous system by the JAK–STAT signaling pathway.Science278 , 477–483 (1997).
  • Nakashima K , YanagisawaM, ArakawaH et al.: Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300.Science284 , 479–482 (1999).
  • Fan G , MartinowichK, ChinMH et al.: DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling.Development132 , 3345–3356 (2005).
  • Rajan P , McKayRD: Multiple routes to astrocytic differentiation in the CNS.J. Neurosci.18 , 3620–3629 (1998).
  • Bugga L , GadientRA, KwanK, StewartCL, PattersonPH: Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor.J. Neurobiol.36 , 509–524 (1998).
  • Koblar SA Turnley AM, Classon BJ et al.: Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor. Proc. Natl Acad. Sci. USA95 , 3178–3181 (1998).
  • He F , GeW, ZhuW, Becker-CataniaS et al.: A positive autoregulation loop of JAK–STAT signaling is part of the clock mechanism regulating astrogliogenesis.Nat. Neurosci.8 , 616–625 (2005).
  • Sauvageot CM , StilesCD: Molecular mechanisms controlling cortical gliogenesis.Curr. Opin. Neurobiol.12 , 244–249 (2002).
  • Takizawa T , NakashimaK, NamihiraM et al.: DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain.Dev. Cell1 , 749–758 (2001).
  • Teter B , RozovskyI, KrohnK, AndersonC, OsterburgH, FinchC: Methylation of the glial fibrillary acidic protein gene shows novel biphasic changes during brain development.Glia17 , 195–205 (1996).
  • Sun YE , MartinowichK, GeW: Making and repairing the mammalian brain – signaling toward neurogenesis and gliogenesis.Sem. Cell. Dev. Biol.14 , 161–168 (2003).
  • Fan G , MartinowichK, ChinMH et al.: DNA methylation controls the timing of astrogliogenesis through regulation of JAK–STAT signaling.Development132 , 3345–3356 (2005).
  • Repetti RL , TaylorSE, SeemanTE: Risky families: family social environments and the mental and physical health of offspring.Psychol. Bull.128 , 330–366 (2002).
  • Rossiter MC : The role of environmental variation in parental effects expression. In: Maternal Effects as Adaptations. (Mousseau TA, Fox CW, Eds). Oxford University Press, Oxford, UK, 112–136 (1998).
  • Mousseau TA , FoxCW: The adaptive significance of maternal effects.Trends Ecol. Evol.13 , 403–407 (1998).
  • Cameron N , ParentC, ChampagneFA, FishE, Ozaki-KurodaK, MeaneyMJ: The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care.Neurosci. Biobehav. Rev.29 , 843–865 (2005).
  • West-Eberhardt MJ : Developmental Plasticity and Evolution. Oxford University Press, Oxford, UK (2003).
  • Gilbert SF , EpelD: Ecological developmental biology. Sinauer Associates, MA, USA (2009).
  • Meaney MJ : The development of individual differences in behavioral and endocrine responses to stress.Annu. Rev. Neurosci.24 , 1161–1192 (2001).
  • Champagne FA , FrancisDD, MarA, MeaneyMJ: Naturally-occurring variations in maternal care in the rat as a mediating influence for the effects of environment on the development of individual differences in stress reactivity.Physiol. Behav.79 , 359–371 (2003).
  • Champagne FA : Epigenetic mechanisms and the transgenerational effects of maternal care.Front. Neuroendocrinol.29 , 386–397 (2008).
  • Schanberg SM , EvoniukG, KuhnCM: Tactile and nutritional aspects of maternal care: specific regulators of neuroendocrine function and cellular development.Proc. Soc. Exp. Biol. Med.175 , 135–146 (1984).
  • Levine S : The ontogeny of the hypothalamic–pituitary–adrenal axis. The influence of maternal factors.Ann. NY Acad. Sci.746 , 275–288 (1994).
  • Hofer MA : The psychobiology of early attachment.Clin. Neurosci. Res.4 , 291–300 (2005).
  • Liu D , DiorioJ, TannenbaumB, CaldjiC et al.: Maternal care, hippocampal glucocorticoid receptors and HPA responses to stress.Science277 , 1659–1662 (1977).
