12,103
Views
0
CrossRef citations to date
0
Altmetric
Review

The Epigenetic Impacts of Social Stress: How does Social Adversity Become Biologically Embedded?

Pages 1653-1669 | Received 22 Jun 2016, Accepted 27 Sep 2016, Published online: 21 Nov 2016

References

  • McEwen BS , WingfieldJC . What is in a name? Integrating homeostasis, allostasis and stress . Hormones Behav.57 ( 2 ), 105 – 111 ( 2010 ).
  • McEwen BS , GrayJ , NascaC . Recognizing resilience: learning from the effects of stress on the brain . Neurobiol. Stress1 , 1 – 11 ( 2015 ).
  • Bohacek J , MansuyIM . Molecular insights into transgenerational non-genetic inheritance of acquired behaviours . Nat. Rev. Genet.16 ( 11 ), 641 – 652 ( 2015 ).
  • Anacker C , O’DonnellKJ , MeaneyMJ . Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function . Dialogues Clin. Neurosci.16 ( 3 ), 321 – 333 ( 2014 ).
  • Maccari S , KrugersHJ , Morley-FletcherS , SzyfM , BruntonPJ . The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations . J. Neuroendocrinol.26 ( 10 ), 707 – 723 ( 2014 ).
  • Kundakovic M , ChampagneFA . Early-life experience, epigenetics, and the developing brain . Neuropsychopharmacology40 ( 1 ), 141 – 153 ( 2015 ).
  • Weaver IC , CervoniN , ChampagneFAet al. Epigenetic programming by maternal behavior . Nat. Neurosci.7 ( 8 ), 847 – 854 ( 2004 ).
  • 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 ).
  • McGowan PO , SudermanM , SasakiAet al. Broad epigenetic signature of maternal care in the brain of adult rats . PLoS ONE6 ( 2 ), e14739 ( 2011 ).
  • Suderman M , McGowanPO , SasakiAet al. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus . Proc. Natl Acad. Sci. USA109 ( Suppl. 2 ), 17266 – 17272 ( 2012 ).
  • Murgatroyd C , PatchevAV , WuYet al. Dynamic DNA methylation programs persistent adverse effects of early-life stress . Nat. Neurosci.12 ( 12 ), 1559 – 1566 ( 2009 ).
  • Franklin TB , RussigH , WeissICet al. Epigenetic transmission of the impact of early stress across generations . Biol. Psychiatry68 ( 5 ), 408 – 415 ( 2010 ).
  • Franklin TB , SaabBJ , MansuyIM . Neural mechanisms of stress resilience and vulnerability . Neuron75 ( 5 ), 747 – 761 ( 2012 ).
  • Provencal N , SudermanMJ , GuilleminCet al. The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells . J. Neurosci.32 ( 44 ), 15626 – 15642 ( 2012 ).
  • Cole SW , ContiG , ArevaloJM , RuggieroAM , HeckmanJJ , SuomiSJ . Transcriptional modulation of the developing immune system by early life social adversity . Proc. Natl Acad. Sci. USA109 ( 50 ), 20578 – 20583 ( 2012 ).
  • Suomi SJ . Risk, resilience, and gene-environment interplay in primates . J. Can. Acad. Child. Adolesc. Psychiatry20 ( 4 ), 289 – 297 ( 2011 ).
  • Dettmer AM , SuomiSJ . Nonhuman primate models of neuropsychiatric disorders: influences of early rearing, genetics, and epigenetics . ILAR J.55 ( 2 ), 361 – 370 ( 2014 ).
  • Kinnally EL . Epigenetic plasticity following early stress predicts long-term health outcomes in rhesus macaques . Am. J. Phys. Anthropol.155 ( 2 ), 192 – 199 ( 2014 ).
  • Nieratschker V , MassartR , GillesMet al. MORC1 exhibits cross-species differential methylation in association with early life stress as well as genome-wide association with MDD . Transl. Psychiatry4 , e429 ( 2014 ).
  • McEwen BS , NascaC , GrayJD . Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex . Neuropsychopharmacology41 ( 1 ), 3 – 23 ( 2016 ).
