Epigenetic programming by stress and glucocorticoids along the human lifespan

A S Zannas; G P Chrousos

doi:10.1038/mp.2017.35

journal article Mar 14, 2017

Epigenetic programming by stress and glucocorticoids along the human lifespan

A S Zannas G P Chrousos

Molecular Psychiatry Vol. 22 No. 5 pp. 640-646 · Springer Science and Business Media LLC

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References

101

[1]

Telese F, Gamliel A, Skowronska-Krawczyk D, Garcia-Bassets I, Rosenfeld MG . ‘Seq-ing’ insights into the epigenetics of neuronal gene regulation. Neuron 2013; 77: 606–623. 10.1016/j.neuron.2013.01.034

[2]

Zannas AS, West AE . Epigenetics and the regulation of stress vulnerability and resilience. Neuroscience 2014; 264: 157–170. 10.1016/j.neuroscience.2013.12.003

[3]

Dias BG, Ressler KJ . Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 2014; 17: 89–96. 10.1038/nn.3594

[4]

Gassen NC, Chrousos GP, Binder EB, Zannas AS . Life stress, glucocorticoid signaling, and the aging epigenome: Implications for aging-related diseases. Neurosci Biobehav Rev 2016 (in press). 10.1016/j.neubiorev.2016.06.003

[5]

Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G et al. Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB j 2010; 24: 3135–3144. 10.1096/fj.09-150490

[6]

Vockley CM, D'Ippolito AM, McDowell IC, Majoros WH, Safi A, Song L et al. Direct GR Binding Sites Potentiate Clusters of TF Binding across the Human Genome. Cell 2016; 166: 1269–1281.e1219. 10.1016/j.cell.2016.07.049

[7]

Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC, Pariante CM et al. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat Neurosci 2013; 16: 33–41. 10.1038/nn.3275

[8]

Wiench M, John S, Baek S, Johnson TA, Sung MH, Escobar T et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO j 2011; 30: 3028–3039. 10.1038/emboj.2011.210

[9]

Thomassin H, Flavin M, Espinas ML, Grange T . Glucocorticoid-induced DNA demethylation and gene memory during development. EMBO j 2001; 20: 1974–1983. 10.1093/emboj/20.8.1974

[10]

Lifetime stress accelerates epigenetic aging in an urban, African American cohort: relevance of glucocorticoid signaling

Anthony S. Zannas, Janine Arloth, Tania Carrillo-Roa et al.

Genome Biology 2015 10.1186/s13059-015-0828-5

[11]

Bose R, Moors M, Tofighi R, Cascante A, Hermanson O, Ceccatelli S . Glucocorticoids induce long-lasting effects in neural stem cells resulting in senescence-related alterations. Cell Death Dis 2010; 1: e92. 10.1038/cddis.2010.60

[12]

Bose R, Spulber S, Kilian P, Heldring N, Lonnerberg P, Johnsson A et al. Tet3 mediates stable glucocorticoid-induced alterations in DNA methylation and Dnmt3a/Dkk1 expression in neural progenitors. Cell Death Dis 2015; 6: e1793. 10.1038/cddis.2015.159

[13]

Resmini E, Santos A, Aulinas A, Webb SM, Vives-Gilabert Y, Cox O et al. Reduced DNA methylation of FKBP5 in Cushing's syndrome. Endocrine 2016; 54: 768–777. 10.1007/s12020-016-1083-6

[14]

Niwa M, Jaaro-Peled H, Tankou S, Seshadri S, Hikida T, Matsumoto Y et al. Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 2013; 339: 335–339. 10.1126/science.1226931

[15]

Sawamura T, Klengel T, Armario A, Jovanovic T, Norrholm SD, Ressler KJ et al. Dexamethasone Treatment Leads to Enhanced Fear Extinction and Dynamic Fkbp5 Regulation in Amygdala. Neuropsychopharmacology 2015; 41: 832–846. 10.1038/npp.2015.210

[16]

Gassen NC, Fries GR, Zannas AS, Hartmann J, Zschocke J, Hafner K et al. Chaperoning epigenetics: FKBP51 decreases the activity of DNMT1 and mediates epigenetic effects of the antidepressant paroxetine. Sci Signal 2015; 8: ra119. 10.1126/scisignal.aac7695

[17]

Yang X, Ewald ER, Huo Y, Tamashiro KL, Salvatori R, Sawa A et al. Glucocorticoid-induced loss of DNA methylation in non-neuronal cells and potential involvement of DNMT1 in epigenetic regulation of Fkbp5. Biochem Biophys Res Commun 2012; 420: 570–575. 10.1016/j.bbrc.2012.03.035