  • Caldji C , TannenbaumB, SharmaS, FrancisDD, PlotskyPM, MeaneyMJ: Maternal care during infancy regulates the development of neural systems mediating the expression of behavioral fearfulness in adulthood in the rat.Proc. Natl Acad. Sci. USA95 , 5335–5340 (1998).
  • Francis DD , DiorioJ, LiuD, MeaneyMJ: Nongenomic transmission across generations in maternal behavior and stress responses in the rat.Science286 , 1155–1158 (1999).
  • Weaver ICG , CervoniN, D‘AlessioAC et al.: Epigenetic programming through maternal behavior.Nat. Neurosci.7 , 847–854 (2004).
  • Weaver ICG , ChampagneFA, BrownSE et al.: Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life.J. Neurosci.25 , 11045–11054 (2005).
  • Menard J , ChampagneD, MeaneyMJ: Maternal care alters behavioral and neural activity patterns in the defensive burying paradigm.Neuroscience129 , 297–308 (2004).
  • Toki S , MorinobuS, ImanakaA, YamamotoS, YamawakiS, HonmaK: Importance of early lighting conditions in maternal care by dam as well as anxiety and memory later in life of offspring.Eur. J. Neurosci.25 , 815–829 (2007).
  • Caldji C , DiorioJ, MeaneyMJ: Variations in maternal care alter GABAA receptor subunit expression in brain regions associated with fear.Neuropsychopharmacology28 , 150–159 (2003).
  • Plotsky PM , CunninghamET Jr, Widmaier EP: Catecholaminergic modulation of corticotropin-releasing factor and adrenocorticotropin secretion. Endocr. Rev.10 , 437–458 (1989).
  • Koob GF , HeinrichsSC, MenzaghiF, PichEM, BrittonKT: Corticotropin-releasing factor, stress and behavior.Sem. Neurosci.6 , 221–229 (1994).
  • Bale TL , ValeWW: CRF and CRF receptors: role in stress responsivity and other behaviors.Annu. Rev. Pharm. Toxicol.44 , 525–557 (2004).
  • Jutapakdeegul N , CasalottiSO, GovitrapongP, KotchabhakdiN: Postnatal touch stimulation acutely alters corticosterone levels and glucocorticoid receptor gene expression in the neonatal rat.Dev. Neurosci.25 , 26–33 (2003).
  • Burton CL , ChatterjeeD, Chatterjee-ChakrabortyM et al.: Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague-Dawley rats.Brain Res.1158 , 28–38 (2007).
  • Gonzalez A , LovicV, WardGR, WainwrightPE, FlemingAS: Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats.Dev. Psychobiol.38 , 11–32 (2001).
  • Fenoglio KA , BrunsonKL, Avishai-ElinerS, StoneBA, KapadiaBJ, BaramTZ: Enduring, handling-evoked enhancement of hippocampal memory function and glucocorticoid receptor expression involves activation of the corticotropin-releasing factor type 1 receptor.Endocrinology146 , 4090–4096 (2005).
  • Lippmann M , BressA, NemeroffCB, PlotskyPM, Monteggia, Lisa M: Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur. J. Neurosci.25 , 3091–3098 (2007).
  • Plotsky PM , ThrivikramanKV, NemeroffCB, CaldjiC, SharmaS, MeaneyMJ: Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring.Neuropsychopharmacology30 , 2192–2204 (2005).
  • Champagne FA , MeaneyMJ: Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model.Biol. Psychiatry59 , 1227–1235 (2006).
  • Bird A : Perceptions of epigenetics.Nature447 , 396–398 (2007).
  • Waterland RA , JirtleRL: Transposable elements: targets for early nutritional effects on epigenetic gene regulation.Mol. Cell. Biol.23 , 5293–5300 (2003).
  • Waterland RA , LinJR, SmithCA, JirtleRL: Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (IGF2) locus.Hum. Mol. Genet.15 , 705–716 (2006).
  • Cooney CA , DaveAA, WolffGL: Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring.J. Nutrition132 , S2393–S2400 (2002).
  • Whitelaw NC , WhitelawE: How lifetimes shape epigenotype within and across generations.Hum. Mol. Genet.15 , R131–R137 (2006).