  • Blaze J , ScheuingL , RothTL . Differential methylation of genes in the medial prefrontal cortex of developing and adult rats following exposure to maltreatment or nurturing care during infancy . Dev. Neurosci.35 ( 4 ), 306 – 316 ( 2013 ).
  • Roth TL , MattS , ChenK , BlazeJ . Bdnf DNA methylation modifications in the hippocampus and amygdala of male and female rats exposed to different caregiving environments outside the homecage . Dev. Psychobiol.56 ( 8 ), 1755 – 1763 ( 2014 ).
  • Doherty TS , ForsterA , RothTL . Global and gene-specific DNA methylation alterations in the adolescent amygdala and hippocampus in an animal model of caregiver maltreatment . Behav. Brain Res.298 ( Pt A ), 55 – 61 ( 2016 ).
  • Wu Y , PatchevAV , DanielG , AlmeidaOF , SpenglerD . Early-life stress reduces DNA methylation of the Pomc gene in male mice . Endocrinology155 ( 5 ), 1751 – 1762 ( 2014 ).
  • Bockmuhl Y , PatchevAV , MadejskaAet al. Methylation at the CpG island shore region upregulates Nr3c1 promoter activity after early-life stress . Epigenetics10 ( 3 ), 247 – 257 ( 2015 ).
  • St-Cyr S , McGowanPO . Programming of stress-related behavior and epigenetic neural gene regulation in mice offspring through maternal exposure to predator odor . Front. Behav. Neurosci.9 , 145 ( 2015 ).
  • Andersen SL . Exposure to early adversity: points of cross-species translation that can lead to improved understanding of depression . Dev. Psychopathol.27 ( 2 ), 477 – 491 ( 2015 ).
  • Turecki G , MeaneyMJ . Effects of the social environment and stress on glucocorticoid receptor gene methylation: a systematic review . Biol. Psychiatry79 ( 2 ), 87 – 96 ( 2016 ).
  • McGowan PO , SasakiA , D’AlessioACet al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse . Nat. Neurosci.12 ( 3 ), 342 – 348 ( 2009 ).
  • Radtke KM , RufM , GunterHMet al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor . Transl. Psychiatry1 , e21 ( 2011 ).
  • Mulligan CJ , D’ErricoNC , SteesJ , HughesDA . Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight . Epigenetics7 ( 8 ), 853 – 857 ( 2012 ).
  • Labonte B , YerkoV , GrossJet al. Differential glucocorticoid receptor exon 1(B), 1(C), and 1(H) expression and methylation in suicide completers with a history of childhood abuse . Biol. Psychiatry72 ( 1 ), 41 – 48 ( 2012 ).
  • Tyrka AR , ParadeSH , EslingerNMet al. Methylation of exons 1D, 1F, and 1H of the glucocorticoid receptor gene promoter and exposure to adversity in preschool-aged children . Dev. Psychopathol.27 ( 2 ), 577 – 585 ( 2015 ).
  • Weder N , ZhangH , JensenKet al. Child abuse, depression, and methylation in genes involved with stress, neural plasticity, and brain circuitry . J. Am. Acad. Child. Adolesc. Psychiatry53 ( 4 ), 417 – 424.e415 ( 2014 ).
  • van der Knaap LJ , RieseH , HudziakJJet al. Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. The TRAILS study . Transl. Psychiatry4 , e381 ( 2014 ).
  • Braithwaite EC , KundakovicM , RamchandaniPG , MurphySE , ChampagneFA . Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation . Epigenetics10 ( 5 ), 408 – 417 ( 2015 ).
  • Murgatroyd C , QuinnJP , SharpHM , PicklesA , HillJ . Effects of prenatal and postnatal depression, and maternal stroking, at the glucocorticoid receptor gene . Transl. Psychiatry5 , e560 ( 2015 ).
  • Radtke KM , SchauerM , GunterHMet al. Epigenetic modifications of the glucocorticoid receptor gene are associated with the vulnerability to psychopathology in childhood maltreatment . Transl. Psychiatry5 , e571 ( 2015 ).