[18]

Benoit JD, Rakic P, Frick KM . Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression. Behav Brain Res 2015; 281: 1–8. 10.1016/j.bbr.2014.12.001

[19]

Dong E, Dzitoyeva SG, Matrisciano F, Tueting P, Grayson DR, Guidotti A . Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice. Biol Psychiatry 2015; 77: 589–596. 10.1016/j.biopsych.2014.08.012

[20]

Zannas AS, Chrousos GP . Glucocorticoid signaling drives epigenetic and transcription factors to induce key regulators of human parturition. Sci Signal 2015; 8: fs19. 10.1126/scisignal.aad3022

[21]

Di Stefano V, Wang B, Parobchak N, Roche N, Rosen T . RelB/p52-mediated NF-kappaB signaling alters histone acetylation to increase the abundance of corticotropin-releasing hormone in human placenta. Sci Signal 2015; 8: ra85. 10.1126/scisignal.aaa9806

[22]

Dwivedi Y, Roy B, Lugli G, Rizavi H, Zhang H, Smalheiser NR . Chronic corticosterone-mediated dysregulation of microRNA network in prefrontal cortex of rats: relevance to depression pathophysiology. Transl Psychiatry 2015; 5: e682. 10.1038/tp.2015.175

[23]

Ko JY, Chuang PC, Ke HJ, Chen YS, Sun YC, Wang FS . MicroRNA-29a mitigates glucocorticoid induction of bone loss and fatty marrow by rescuing Runx2 acetylation. Bone 2015; 81: 80–88. 10.1016/j.bone.2015.06.022

[24]

Ewald ER, Wand GS, Seifuddin F, Yang X, Tamashiro KL, Potash JB et al. Alterations in DNA methylation of Fkbp5 as a determinant of blood-brain correlation of glucocorticoid exposure. Psychoneuroendocrinology 2014; 44: 112–122. 10.1016/j.psyneuen.2014.03.003

[25]

Lee RS, Tamashiro KL, Yang X, Purcell RH, Harvey A, Willour VL et al. Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinology 2010; 151: 4332–4343. 10.1210/en.2010-0225

[26]

Yehuda R, Daskalakis NP, Bierer LM, Bader HN, Klengel T, Holsboer F et al. Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation. Biol Psychiatry 2015; 80: 372–380. 10.1016/j.biopsych.2015.08.005

[27]

Montagud-Romero S, Montesinos J, Pascual M, Aguilar MA, Roger-Sanchez C, Guerri C et al. ‘Up-regulation of histone acetylation induced by social defeat mediates the conditioned rewarding effects of cocaine. Prog Neuropsychopharmacol Biol Psychiatry 2016; 70: 39–48. 10.1016/j.pnpbp.2016.04.016

[28]

Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation

Ali B. Rodgers, Christopher P. Morgan, Stefanie L. Bronson et al.

The Journal of Neuroscience 2013 10.1523/jneurosci.0914-13.2013

[29]

Rodgers AB, Morgan CP, Leu NA, Bale TL . Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci USA 2015; 112: 13699–13704. 10.1073/pnas.1508347112

[30]

Mychasiuk R, Schmold N, Ilnytskyy S, Kovalchuk O, Kolb B, Gibb R . Prenatal bystander stress alters brain, behavior, and the epigenome of developing rat offspring. Dev Neurosci 2011; 33: 159–169. 10.1159/000330034

[31]

Xu L, Sun Y, Gao L, Cai YY, Shi SX . Prenatal restraint stress is associated with demethylation of corticotrophin releasing hormone (CRH) promoter and enhances CRH transcriptional responses to stress in adolescent rats. Neurochem Res 2014; 39: 1193–1198. 10.1007/s11064-014-1296-0

[32]

Palma-Gudiel H, Cordova-Palomera A, Eixarch E, Deuschle M, Fananas L . Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: a meta-analysis. Epigenetics 2015; 10: 893–902. 10.1080/15592294.2015.1088630

[33]

Prenatal stress decreasesBdnfexpression and increases methylation ofBdnfexon IV in rats

Gretha J Boersma, Richard S Lee, Zachary A Cordner et al.

