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Review

Sex Differences in Brain Epigenetics

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Pages 807-821 | Published online: 15 Dec 2010

Bibliography

  • Zucker I , BeeryAK: Males still dominate animal studies.Nature465(7299) , 690 (2010).
  • Kim AM , TingenCM, WoodruffTK: Sex bias in trials and treatment must end.Nature465(7299) , 688–689 (2010).
  • Holden C : Women abound in NIH trials.Science322(5899) , 219 (2008).
  • Gillies GE , McArthurS: Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines.Pharmacol. Rev.62(2) , 155–198 (2010).
  • Anderson GD : Sex and racial differences in pharmacological response: where is the evidence? Pharmacogenetics, pharmacokinetics, and pharmacodynamics.J. Womens Health (Larchmt.)14(1) , 19–29 (2005).
  • Arnold AP , XuJ, GrishamW, ChenX, KimYH, ItohY: Minireview: sex chromosomes and brain sexual differentiation.Endocrinology145(3) , 1057–1062 (2004).
  • Negri-Cesi P , ColciagoA, PravettoniA, CasatiL, ContiL, CelottiF: Sexual differentiation of the rodent hypothalamus: hormonal and environmental influences.J. Steroid Biochem. Mol. Biol.109(3–5) , 294–299 (2008).
  • Roselli CE , AbdelgadirSE, ReskoJA: Regulation of aromatase gene expression in the adult rat brain.Brain Res. Bull.44(4) , 351–357 (1997).
  • Perez SE , ChenEY, MufsonEJ: Distribution of estrogen receptor α and β immunoreactive profiles in the postnatal rat brain.Brain Res. Dev. Brain Res.145(1) , 117–139 (2003).
  • Wilson ME , RosewellKL, KashonML, ShughruePJ, MerchenthalerI, WisePM: Age differentially influences estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) gene expression in specific regions of the rat brain.Mech. Ageing Dev.123(6) , 593–601 (2002).
  • Kühnemann S , BrownTJ, HochbergRB, MacLuskyNJ: Sex differences in the development of estrogen receptors in the rat brain.Horm. Behav.28(4) , 483–491 (1994).
  • Kudwa AE , MichopoulosV, GatewoodJD, RissmanEF: Roles of estrogen receptors α and β in differentiation of mouse sexual behavior.Neuroscience138(3) , 921–928 (2006).
  • Negri-Cesi P , PolettiA, CelottiF: Metabolism of steroids in the brain: a new insight into the role of 5α-reductase and aromatase in brain differentiation and functions.J. Steroid Biochem. Mol. Biol.58(5–6) , 455–466 (1996).
  • Amateau SK , AltJJ, StampsCL, McCarthyMM: Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon.Endocrinology145(6) , 2906–2917 (2004).
  • Poletti A , Negri-CesiP, MelcangiRC, ColciagoA, MartiniL, CelottiF: Expression of androgen-activating enzymes in cultured cells of developing rat brain.J. Neurochem.68(3) , 1298–1303 (1997).
  • Ribeiro CM , PereiraOC: 5α-reductase 2 inhibition impairs brain defeminization of male rats: reproductive aspects.Pharmacol. Biochem. Behav.82(1) , 228–235 (2005).
  • Goto K , KoizumiK, OhtaY et al.: Evaluation of general behavior, memory, learning performance, and brain sexual differentiation in F1 offspring males of rats treated with flutamide during late gestation.J. Toxicol. Sci.30(3) , 249–259 (2005).
  • Sato T , MatsumotoT, KawanoH et al.: Brain masculinization requires androgen receptor function.Proc. Natl Acad. Sci. USA101(6) , 1673–1678 (2004).
  • Quadros PS , WagnerCK: Regulation of progesterone receptor expression by estradiol is dependent on age, sex and region in the rat brain.Endocrinology149(6) , 3054–3061 (2008).
  • Weisz J , WardIL: Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring.Endocrinology106(1) , 306–316 (1980).
  • Quadros PS , PfauJL, GoldsteinAY, De Vries GJ, Wagner CK: Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Endocrinology143(10) , 3727–3739 (2002).
  • Wagner CK : Progesterone receptors and neural development: a gap between bench and bedside?Endocrinology149(6) , 2743–2749 (2008).
  • McCarthy MM , AugerAP, BaleTL et al.: The epigenetics of sex differences in the brain.J. Neurosci.29(41) , 12815–12823 (2009).
  • Jaenisch R , BirdA: Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals.Nat. Genet.33(Suppl.) , 245–254 (2003).
  • Reik W : Stability and flexibility of epigenetic gene regulation in mammalian development.Nature447(7143) , 425–432 (2007).