  • Kertes DA , KaminHS , HughesDA , RodneyNC , BhattS , MulliganCJ . Prenatal maternal stress predicts methylation of genes regulating the hypothalamic–pituitary–adrenocortical system in mothers and newborns in the Democratic Republic of Congo . Child. Dev.87 ( 1 ), 61 – 72 ( 2016 ).
  • Kino T , HurtDE , IchijoT , NaderN , ChrousosGP . Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor . Sci. Signal.3 ( 107 ), ra8 ( 2010 ).
  • Hudson WH , PickardMR , de VeraIMet al. Conserved sequence-specific lincRNA-steroid receptor interactions drive transcriptional repression and direct cell fate . Nat. Commun.5 , 5395 ( 2014 ).
  • Vreugdenhil E , VerissimoCS , MarimanRet al. MicroRNA 18 and 124a down-regulate the glucocorticoid receptor: implications for glucocorticoid responsiveness in the brain . Endocrinology150 ( 5 ), 2220 – 2228 ( 2009 ).
  • Pan-Vazquez A , RyeN , AmeriMet al. Impact of voluntary exercise and housing conditions on hippocampal glucocorticoid receptor, miR-124 and anxiety . Mol. Brain8 , 40 ( 2015 ).
  • Melas PA , WeiY , WongCCet al. Genetic and epigenetic associations of MAOA and NR3C1 with depression and childhood adversities . Int. J. Neuropsychopharmacol.16 ( 7 ), 1513 – 1528 ( 2013 ).
  • Cao-Lei L , MassartR , SudermanMJet al. DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: Project Ice Storm . PLoS ONE9 ( 9 ), e107653 ( 2014 ).
  • Khulan B , ManningJR , DunbarDRet al. Epigenomic profiling of men exposed to early-life stress reveals DNA methylation differences in association with current mental state . Transl. Psychiatry4 , e448 ( 2014 ).
  • Non AL , HollisterBM , HumphreysKLet al. DNA methylation at stress-related genes is associated with exposure to early life institutionalization . Am. J. Phys. Anthropol.161 ( 1 ), 84 – 93 ( 2016 ).
  • Houtepen LC , VinkersCH , Carrillo-RoaTet al. Genome-wide DNA methylation levels and altered cortisol stress reactivity following childhood trauma in humans . Nat. Commun.7 , 10967 ( 2016 ).
  • Suderman M , BorgholN , PappasJJet al. Childhood abuse is associated with methylation of multiple loci in adult DNA . BMC Med. Genomics7 , 13 ( 2014 ).
  • Sapolsky RM . The influence of social hierarchy on primate health . Science308 ( 5722 ), 648 – 652 ( 2005 ).
  • Marmot MG , SapolskyRobert . Of Baboons And Men: Social Circumstances, Biology And The Social Gradient In Health . The National Academies Press , Washington DC, USA ( 2014 ).
  • Rubenstein DR . Stress hormones and sociality: integrating social and environmental stressors . Proc. Biol. Sci.274 ( 1612 ), 967 – 975 ( 2007 ).
  • Cavigelli SA , CarusoMJ . Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics . Phil. Trans. R Soc. Lond. B Biol. Sci.370 ( 1669 ), 20140103 ( 2015 ).
  • Sapolsky R . The Physiology of Dominance in Stable Versus Unstable Social Hierarchies . SUNY Press , NY, USA ( 1993 ).
  • Gust DA , GordonTP , WilsonME , Ahmed-AnsariA , BrodieAR , McClureHM . Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems . Brain Behav. Immun.5 ( 3 ), 296 – 307 ( 1991 ).
  • Shively CA , ClarksonTB . Social status and coronary artery atherosclerosis in female monkeys . Arterioscler. Thromb.14 ( 5 ), 721 – 726 ( 1994 ).
  • Sapolsky RM , ShareLJ . A pacific culture among wild baboons: its emergence and transmission . PLoS Biol.2 ( 4 ), E106 ( 2004 ).
  • Archie EA , AltmannJ , AlbertsSC . Social status predicts wound healing in wild baboons . Proc. Natl Acad. Sci. USA109 ( 23 ), 9017 – 9022 ( 2012 ).
