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Review

The Lasting Legacy of Social Stress on the Epigenome of the Hypothalamic–Pituitary–Adrenal Axis

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Pages 431-444 | Published online: 24 Aug 2012

References

  • Fox SE , LevittP, NelsonCA. How the timing and quality of early experiences influence the development of brain architecture. Child Dev.81(1) , 28–40 (2010).
  • Shonkoff JP . From neurons to neighborhoods: old and new challenges for developmental and behavioral pediatrics. J. Dev. Behav. Pediatr.24(1) , 70–76 (2003).
  • Edwards VJ , HoldenGW, FelittiVJ, AndaRF. Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse childhood experiences study. Am. J. Psychiatry160(8) , 1453–1460 (2003).
  • Green JG , McLaughlinKA, BerglundPA et al. Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Arch. Gen. Psychiatry 67(2) , 113–123 (2010).
  • McLaughlin KA , GreenJG, GruberMJ, SampsonNA, ZaslavskyAM, KesslerRC. Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: associations with persistence of DSM-IV disorders. Arch. Gen. Psychiatry67(2) , 124–132 (2010).
  • de Kloet ER , JoëlsM, HolsboerF. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci.6(6) , 463–475 (2005).
  • Loman MM , GunnarMR. Early experience and the development of stress reactivity and regulation in children. Neurosci. Biobehav. Rev.34(6) , 867–876 (2010).
  • Lupien SJ , McEwenBS, GunnarMR, HeimC. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci.10(6) , 434–445 (2009).
  • Heim C , ShugartM, CraigheadWE, NemeroffCB. Neurobiological and psychiatric consequences of child abuse and neglect. Dev. Psychobiol.52(7) , 671–690 (2010).
  • Gluckman PD , HansonMA, CooperC, ThornburgKL. Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med.359(1) , 61–73 (2008).
  • Spork P . Der Zweite Code: EPIGENETIK oder: Wie wir unser Erbgut steuern können. Rowohlt Verlag GmbH, Hamburg, Berlin (2009).
  • Field T . Postpartum depression effects on early interactions, parenting, and safety practices: a review. Infant. Behav. Dev.33(1) , 1–6 (2010).
  • Allis CD , JenuweinT and Reinberg D (Eds).Epigenetics. Cold Spring Harbor Laboratory Press, NY, USA (2007).
  • Bird A . DNA methylation patterns and epigenetic memory. Genes Dev.16(1) , 6–21 (2002).
  • Probst AV , DunleavyE, AlmouzniG. Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell. Biol.10(3) , 192–206 (2009).
  • Kareta MS , BotelloZM, EnnisJJ, ChouC, ChédinF. Reconstitution and mechanism of the stimulation of de novo methylation by human DNMT3L. J. Biol. Chem.281(36) , 25893–25902 (2006).
  • Lehnertz B , UedaY, DerijckAA et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13(14) , 1192–1200 (2003).
  • Viré E , BrennerC, DeplusR et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439(7078) , 871–874 (2006).
  • Tachibana M , SugimotoK, NozakiM et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16(14) , 1779–1791 (2002).
  • Fuks F , HurdPJ, DeplusR, KouzaridesT. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res.31(9) , 2305–2312 (2003).
  • Ooi SKT , QiuC, BernsteinE et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448(7154) , 714–717 (2007).
  • Ruthenburg AJ , AllisCD, WysockaJ. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell25(1) , 15–30 (2007).
  • Jeong S , LiangG, SharmaS et al. Selective anchoring of DNA methyltransferases 3A and 3B to nucleosomes containing methylated DNA. Mol. Cell. Biol. 29(19) , 5366–5376 (2009).
  • Chodavarapu RK , FengS, BernatavichuteYV et al. Relationship between nucleosome positioning and DNA methylation. Nature 466(7304) , 388–392 (2010).
  • Saxonov S , BergP, BrutlagDL. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl Acad. Sci. USA103(5) , 1412–1417 (2006).
  • Weber M , HellmannI, StadlerMB et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 39(4) , 457–466 (2007).
  • Lister R , PelizzolaM, DowenRH et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462(7271) , 315–322 (2009).
  • Zemach A , McDanielIE, SilvaP, ZilbermanD. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science328(5980) , 916–919 (2010).
  • Feng S , CokusSJ, ZhangX et al. Conservation and divergence of methylation patterning in plants and animals. Proc. Natl Acad. Sci. USA 107(19) , 8689–8694 (2010).
  • Maunakea AK , NagarajanRP, BilenkyM et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466(7303) , 253–257 (2010).
  • Stadler MB , MurrR, BurgerL et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480(7378) , 490–495 (2011).
  • Ooi SKT , BestorTH. The colorful history of active DNA demethylation. Cell133(7) , 1145–1148 (2008).
  • Wu SC , ZhangY. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell. Biol.11(9) , 607–620 (2010).
  • Guo JU , SuY, ZhongC, MingG, SongH. Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond. Cell Cycle10(16) , 2662–2668 (2011).
  • Guo JU , MaDK, MoH et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat. Neurosci. 14(10) , 1345–1351 (2011).
  • Yildirim O , LiR, HungJ et al. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 147(7) , 1498–1510 (2011).
  • Griffith JS , MahlerHR. DNA ticketing theory of memory. Nature223(5206) , 580–582 (1969).
  • Holliday R . Is there an epigenetic component in long-term memory? J. Theor. Biol.200(3) , 339–341 (1999).