  • Bruniquel D , SchwartzRH: Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process.Nat. Immunol.4 , 235–240 (2003).
  • Murayama A , SakuraK, NakamaM et al.: A specific CpG site demethylation in the human interleukin 2 gene promoter is an epigenetic memory.EMBO J.25 , 1081–1092 (2006).
  • Martinowich K , HattoriD, WuH et al.: DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation.Science302 , 890–893 (2003).
  • Weaver ICG , DiAlessioAC, BrownSE et al.: The transcription factor NGFI-A mediates epigenetic programming: altering epigenetic marking through immediate early genes.J. Neurosci.27 , 1756–1768 (2007).
  • Champagne FA , WeaverICG, DiorioJ, DymovS, SzyfM, MeaneyMJ: Maternal care regulates methylation of the estrogen receptor a 1b promoter and estrogen receptor a expression in the medial preoptic area of female offspring.Endocrinology147 , 2909–2915 (2006).
  • Lubin FD , RothTL, SweattJD: Epigenetic regulation of bdnf gene transcription in the consolidation of fear memory.J. Neurosci.28 , 10576–10586 (2008).
  • Meaney MJ . Diorio J, Donaldson L, Yau J, Chapman K, Seckl JR: Handling alters the expression of messenger RNAs for AP-2, NGFI-A and NGFI-B in the hippocampus of neonatal rats. J. Neurosci.20 , 3936–3945 (2000).
  • Brandeis M , FrankD, KeshetI et al.: Sp1 elements protect a CpG island from de novo methylation.Nature371 , 435–438 (1994).
  • Kalkhoven E : CBP and p300: HATs for different occasions.Biochem. Pharmacol.68 , 1145–1155 (2004).
  • Szyf M , EliassonV, MannG, Klein, Razin A: Cellular and viral DNA hypomethylation associated with induction of Epstein-Barr virus lyticcycle. Proc. Natl Acad. Sci. USA82 , 8090–8094 (1985).
  • Detich N , BovenziV, SzyfM: Valproate induces replication-independent active DNA demethylation.J. Biol. Chem.278 , 27586–27592 (2003).
  • Wu LP , WangX, LiL et al.: Histone deacetylase inhibitor depsipeptide activates silenced genes through decreasing both CpG and H3k9 methylation on the promoter.Mol. Cell. Biol.28 , 3219–3235 (2008).
  • Cameron EE , BachmanKE, MyohanenS, HermanJG, BaylinSB: Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer.Nat. Genet.21 , 103–107 (1999).
  • Bachman KE , ParkBH, RheeI et al.: Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene.Cancer Cell3 , 89–95 (2003).
  • Belinsky SA , KlingeDM, StidleyCA et al.: Inhibition of DNA methylation and histone deacetylation prevents murine lung cancer.Cancer Res. CA63 , 7089–7093 (2003).
  • Levenson JM , O‘RiordanKJ, BrownKD, TrinhMA, MolfeseDL, SweattJD: Regulation of histone acetylation during memory formation in the hippocampus.J. Biol. Chem.279 , 40545–40559 (2004).
  • Weaver IC . Meaney MJ. Szyf M: Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl Acad. Sci. USA103 , 3480–3485 (2006).
  • Dragunow M : A role for immediate-early transcription factors in learning and memory.Behav. Genet.26 , 293–299 (1996).
  • O‘Donovan KJ , TourtellotteWG, MillbrandtJ, BarabanJM: The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience.Trends Neurosci.22 , 167–173 (1999).
  • Jones MW , ErringtonML, FrenchPJ et al.: A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories.Nat. Neurosci.4 , 289–296 (2001).
  • Knapska E , KaczmarekL: A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK?Prog. Neurobiol.74 , 183–211 (2004).
  • Liu D , DiorioJ, DayJC, FrancisDD, MarA, MeaneyMJ: Maternal care, hippocampal synaptogenesis and cognitive development in the Rat.Nat. Neurosci.3 , 799–806 (2000).
  • Bredy TW , HumpartzoomianRA, CainDP, MeaneyMJ: The influence of maternal care and environmental enrichment on hippocampal development and function in the rat.Neuroscience118 , 571–576 (2003).