  • Bernstein IS . Dominance, aggression and reproduction in primate societies . J. Theor. Biol.60 ( 2 ), 459 – 472 ( 1976 ).
  • Jarrell H , HoffmanJB , KaplanJR , BergaS , KinkeadB , WilsonME . Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys . Physiol. Behav.93 ( 4–5 ), 807 – 819 ( 2008 ).
  • Tung J , BarreiroLB , JohnsonZPet al. Social environment is associated with gene regulatory variation in the rhesus macaque immune system . Proc. Natl Acad. Sci. USA109 ( 17 ), 6490 – 6495 ( 2012 ).
  • Paiardini M , HoffmanJ , CervasiBet al. T-cell phenotypic and functional changes associated with social subordination and gene polymorphisms in the serotonin reuptake transporter in female rhesus mon keys . Brain Behav. Immun.23 ( 2 ), 286 – 293 ( 2009 ).
  • Arce M , MichopoulosV , ShepardKN , HaQC , WilsonME . Diet choice, cortisol reactivity, and emotional feeding in socially housed rhesus monkeys . Physiol. Behav.101 ( 4 ), 446 – 455 ( 2010 ).
  • Shively CA , RegisterTC , AdamsMR , GoldenDL , WillardSL , ClarksonTB . Depressive behavior and coronary artery atherogenesis in adult female cynomolgus monkeys . Psychosom. Med.70 ( 6 ), 637 – 645 ( 2008 ).
  • Shively CA , RegisterTC , ClarksonTB . Social stress, visceral obesity, and coronary artery atherosclerosis in female primates . Obesity (Silver Spring)17 ( 8 ), 1513 – 1520 ( 2009 ).
  • Kaplan JR , ChenH , ApptSEet al. Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in premenopausal monkeys and not mitigated by a high-isoflavone soy diet . Hum. Reprod.25 ( 12 ), 3083 – 3094 ( 2010 ).
  • Shively CA , MusselmanDL , WillardSL . Stress, depression, and coronary artery disease: modeling comorbidity in female primates . Neurosci. Biobehav. Rev.33 ( 2 ), 133 – 144 ( 2009 ).
  • Shively CA , RegisterTC , ClarksonTB . Social stress, visceral obesity, and coronary artery atherosclerosis: product of a primate adaptation . Am. J. Primatol.71 ( 9 ), 742 – 751 ( 2009 ).
  • Blomquist GE , Sade DonaldS , BerardJD . Rank-related fitness differences and their demographic pathways in semi-free-ranging rhesus macaques (Macaca mulatta) . Int. J. Primatol.32 ( 1 ), 193 – 208 ( 2011 ).
  • Snyder-Mackler N , KohnJN , BarreiroLB , JohnsonZP , WilsonME , TungJ . Social status drives social relationships in groups of unrelated female rhesus macaques . Anim. Behav.111 , 307 – 317 ( 2016 ).
  • Pickett KE , WilkinsonRG . Income inequality and health: a causal review . Soc. Sci. Med.128 , 316 – 326 ( 2015 ).
  • Grosenick L , ClementTS , FernaldRD . Fish can infer social rank by observation alone . Nature445 ( 7126 ), 429 – 432 ( 2007 ).
  • Fernald RD , MaruskaKP . Social information changes the brain . Proc. Natl Acad. Sci. USA109 ( Suppl. 2 ), 17194 – 17199 ( 2012 ).
  • Oliveira RF . Social plasticity in fish: integrating mechanisms and function . J. Fish Biol.81 ( 7 ), 2127 – 2150 ( 2012 ).
  • Cardoso SD , TelesMC , OliveiraRF . Neurogenomic mechanisms of social plasticity . J. Exp. Biol.218 ( Pt 1 ), 140 – 149 ( 2015 ).
  • Carpenter RE , MaruskaKP , BeckerL , FernaldRD . Social opportunity rapidly regulates expression of CRF and CRF receptors in the brain during social ascent of a teleost fish, Astatotilapia burtoni . PLoS ONE9 ( 5 ), e96632 ( 2014 ).