  • Levine S . Infantile experience and resistance to physiological stress. Science126(3270) , 405 (1957).
  • Meaney MJ , SzyfM. Maternal care as a model for experience-dependent chromatin plasticity? Trends Neurosci.28(9) , 456–463 (2005).
  • Weaver IC , CervoniN, ChampagneFA et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7(8) , 847–854 (2004).
  • Deaton AM , BirdA. CpG islands and the regulation of transcription. Genes Dev.25(10) , 1010–1022 (2011).
  • Klose RJ , BirdAP. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci.31(2) , 89–97 (2006).
  • McGowan PO , SudermanM, SasakiA et al. Broad epigenetic signature of maternal care in the brain of adult rats. PLoS ONE 6(2) , e14739 (2011).
  • McGowan PO , SasakiA, D‘AlessioAC et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12(3) , 342–348 (2009).
  • Talge NM , NealC, GloverV. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J. Child Psychol. Psychiatry48(3–4) , 245–261 (2007).
  • Holsboer F . The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology23(5) , 477–501 (2000).
  • Markham JA , KoenigJI. Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology (Berl.)214(1) , 89–106 (2011).
  • Oberlander TF , WeinbergJ, PapsdorfM, GrunauR, MisriS, DevlinAM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics3(2) , 97–106 (2008).
  • Radtke KM , RufM, GunterHM et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl. Psychiatry 1 , E21 (2011).
  • Perroud N , Paoloni-GiacobinoA, PradaE et al. Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma. Transl. Psychiatry 1 , E59 (2011).
  • Tyrka AR , PriceLH, MarsitC, WaltersOC, CarpenterLL. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS ONE7(1) , e30148 (2012).
  • Moser D , MolitorA, KumstaR, TatschnerT, RiedererP, MeyerJ. The glucocorticoid receptor gene exon 1-F promoter is not methylated at the NGFI-A binding site in human hippocampus. World J. Biol. Psychiatry8(4) , 262–268 (2007).
  • Alt SR , TurnerJD, KlokMD et al. Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology 35(4) , 544–556 (2010).
  • Storer CL , DickeyCA, GalignianaMD, ReinT, CoxMB. FKBP51 and FKBP52 in signaling and disease. Trends Endocrinol. Metab.22(12) , 481–490 (2011).
  • Lee RS , TamashiroKLK, YangX et al. Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinology 151(9) , 4332–4343 (2010).
  • Wiench M , JohnS, BaekS et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO J. 30(15) , 3028–3039 (2011).
  • Lee RS , TamashiroKLK, YangX et al. A measure of glucocorticoid load provided by DNA methylation of Fkbp5 in mice. Psychopharmacology (Berl.) 218(1) , 303–312 (2011).
  • Smith MA , MakinoS, KvetnanskyR, PostRM. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci.15(3 Pt 1) , 1768–1777 (1995).
  • Schaaf MJ , de Kloet ER, Vreugdenhil E. Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation. Stress3(3) , 201–208 (2000).
  • Hansson AC , SommerW, RimondiniR, AndbjerB, StrömbergI, FuxeK. c-fos reduces corticosterone-mediated effects on neurotrophic factor expression in the rat hippocampal CA1 region. J. Neurosci.23(14) , 6013–6022 (2003).
  • Hansson AC , SommerWH, MetsisM, StrömbergI, AgnatiLF, FuxeK. Corticosterone actions on the hippocampal brain-derived neurotrophic factor expression are mediated by exon IV promoter. J. Neuroendocrinol.18(2) , 104–114 (2006).
  • Gomez-Pinilla F , ZhuangY, FengJ, YingZ, FanG. Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur. J. Neurosci.33(3) , 383–390 (2011).
  • Roth TL , LubinFD, FunkAJ, SweattJD. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol. Psychiatry65(9) , 760–769 (2009).
  • Mueller BR , BaleTL. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci.28(36) , 9055–9065 (2008).
  • Elliott E , Ezra-NevoG, RegevL, Neufeld-CohenA, ChenA. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat. Neurosci.13(11) , 1351–1353 (2010).
  • Sterrenburg L , GasznerB, BoerrigterJ et al. Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat. PLoS ONE 6(11) , e28128 (2011).
  • Menger Y , BettscheiderM, MurgatroydC, SpenglerD. Sex differences in brain epigenetics. Epigenomics2(6) , 807–821 (2010).
  • Murgatroyd C , PatchevAV, WuY et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 12(12) , 1559–1566 (2009).
  • Guy J , ChevalH, SelfridgeJ, BirdA. The role of MeCP2 in the brain. Annu. Rev. Cell Dev. Biol.27 , 631–652 (2011).
  • Skene PJ , IllingworthRS, WebbS et al. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 37(4) , 457–468 (2010).
  • Zhou Z , HongEJ, CohenS et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52(2) , 255–269 (2006).
  • Kendler KS , ThorntonLM, PedersenNL. Tobacco consumption in Swedish twins reared apart and reared together. Arch. Gen. Psychiatry57(9) , 886–892 (2000).
  • Murgatroyd C , SpenglerD. Genetic variation in the epigenetic machinery and mental health. Curr. Psychiatry Rep.14(2) , 138–149 (2012).
  • Feinberg AP , IrizarryRA. Evolution in health and medicine Sackler colloquium: Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc. Natl Acad. Sci. USA107(Suppl. 1) , S1757–S1764 (2010).
  • Rakyan VK , DownTA, BaldingDJ, BeckS. Epigenome-wide association studies for common human diseases. Nat. Rev. Genet.12(8) , 529–541 (2011).
  • Andersen SL , TeicherMH. Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci.31(4) , 183–191 (2008).

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