  • Cardoso MC , LeonhardtH: DNA methyltransferase is actively retained in the cytoplasm during early development.J. Cell Biol.147(1) , 25–32 (1999).
  • Okano M , BellDW, HaberDA, LiE: DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development.Cell99(3) , 247–257 (1999).
  • J⊘rgensen HF , BirdA: MeCP2 and other methyl-CpG binding proteins.Ment. Retard. Dev. Disabil. Res. Rev.8(2) , 87–93 (2002).
  • Fuks F , BurgersWA, GodinN, KasaiM, KouzaridesT: DNMT3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription.EMBO J.20(10) , 2536–2544 (2001).
  • Westberry JM , TroutAL, WilsonME: Epigenetic regulation of estrogen receptor α gene expression in the mouse cortex during early postnatal development.Endocrinology151(2) , 731–740 (2010).
  • Schwarz JM , NugentBM, McCarthyMM: Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span.Endocrinology151(10) , 4871–4881 (2010).
  • Kurian JR , OlesenKM, AugerAP: Sex differences in epigenetic regulation of the estrogen receptor-α promoter within the developing preoptic area.Endocrinology151(5) , 2297–2305 (2010).
  • Wagner CK , PfauJL, De Vries GJ, Merchenthaler IJ: Sex differences in progesterone receptor immunoreactivity in neonatal mouse brain depend on estrogen receptor expression. J. Neurobiol.47 , 176–182 (2001).
  • Nugent BM , SchwarzJM, McCarthyMM: Hormonally mediated epigenetic changes to steroid receptors in the developing brain: Implications for sexual differentiation.Horm. Behav. DOI: 10.1016/j.yhbeh.2010.08.009 (2010) (Epub ahead of print).
  • Kumar RC , ThakurMK: Androgen receptor mRNA is inversely regulated by testosterone and estradiol in adult mouse brain.Neurobiol. Aging25(7) , 925–933 (2004).
  • Xiao Y , WordB, Starlard-DavenportA, HaefeleA, Lyn-CookBD, HammonsG: Age and gender affect DNMT3a and DNMT3b expression in human liver.Cell. Biol. Toxicol.24(3) , 265–272 (2008).
  • Galetzka D , WeisE, TralauT, SeidmannL, HaafT: Sex-specific windows for high mRNA expression of DNA methyltransferases 1 and 3a and methyl-CpG-binding domain proteins 2 and 4 in human fetal gonads.Mol. Reprod. Dev.74(2) , 233–241 (2007)
  • Yamagata Y , AsadaH, TamuraI: DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen.Hum. Reprod.24(5) , 1126–1132 (2009).
  • Zhao Z , FanL, FrickKM: Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation.Proc. Natl Acad. Sci. USA107(12) , 5605–5610 (2010).
  • McCarthy MM , AugerAP, BaleTL et al.: The epigenetics of sex differences in the brain.J. Neurosci.29(41) , 12815–12823 (2009).
  • Pathak S , D‘SouzaR, AnkolkarM, GaonkarR, BalasinorNH: Potential role of estrogen in regulation of the insulin-like growth factor2-H19 locus in the rat testis.Mol. Cell. Endocrinol.314(1) , 110–117 (2010).
  • Kurian JR , Forbes-LormanRM, AugerAP: Sex difference in MeCP2 expression during a critical period of rat brain development.Epigenetics2(3) , 173–178 (2007).
  • Kurian JR , BychowskiME, Forbes-LormanRM, AugerCJ, AugerAP: MeCP2 organizes juvenile social behavior in a sex-specific manner.J. Neurosci.28(28) , 7137–7142 (2008).
  • Koh SS , ChenD, LeeYH, StallcupMR: Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities.J. Biol. Chem.276(2) , 1089–1098 (2001).
  • Bousios S , KarandreaD, KittasC, KitrakiE: Effects of gender and stress on the regulation of steroid receptor coactivator-1 expression in the rat brain and pituitary.J. Steroid Biochem. Mol. Biol.78(5) , 401–407 (2001).
  • Auger AP , Perrot-SinalTS, AugerCJ, EkasLA, TetelMJ, MccarthyMM: Expression of the nuclear receptor coactivator, cAMP response element-binding protein, is sexually dimorphic and modulates sexual differentiation of neonatal rat brain.Endocrinology143(8) , 3009–3016 (2002).
  • Jessen HM , KolodkinMH, BychowskiME, AugerCJ, AugerAP: The nuclear receptor corepressor has organizational effects within the developing amygdala on juvenile social play and anxiety-like behavior.Endocrinology151(3) , 1212–1220 (2010).