  • Maruska KP , ZhangA , NebooriA , FernaldRD . Social opportunity causes rapid transcriptional changes in the social behaviour network of the brain in an African cichlid fish . J. Neuroendocrinol.25 ( 2 ), 145 – 157 ( 2013 ).
  • Goodson JL . The vertebrate social behavior network: evolutionary themes and variations . Horm. Behav.48 ( 1 ), 11 – 22 ( 2005 ).
  • Maruska KP , BeckerL , NebooriA , FernaldRD . Social descent with territory loss causes rapid behavioral, endocrine and transcriptional changes in the brain . J. Exp. Biol.216 ( Pt 19 ), 3656 – 3666 ( 2013 ).
  • Lenkov K , LeeMH , LenkovOD , SwaffordA , FernaldRD . Epigenetic DNA methylation linked to social dominance . PLoS ONE10 ( 12 ), e0144750 ( 2015 ).
  • Teles MC , CardosoSD , OliveiraRF . Social plasticity relies on different neuroplasticity mechanisms across the brain social decision-making network in zebrafish . Front. Behav. Neurosci.10 , 16 ( 2016 ).
  • Oliveira RF , SimoesJM , TelesMC , OliveiraCR , BeckerJD , LopesJS . Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain . Proc. Natl Acad. Sci. USA113 ( 5 ), E654 – E661 ( 2016 ).
  • Paull GC , FilbyAL , GiddinsHG , CoeTS , HamiltonPB , TylerCR . Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success . Zebrafish7 ( 1 ), 109 – 117 ( 2010 ).
  • Filby AL , PaullGC , BartlettEJ , Van LookKJ , TylerCR . Physiological and health consequences of social status in zebrafish (Danio rerio) . Physiol. Behav.101 ( 5 ), 576 – 587 ( 2010 ).
  • O’Connell LA , HofmannHA . Evolution of a vertebrate social decision-making network . Science336 ( 6085 ), 1154 – 1157 ( 2012 ).
  • Abril-de-Abreu R , CruzJ , OliveiraRF . Social eavesdropping in zebrafish: tuning of attention to social interactions . Sci. Rep.5 , 12678 ( 2015 ).
  • Lopes JS , Abril-de-AbreuR , OliveiraRF . Brain transcriptomic response to social eavesdropping in zebrafish (Danio rerio) . PLoS ONE10 ( 12 ), e0145801 ( 2015 ).
  • Norton WH . Toward developmental models of psychiatric disorders in zebrafish . Front. Neural Circuits7 , 79 ( 2013 ).
  • Jones LJ , NortonWH . Using zebrafish to uncover the genetic and neural basis of aggression, a frequent comorbid symptom of psychiatric disorders . Behav. Brain Res.276 , 171 – 180 ( 2015 ).
  • Stewart AM , UllmannJF , NortonWHet al. Molecular psychiatry of zebrafish . Mol. Psychiatry20 ( 1 ), 2 – 17 ( 2015 ).
  • Wilkinson R , PickettK . The Spirit Level: Why Equality is Better for Everyone . Penguin , London, UK ( 2010 ).
  • Marmot M . The Health Gap: the Challenge of an Unequal World . Bloomsbury Publishing , London, UK ( 2015 ).
  • Bourdieu P . The Forms Of Capital . In : Handbook Of Theory And Research For The Sociology Of Education . Greenwood, New York, NY, USA , 241 – 258 ( 1986 ).
  • Coleman J . Foundations of Social Theory . Harvard University Press , Cambridge, USA ( 1994 ).
  • Putnam RD . Bowling Alone: The Collapse and Revival of American Community . Simon and Schuster , NY, USA ( 2001 ).
  • Dickerson SS , KemenyME . Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research . Psychol. Bull.130 ( 3 ), 355 – 391 ( 2004 ).
  • Gilbert P , McEwanK , BellewR , MillsA , GaleC . The dark side of competition: how competitive behaviour and striving to avoid inferiority are linked to depression, anxiety, stress and self-harm . Psychol. Psychother.82 ( Pt 2 ), 123 – 136 ( 2009 ).