  • Champagne DL . Bagot RC. van Hasselt F et al.: Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci.28 , 6037–6045 (2008).
  • Bagot RC , van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joëls M: Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol. Learn. Mem.92(3) , 292–300 (2009).
  • Smit-Rigter LA , ChampagneDL, van Hooft JA: Dendritic structure and function of cortical layer 2/3 pyramidal neurons in rat offspring. PLoS ONE4 , e5167 (2009).
  • Malenka RC , NicollRA: NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms.Trends Neurosci.16 , 521–527 (1993).
  • Bear MF , MalenkaRC: Synaptic plasticity: LTP and LTD.Curr. Opin. Neurobiol.4 , 389–399 (1994).
  • Morris RG , FreyU: Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience?Philos. Trans. R. Soc. Lond., B, Biol. Sci.352 , 1489–1503 (1997).
  • Ali DW , SalterMW: NMDA receptor regulation by Src kinase signaling in excitatory synaptic transmission and plasticity.Curr. Opin. Neurobiol.11 , 336–342 (2001).
  • Alberini CM , GhirardiM, HuangYY, NguyenPV, KandelER: A molecular switch for the consolidation of long-term memory: cAMP-inducible gene expression.Ann. NY Acad. Sci.758 , 261–286 (1995).
  • Kandel ER : The molecular biology of memory storage: a dialogue between genes and synapses.Science294 , 1030–1038 (2001).
  • Lynch MA : Long-term potentiation and memory.Physiol. Rev.84 , 87–136 (2004).
  • Alarcon JM , MalleretG, TouzaniK et 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 , 947–959 (2004).
  • Lubin FD , RothTL, SweattJD: Epigenetic regulation of bdnf gene transcription in the consolidation of fear memory.J. Neurosci.28 , 10576–10586 (2008).
  • Miller CA , SweattJD: Covalent modification of DNA regulates memory formation.Neuron53 , 857–869 (2007).
  • 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 , 1286–1292 (2004).
  • Bredy TW , WuH, CregoC, ZellhoeferJ, SunYE, BaradM: Histone modifications around individual BDNF gene promoters in prefrontalcortex are associated with extinction of conditioned fear.Learn. Mem.14 , 268–276 (2007).
  • Oike Y , HataA, MamiyaT et al.: Truncated CBP protein leads to classical Rubinstein–Taybi syndrome phenotypes in mice: implications for a dominant-negative mechanism.Hum. Mol. Genet.8 , 387–396 (1999).
  • Bourtchouladze R , LidgeR, CatapanoR et al.: A mouse model of Rubinstein–Taybi syndrome: defective long-term memory isameliorated by inhibitors of phosphodiesterase 4.Proc. Natl Acad. Sci. USA100 , 10518–10522 (2003).
  • Korzus E , RosenfeldMG, MayfordM: CBP histone acetyltransferase activity is a critical component of memory consolidation.Neuron42 , 961–972 (2004).
  • Wood MA , AttnerMA, OliveiraAM, BrindlePK, AbelT: A transcription factor-binding domain of the co-activator CBP is essential for long-term memory and the expression of specific target genes.Learn. Mem.13 , 609–617 (2006).
  • Vecsey CG , HawkJD, LattalKM et al.: Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB: CBP-dependent transcriptional activation.J. Neurosci.27 , 6128–6140 (2007).
  • Petrij F , GilesRH, DauwerseHG et al.: Rubinstein–Taybi syndrome caused by mutations in the transcriptional co-activator CBP.Nature376 , 348–351 (1995).
  • Levenson JM , SweattJD: Epigenetic mechanisms in memory formation.Nat. Rev. Neurosci.6 , 108–118 (2005).
  • Guan Z , GiustettoM, LomvardasS et al.: Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure.Cell111 , 483–493 (2002).
  • Miller CA , CampbellSL, SweattJD: DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity.Neurobiol. Learn. Mem.89 , 599–603 (2008).
  • West AE , ChenWG, DalvaMB et al.: Calcium regulation of neuronal gene expression.Proc. Natl Acad. Sci. USA.98 , 11024–11031 (2001).
  • Timmusk T , PalmK, MetsisM et al.: Multiple promoters direct tissue-specific expression of the rat BDNF gene.Neuron10 , 475–479 (1993).