Epigenetics 2014 10.4161/epi.27558

[34]

Palacios-Garcia I, Lara-Vasquez A, Montiel JF, Diaz-Veliz GF, Sepulveda H, Utreras E et al. Prenatal stress down-regulates Reelin expression by methylation of its promoter and induces adult behavioral impairments in rats. PLoS ONE 2015; 10: e0117680. 10.1371/journal.pone.0117680

[35]

Mulligan CJ, D'Errico NC, Stees J, Hughes DA . Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics 2012; 7: 853–857. 10.4161/epi.21180

[36]

Cao-Lei L, Massart R, Suderman MJ, Machnes Z, Elgbeili G, Laplante DP et al. DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: Project Ice Storm. PLoS ONE 2014; 9: e107653. 10.1371/journal.pone.0107653

[37]

Schraut KG, Jakob SB, Weidner MT, Schmitt AG, Scholz CJ, Strekalova T et al. Prenatal stress-induced programming of genome-wide promoter DNA methylation in 5-HTT-deficient mice. Transl Psychiatry 2014; 4: e473. 10.1038/tp.2014.107

[38]

Winston JH, Li Q, Sarna SK . Chronic prenatal stress epigenetically modifies spinal cord BDNF expression to induce sex-specific visceral hypersensitivity in offspring. Neurogastroenterol Motil 2014; 26: 715–730. 10.1111/nmo.12326

[39]

Monteleone MC, Adrover E, Pallares ME, Antonelli MC, Frasch AC, Brocco MA . Prenatal stress changes the glycoprotein GPM6A gene expression and induces epigenetic changes in rat offspring brain. Epigenetics 2014; 9: 152–160. 10.4161/epi.25925

[40]

Zucchi FC, Yao Y, Ward ID, Ilnytskyy Y, Olson DM, Benzies K et al. Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring. PLoS ONE 2013; 8: e56967. 10.1371/journal.pone.0056967

[41]

Anier K, Malinovskaja K, Pruus K, Aonurm-Helm A, Zharkovsky A, Kalda A . Maternal separation is associated with DNA methylation and behavioural changes in adult rats. Eur Neuropsychopharmacol 2014; 24: 459–468. 10.1016/j.euroneuro.2013.07.012

[42]

Doherty TS, Forster A, Roth TL . Global and gene-specific DNA methylation alterations in the adolescent amygdala and hippocampus in an animal model of caregiver maltreatment. Behav Brain Res 2016; 298 (Pt A): 55–61. 10.1016/j.bbr.2015.05.028

[43]

Roth TL, Lubin FD, Funk AJ, Sweatt JD . Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 2009; 65: 760–769. 10.1016/j.biopsych.2008.11.028

[44]

Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847–854. 10.1038/nn1276

[45]

Tyrka AR, Price LH, Marsit C, Walters OC, Carpenter LL . Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS ONE 2012; 7: e30148. 10.1371/journal.pone.0030148

[46]

Houtepen LC, Vinkers CH, Carrillo-Roa T, Hiemstra M, van Lier PA, Meeus W et al. Genome-wide DNA methylation levels and altered cortisol stress reactivity following childhood trauma in humans. Nat Commun 2016; 7: 10967. 10.1038/ncomms10967

[47]

Ouellet-Morin I, Wong CC, Danese A, Pariante CM, Papadopoulos AS, Mill J et al. Increased serotonin transporter gene (SERT) DNA methylation is associated with bullying victimization and blunted cortisol response to stress in childhood: a longitudinal study of discordant monozygotic twins. Psychol Med 2013; 43: 1813–1823. 10.1017/s0033291712002784

[48]

Unternaehrer E, Luers P, Mill J, Dempster E, Meyer AH, Staehli S et al. Dynamic changes in DNA methylation of stress-associated genes (OXTR, BDNF ) after acute psychosocial stress. Transl Psychiatry 2012; 2: e150. 10.1038/tp.2012.77

[49]

van der Knaap LJ, Riese H, Hudziak JJ, Verbiest MM, Verhulst FC, Oldehinkel AJ et al. Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. The TRAILS study. Transl Psychiatry 2014; 4: e381. 10.1038/tp.2014.22

[50]

Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 2009; 12: 1559–1566. 10.1038/nn.2436

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Published: Mar 14, 2017
Vol/Issue: 22(5)
Pages: 640-646
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A S Zannas, G P Chrousos (2017). Epigenetic programming by stress and glucocorticoids along the human lifespan. Molecular Psychiatry, 22(5), 640-646. https://doi.org/10.1038/mp.2017.35

Epigenetic programming by stress and glucocorticoids along the human lifespan

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