  • Auger AP , TetelMJ, McCarthyMM: Steroid receptor coactivator-1 (SRC-1) mediates the development of sex-specific brain morphology and behavior.Proc. Natl Acad. Sci. USA97(13) , 7551–7555 (2000).
  • Rosenfeld MG , LunyakVV, GlassCK: Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response.Genes Dev.20(11) , 1405–1428 (2006).
  • Hsieh J , GageFH: Chromatin remodeling in neural development and plasticity.Curr. Opin. Cell Biol.17(6) , 664–671 (2005).
  • Gagnidze K , WeilZM, PfaffDW: Histone modifications proposed to regulate sexual differentiation of brain and behavior.Bioessays DOI: 10.1002/bies.201000064 (2010) (Epub ahead of print).
  • Tsai HW , GrantPA, RissmanEF: Sex differences in histone modifications in the neonatal mouse brain.Epigenetics4(1) , 47–53 (2009).
  • Murray EK , HienA, De Vries GJ, Forger NG: Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis. Endocrinology150(9) , 4241–4247 (2009).
  • Baum MJ : New evidence that an epigenetic mechanism mediates testosterone-dependent brain masculinization.Endocrinology150(9) , 3980–3982 (2009).
  • Jensen LR , AmendeM, GurokU: Mutations in the JARID1C gene, which is involved in transcriptional regulation and chromatin remodeling, cause X-linked mental retardation.Am. J. Hum. Genet.76(2) , 227–236 (2005).
  • Xu J , DengX, WatkinsR, DistecheCM: Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons.J. Neurosci.28(17) , 4521–4527 (2008).
  • Xu J , AndreassiM: Reversible histone methylation regulates brain gene expression and behavior.Horm. Behav. DOI: 10.1016/j.yhbeh.2010.08.019 (2010) (Epub ahead of print).
  • van Haaften G , DalglieshGL, DaviesH: Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer.Nat. Genet.41(5) , 521–523 (2009).
  • Bateson P , BarkerD, Clutton-BrockT et al.: Developmental plasticity and human health.Nature430(6998) , 419–421 (2004).
  • Gluckman PD , HansonMA, BatesonP et al.: Towards a new developmental synthesis: adaptive developmental plasticity and human disease.Lancet373(9675) , 1654–1657 (2009).
  • Ke X , LeiQ, JamesSJ et al.: Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats.Physiol. Genomics25(1) , 16–28 (2006).
  • Jarvis S , GlinianaiaSV, ArnaudC et al.: Case gender and severity in cerebral palsy varies with intrauterine growth.Arch. Dis. Child.90(5) , 474–479 (2005).
  • Stevenson DK , VerterJ, FanaroffAA et al.: Sex differences in outcomes of very low birthweight infants: the newborn male disadvantage.Arch. Dis. Child. Fetal Neonatal Ed.83(3) , F182–F185 (2000).
  • Champagne FA , WeaverIC, DiorioJ, DymovS, SzyfM, MeaneyMJ: Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring.Endocrinology147(6) , 2909–2915 (2006).
  • Murgatroyd C , PatchevAV, WuY et al.: Dynamic DNA methylation programs persistent adverse effects of early-life stress.Nat. Neurosci.12(12) , 1559–1566 (2009).
  • Binder EB , KünzelHE, NickelT et al.: HPA-axis regulation at in-patient admission is associated with antidepressant therapy outcome in male but not in female depressed patients.Psychoneuroendocrinology34(1) , 99–109 (2009).
  • Nolen-Hoeksema S , GirgusJS: The emergence of gender differences in depression during adolescence.Psychol. Bull.115(3) , 424–443 (1994).
  • Swarr AE , RichardsMH: Longitudinal effects of adolescent girls‘ pubertal development, perceptions of pubertal timing, and parental relations of eating problems.Dev. Psychol.32 , 636–646 (1996).
  • Ge X , CongerRD, ElderGH: Pubertal transition, stressful life events, and the emergence of gender differences in adolescent depressive symptoms.Dev. Psychol.37 , 404–417 (2001).
  • Mill J , TangT, KaminskyZ et al.: Epigenomic profiling reveals DNA-methylation changes associated with major psychosis.Am. J. Hum. Genet.82(3) , 696–711 (2008).
  • Akbarian S , KimJJ, PotkinSG et al.: Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics.Arch. Gen. Psychiatry52(4) , 258–266 (1995).
  • Heckers S , StoneD, WalshJ, ShickJ, KoulP, BenesFM: Differential hippocampal expression of glutamic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia.Arch. Gen. Psychiatry59(6) , 521–529 (2002).
  • 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(42) , 11254–11262 (2007).
  • Westberry JM , PrewittAK, WilsonME: Epigenetic regulation of the estrogen receptor α promoter in the cerebral cortex following ischemia in male and female rats.Neuroscience152(4) , 982–989 (2008).