  • Zoghbi HY : Postnatal neurodevelopmental disorders: meeting at the synapse?Science302 , 826–830 (2003).
  • Zhou Z , HongEJ, CohenS et al.: Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation.Neuron52 , 255–269 (2006).
  • Chen WG , ChangQ, LinY et al.: Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2.Science302 , 793–795 (2003).
  • Kishi N , MacklisJD: MECP2 is progressively expressed in post-migratory neurons and is involved in neuronal maturation rather than cell fate decisions.Mol. Cell. Neurosci.27 , 306–321 (2004).
  • Moretti P , LevensonJM, BattagliaF et al.: Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome.J. Neurosci.26 , 319–327 (2006).
  • Asaka Y , JugloffDG, ZhangL, EubanksJH, FitzsimondsRM: Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome.Neurobiol. Dis.21 , 217–227 (2006).
  • Nelson ED , KavalaliET, MonteggiaLM: MeCP2-dependent transcriptional repression regulates excitatory neurotransmission.Curr. Biol.16 , 710–716 (2006).
  • Pelka GJ , WatsonCM, RadziewicT et al.: Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice.Brain129 , 887–898 (2006).
  • Linnarsson S , BjörklundA, ErnforsP: Learning deficit in BDNF mutant mice.Eur. J. Neurosci.9 , 2581–2587 (1997).
  • Hall J , ThomasKL, EverittBJ: Rapid and selective induction of BDNF expression in the hippocampus during contextual learning.Nat. Neurosci.3 , 533–535 (2000).
  • Maren S , QuirkGJ: Neuronal signaling of fear memory.Nat. Rev. Neurosci.5 , 844–852 (2000).
  • Roceri M , CirulliF, PessinaC, PerettoP, RacagniG, RivaMA: Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions.Biol. Psychiatry55 , 708–714 (2004).
  • Roceri M , HendriksW, RacagniG, EllenbroekBA, RivaMA: Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus.Mol. Psychiatry7 , 609–616 (2002).
  • Branchi I , D‘AndreaI, FioreM, Di Fausto V, Aloe L, Alleva E: Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol. Psychiatry60 , 690–696 (2006).
  • Greisen MH , AltarCA, BolwigTG, WhiteheadR, WortweinG: Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats.Trends Genet.22 , 347–350 (2006).
  • Roth TL , LubinFD, FunkAJ, SweattJD: Lasting epigenetic influence of early-life adversity on the BDNF gene.Biol. Psychiatry65 , 760–769 (2009).
  • Hensch TK : Recovery in the blink of an eye, Neuron 48, 166–168 (2005).
  • Knudsen EI : Sensitive periods in the development of the brain and behaviorJ. Cogn. Neurosci.16 , 1412–1425 (2004).
  • Hooks BM , ChenC: Critical periods in the visual system: changing views for a model of experience-dependent plasticity.Neuron56 , 312–326 (2007).
  • Hensch TK : Critical period regulation.Ann. Rev. Neurosci.27 , 549–579 (2004).
  • Daw N : Visual Development. Plenum Press, NY, USA (1995).
  • O‘Leary DDM , RuffNL, DyckRH: Development, critical period plasticity, and adult reorganizations of mammalian somatosensory system.Curr. Opin. Neurobiol.4 , 535–544 (1994).
  • Fox K , SchlaggarBL, GlazewskiS, O‘LearyDDM: Glutamate receptor blockade at cortical synapses disrupts development of thalamocortical and columnar organization in somatosensory cortex.Proc. Natl Acad. Sci. USA93 , 5584–5589 (1996).
  • Van der Loos H , WoolseyTA: Somatosensory cortex: structural alterations following early injury to sense organs.Science179 , 395–398 (1973).
  • Iwasato T , DatwaniA, WolfAM et al.: Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex.Nature406 , 726–731 (2000).
  • Chang EF , MerzenichMM: Environmental noise retards auditory cortical development.Science300 , 498–502 (2003).
  • Lenneberg EH : Biological Foundations of Language. Wiley, NY, USA (1967).
  • Wiesel TN , HubelDH: Single-cell responses in striate cortex of kittens deprived of vision in one eye.J. Neurophysiol.26 , 1003–1017.
  • Prusky GT , DouglasRM: Developmental plasticity of mouse visual acuity.Eur. J. Neurosci.17 , 167–173 (2003).
  • Ossipow V , PellissierF, SchaadO, BallivetM: Gene expression analysis of the critical period in the visual cortex.Mol. Cell. Neurosci.27 , 70–83 (2004).
  • Majdan M , ShatzCJ: Effects of visual experience on activity-dependent gene regulation in cortex.Nat. Neurosci.9 , 650–659 (2006).
  • Tropea D , KreimanG, LyckmanA, MukherjeeS, YuH, HorngS, SurM: Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex.Nat. Neurosci.9 , 660–668 (2006).
  • Crosio C , CermakianN, AllisCD, Sassone-CorsiP: Light induces chromatin modification in cells of the mammalian circadian clock.Nat. Neurosci.3 , 1241–1247 (2000).
  • Korzus E , RosenfeldMG, MayfordM: CBP histone acetyltransferase activity is a critical component of memory consolidation.Neuron42 , 961–972 (2004).
  • Huang YF , 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 , 8422–8428 (2002).
  • Sng JCG , TaniuraH, YonedaY: Histone modifications in kainite induced status epilepticus.Eur. J. Neurosci.23 , 1269–1282 (2006).
  • Putignano E , LonettiG, CanceddaL et al.: Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity.Neuron53 , 747–759 (2007).
  • Pham TA , GrahamSJ, SuzukiS et al.: A semi-persistent adult ocular dominance plasticity in visual cortex is stabilized by activated CREB.Learn. Mem.11 , 738–747 (2004).
  • Sawtell NB , FrenkelMY, PhilpotBD, NakazawaK, TonegawaS, BearMF: NMDA receptor-dependent ocular dominance plasticity in adult visual cortex.Neuron38 , 977–985 (2003).
  • Pizzorusso T , MediniP, BerardiN et al.: Reactivation of ocular dominance plasticity in the adult visual cortex.Science298 , 1248–1251 (2002).
  • Pizzorusso T , MediniP, LandiS, BaldiniS, BerardiN, MaffeiL: Structural and functional recovery from early monocular deprivation in adult rats.Proc. Natl Acad. Sci. USA103 , 8517–8522 (2006).
  • Cancedda L , PutignanoE, SaleA, ViegiA, BerardiN, MaffeiL: Acceleration of visual system development by environmental enrichment.J. Neurosci.24 , 4840–4848 (2004).
  • van Praag H , KempermannG, GageFH: Neural consequences of environmental enrichment.Nat. Rev. Neurosci.1 , 191–198 (2002).
  • Nithianantharajah J , HannanAJ: Dynamic mutations as digital genetic modulators of brain development, function and dysfunction.Bioessays29 , 525–535 (2007).
  • Galimberti I , GogollaN, AlberiS, SantosAF, MullerD, CaroniP: Long-term rearrangements of hippocampal mossy fiber terminal connectivity in the adult regulated by experience.Neuron50 , 749–763 (2006).
  • Guan J -S, Haggarty SJ, Giacometti E et al.: HDAC2 negatively regulates memory formation and synaptic plasticity. Nature459 , 55–60 (2009).
  • Benes FM , BerrettaS: GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder.Neuropsychopharmacology25 , 1–27 (2001).
  • Fatemi SH , EarleJA, McMenomyT: Reduction in reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression.Mol. Psychiatry5 , 654–663 (2000).
  • Guidotti A , AutaJ, DavisJM et al.: Decrease in reelin and glutamic acid67 (GAD67) expression in schizophrenia and bipolar disorder.Arch. Gen. Psychiatry57 , 1061–1069 (2000).
  • Eastwood SL , HarrisonPJ: Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis.Mol. Psychiatry769 , 821–831 (2003).
  • Torrey EF , BarciBM, WebsterMJ, BartkoJJ, Meador-WoodruffJH, KnableMB: Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains.Biol. Psychiatry57 , 252–260 (2005).
  • Costa E , DavisJM, DongE et al.: A GABAergic cortical deficit dominates schizophrenia pathophysiology.Crit. Rev. Neurobiol.16 , 1–23 (2004).