  • Seeman MV : Psychopathology in women and men: focus on female hormones.Am. J. Psychiatry154(12) , 1641–1647 (1997).
  • Mani ST , ThakurMK: In the cerebral cortex of female and male mice, amyloid precursor protein (APP) promoter methylation is higher in females and differentially regulated by sex steroids.Brain Res.1067(1) , 43–47 (2006).
  • Zhou L , ChengX, ConnollyBA, DickmanMJ, HurdPJ, HornbyDP: Zebularine: a novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases.J. Mol. Biol.321(4) , 591–599 (2002).
  • Drummond DC , NobleCO, KirpotinDB, GuoZ, ScottGK, BenzCC: Clinical development of histone deacetylase inhibitors as anticancer agents.Annu. Rev. Pharmacol. Toxicol.45 , 495–528 (2005).
  • McGowan PO , MeaneyMJ, SzyfM: Diet and the epigenetic (re)programming of phenotypic differences in behavior.Brain Res.1237 , 12–24 (2008).
  • 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).
  • Schroeder FA , LinCL, CrusioWE, AkbarianS: Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse.Biol. Psychiatry62(1) , 55–64 (2007).
  • Covington HE 3rd, Maze I, Laplant QC et al.: Antidepressant actions of histone deacetylase inhibitors. J. Neurosci.29(37) , 11451–11460 (2009).
  • Szyf M , WeaverIC, ChampagneFA, DiorioJ, MeaneyMJ: Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat.Front. Neuroendocrinol.26(3–4) , 139–162 (2005).
  • Weaver IC , CervoniN, ChampagneFA et al.: Epigenetic programming by maternal behavior.Nat. Neurosci.7(8) , 847–854 (2004).
  • Papakostas GI : Evidence for S-adenosyl-L-methionine (SAM-e) for the treatment of major depressive disorder.J. Clin. Psychiatry70(Suppl. 5) , 18–22 (2009).
  • Coppen A , Bolander-GouailleC: Treatment of depression: time to consider folic acid and vitamin B12.J. Psychopharmacol.19(1) , 59–65 (2005).
  • Taylor MJ , CarneySM, GoodwinGM, GeddesJR: Folate for depressive disorders: systematic review and meta-analysis of randomized controlled trials.J. Psychopharmacol.18(2) , 251–256 (2004).
  • Pogribny IP , JamesSJ, JerniganS, PogribnaM: Genomic hypomethylation is specific for preneoplastic liver in folate/methyl deficient rats and does not occur in non-target tissues.Mutat. Res.548(1–2) , 53–59 (2004).
  • Weaver IC , 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(47) , 11045–11054 (2005).
  • Weaver IC , MeaneyMJ, SzyfM: Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood.Proc. Natl Acad. Sci. USA103(9) , 3480–3485 (2006).
  • Bottiglieri T : S-adenosyl-L-methionine (SAMe): from the bench to the bedside – molecular basis of a pleiotrophic molecule.Am. J. Clin. Nutr.76(5) , 1151–1157 (2002).
  • Eden A , GaudetF, WaghmareA, JaenischR: Chromosomal instability and tumors promoted by DNA hypomethylation.Science300(5618) , 455 (2003).
  • Brueckner B , Garcia Boy R, Siedlecki P et al.: Epigenetic reactivation of tumor suppressor genes by a novel small-molecule inhibitor of human DNA methyltransferases. Cancer Res.65(14) , 6305–6311 (2005).
  • Perisic T , ZimmermannN, KirmeierT et al.: Valproate and amitriptyline exert common and divergent influences on global and gene promoter-specific chromatin modifications in rat primary astrocytes.Neuropsychopharmacology35(3) , 792–805 (2010).
  • Cassel S , CarougeD, GensburgerC et al.: Fluoxetine and cocaine induce the epigenetic factors MeCP2 and MBD1 in adult rat brain.Mol. Pharmacol.70(2) , 487–492 (2006).
  • Hunter RG , McCarthyKJ, MilneTA, PfaffDW, McEwenBS: Regulation of hippocampal H3 histone methylation by acute and chronic stress.Proc. Natl Acad. Sci. USA106(49) , 20912–20917 (2009).
  • Göttlicher M , MinucciS, ZhuP et al.: Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells.EMBO J.20(24) , 6969–6978 (2001).
  • Fukagawa NK , MartinJM, WurthmannA, PrueAH, EbensteinD, O‘RourkeB: Sex-related differences in methionine metabolism and plasma homocysteine concentrations.Am. J. Clin. Nutr.72(1) , 22–29 (2000).

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