  • Akbarian S , HuangHS: Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders.Brain Res. Brain Res. Rev.52 , 293–304 (2006).
  • Lewis DA , HashimotoT, VolkDW: Cortical inhibitory neurons and schizophrenia.Nat. Rev. Neurosci.6 , 312–324 (2005).
  • Straub RE , LipskaBK, EganMF, GoldbergTE, KleinmanJE: Allelic variation in GAD1 (GAD67) is associated with schizophrenia and influences cortical function and gene expression.Mol. Psychiatry10 , 1038 (2007).
  • Abdolmaleky HM , ChengK, RussoA et al.: Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: a preliminary report.Am. J. Med. Genet. B Neuropsychiatry Genet.134 , 60–66 (2005).
  • Grayson DR , JiaX, ChenY et al.: Reelin promoter hypermethylation in schizophrenia.Proc. Natl Acad. Sci. USA102 , 9341–9346 (2005).
  • Huang HS , MatevossianA, WhittleC et al.: Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters.J. Neurosci.27 , 11254–11262 (2007).
  • Mill J , TangT, KaminskyZ et al.: Epigenomic profiling reveals DNA-methylation changes associated with major psychosis.Am. J. Hum. Genet.82 , 696–711 (2008).
  • Kundakovic M , ChenY, CostaE, GraysonDR: DNA methyltransferase inhibitors coordinately induce expression of the human reelin and glutamic acid decarboxylase 67 genes.Mol. Pharmacol.71 , 644–653 (2007).
  • Veldic M , CarunchoHJ, LiuS et al.: DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains.Proc. Natl Acad. Sci. USA101 , 348–353 (2004).
  • Ruzicka WB , ZhubiA, VeldicM, GraysonDR, CostaE, GuidottiA: Selective epigenetic alteration of layer I GABAergic neurons isolated from prefrontal cortex of schizophrenia patients using laser-assisted microdissection.Mol. Psychiatry12 , 385–397 (2007).
  • Selker EU : Trichostatin A causes selective loss of DNA methylation in Neurospora.Proc. Natl Acad. Sci. USA95 , 9430–9435 (1998).
  • McGowan PO , SasakiA, DymovS, TureckiG, SzyfM, MeaneyMJ: Differential methylation of a neuron-enriched glucocorticoid receptor gene promoter in human hippocampus is associated with early child trauma and adult psychopathology.Nat. Neurosci.12 , 342–348 (2009).
  • McGirr A , RenaudJ, SeguinM, AldaM, TureckiG: Course of major depressive disorder and suicide outcome: a psychological autopsy study.J. Clin. Psychiatry69 , 966–970 (2008).
  • Turner JD , MullerCP: Structure of the glucocorticoid receptor (NR3C1) gene 5´untranslated region: identification and tissue distribution of multiple new human exon 1.J. Mol. Endocrinol.35 , 283–292 (2005).
  • Heim C , NewportDJ, HeitS et al.: Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood.JAMA284 , 592–597 (2009).
  • Jiang Y , LangleyB, LubinFD et al.: Epigenetics in the nervous system.J. Neurosci.28 , 11753–11759 (2008).
  • Akbarian S , HuangHS: Epigenetic regulation in human brain-focus on histone lysine methylation.Biol. Psychiatry65 , 198–203 (2009).
  • Renthal W , NestlerEJ: Epigenetic mechanisms in drug addiction.Trends Mol. Med.14 , 34150 (2008).
  • Nestler EJ : Epigenetic mechanisms in psychiatry.Biol. Psychiatry65 , 189–190 (2009).
  • Poulter MO , DuL, WeaverIC et al.: GABAA receptor promoter hypermethylation in suicide brain: implications for the involvement of epigenetic processes.Biol. Psychiatry64 , 645–652 (2006).
  • McGowan PO , SasakiA, HuangTC et al.: Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain.PLoS ONE3 , e2085 (2008).
  • Kumar A , ChoiKH, RenthalW et al.: Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum.Neuron48 , 303–314 (2005).
  • Renthal W , KumarA, XiaoG et al.: Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins.Neuron62 , 335–348 (2009).
  • Kalivas PW , StewartJ: Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity.Brain Res. Brain Res. Rev.16 , 223–244 (1991).
  • Bushati N , CohenSM: MicroRNA functions.Annu. Rev. Cell. Dev. Biol.23 , 175–205 (2007).
  • Kosic KS : The neuronal microRNA system.Nat. Rev. Neurosci.7 , 911–920 (2006).
  • Schratt GM , TuebingF, NighEA et al.: A brain-specific microRNA regulates dendritic spine development.Nature439 , 283–289 (2006).
  • Kocerha J , FaghihiMA, Lopez-ToedanoMA et al.: MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction.Proc. Natl Acad. Sci. USA.106 , 3507–3512 (2009).
  • Mercer TR , DingerME, MarianiJ, KosikKS, MehlerMF, MattickJS: Noncoding RNAs in long-term memory formation.Neuroscientist14 , 434–444 (2008).
  • Yoo AS , StaahlBT, Chen Lei, Crabtree GR: MicroRNA-mediated switching of chromatin-remodeling complexes in neural development. Nature460 , 642–646 (2009).
  • Li X , CassidyJJ, ReinkeCA, FischboeckS, CarthewRW: A microRNA imparts robustness against environmental fluctuation during development.Cell137 , 273–282 (2009).
  • Blakaj A , LinH: Piecing together the mosaic of early mammalian development through microRNAs.J. Biol. Chem.283 , 9505–9508 (2008).
  • Makeyev EV , ZhangJ, CarrascoMA, ManiatisT: The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing.Mol. Cell27 , 435–448 (2007).
  • Schratt G : Fine-tuning neural gene expression with microRNAs.Curr. Opin. Neurobiol.19 , 213–219 (2009).
  • Ashraf SI , McLoonAL, SclarsicSM, KunesS: Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila.Cell124 , 191–205 (2006).
  • Giraldez AJ , CinalliRM, GlasnerME et al.: MicroRNAs regulate brain morphogenesis in zebrafish.Science308 , 833–838 (2005).
  • Choi PS , ZakharyL, ChoiWY et al.: Members of the miRNA-200 family regulate olfactory neurogenesis.Neuron57 , 41–55 (2008).
  • Conaco C , OttoS, HanJJ, MandelG: Reciprocal actions of REST and a microRNA promote neuronal identity.Proc. Natl Acad. Sci. USA103 , 2422–2427 (2006).
  • Seigel G , ObernostererG, Roberto Fiore R et al.: A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol.11 , 705–716 (2009).
  • Sokolowski MB : Drosophila: genetics meets behaviour.Nat. Rev. Genet.2 , 879–890 (2001).
  • Sokolowski MB , WahlstenD: Gene–environment interaction and complex behavior. In: Methods in genomic neuroscience. Moldin SO, Boca Raton FL (Eds), CRC Press, FL, USA, 3–27 (2001).
  • Hebb DO : A Textbook in Psychology. Saunders, PA, USA (1958).
  • Gehring M , ReikW, HenikoffS: DNA demethylation by DNA repair.Trends Genet.25 , 82–90 (2009).
  • Reik W , DeanJW: Epigenetic reprogramming in mammalian development.Science293 , 1089–1093 (2001).
  • Kangaspeska S , StrideB, MétivierR et al.: Transient cyclical methylation of promoter DNA.Nature452 , 112–115 (2008).
  • Metivier R , GallaisC, TiffocheC et al.: Cyclical DNA methylation of a transcriptionally active promoter.Nature452 , 45–50 (2008).
  • Ma DK , Jang M-H, Guo JU et al.: Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science323 , 1074–1077 (2009).
  • Barreto G , SchaferA, MarholdJ et al.: Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation.Nature445 , 671–675 (2007).
  • Wu H , SunYE: Reversing DNA methylation: new insights from neuronal activity inducedgadd45b in adult neurogenesis.Sci. Signal.2 , pe17 (2009).
  • Rai K , HugginsIJ, JamesSR, KarpfAR, JonesDA, CairnsBR: DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45.Cell135 , 1201–1212 (2008).
  • Weber M , HellmannI, StadlerMB et al.: Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome.Nat. Genet.39 , 457–466 (2007).

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.