  • Layte R . The association between income inequality and mental health: testing status anxiety, social capital, and neo-materialist explanations . Eur. Soc. Rev.28 ( 4 ), 498 – 511 ( 2011 ).
  • Layte R , WhelanCT . Who feels inferior? A test of the status anxiety hypothesis of social inequalities in health . Eur. Soc. Rev.30 ( 4 ), 525 – 535 ( 2014 ).
  • Mascaro O , CsibraG . Representation of stable social dominance relations by human infants . Proc. Natl Acad. Sci. USA109 ( 18 ), 6862 – 6867 ( 2012 ).
  • Frankel D , ArbelT . Group formation by two-year olds . Int. J. Behav. Dev.3 ( 3 ), 287 – 298 ( 1980 ).
  • Dickerson SS , GableSL , IrwinMR , AzizN , KemenyME . Social-evaluative threat and proinflammatory cytokine regulation: an experimental laboratory investigation . Psychol. Sci.20 ( 10 ), 1237 – 1244 ( 2009 ).
  • Chiang JJ , EisenbergerNI , SeemanTE , TaylorSE . Negative and competitive social interactions are related to heightened proinflammatory cytokine activity . Proc. Natl Acad. Sci. USA109 ( 6 ), 1878 – 1882 ( 2012 ).
  • Packard CJ , BezlyakV , McLeanJSet al. Early life socioeconomic adversity is associated in adult life with chronic inflammation, carotid atherosclerosis, poorer lung function and decreased cognitive performance: a cross-sectional, population-based study . BMC Public Health11 , 42 ( 2011 ).
  • Kumari M , ShipleyM , StaffordM , KivimakiM . Association of diurnal patterns in salivary cortisol with all-cause and cardiovascular mortality: findings from the Whitehall II study . J. Clin. Endocrinol. Metab.96 ( 5 ), 1478 – 1485 ( 2011 ).
  • Kumari M , BadrickE , ChandolaTet al. Measures of social position and cortisol secretion in an aging population: findings from the Whitehall II study . Psychosom. Med.72 ( 1 ), 27 – 34 ( 2010 ).
  • Stringhini S , BattyGD , BovetPet al. Association of lifecourse socioeconomic status with chronic inflammation and Type 2 diabetes risk: the Whitehall II prospective cohort study . PLoS Med.10 ( 7 ), e1001479 ( 2013 ).
  • Brody GH , YuT , ChenE , MillerGE , KoganSM , BeachSR . Is resilience only skin deep?: rural African Americans’ socioeconomic status-related risk and competence in preadolescence and psychological adjustment and allostatic load at age 19 . Psychol. Sci.24 ( 7 ), 1285 – 1293 ( 2013 ).
  • Powell ND , SloanEK , BaileyMTet al. Social stress up-regulates inflammatory gene expression in the leukocyte transcriptome via beta-adrenergic induction of myelopoiesis . Proc. Natl Acad. Sci. USA110 ( 41 ), 16574 – 16579 ( 2013 ).
  • Petrovic D , PivinE , PonteBet al. Sociodemographic, behavioral and genetic determinants of allostatic load in a Swiss population-based study . Psychoneuroendocrinology67 , 76 – 85 ( 2016 ).
  • Kiecolt-Glaser JK , GouinJP , HantsooL . Close relationships, inflammation, and health . Neurosci. Biobehav. Rev.35 ( 1 ), 33 – 38 ( 2010 ).
  • Aslund C , StarrinB , NilssonKW . Social capital in relation to depression, musculoskeletal pain, and psychosomatic symptoms: a cross-sectional study of a large population-based cohort of Swedish adolescents . BMC Public Health10 , 715 ( 2010 ).
  • Aslund C , StarrinB , NilssonKW . Psychosomatic symptoms and low psychological well-being in relation to employment status: the influence of social capital in a large cross-sectional study in Sweden . Int. J. Equity Health13 , 22 ( 2014 ).
  • Youm Y , LaumannEO , FerraroKFet al. Social network properties and self-rated health in later life: comparisons from the Korean social life, health, and aging project and the national social life, health and aging project . BMC Geriatr.14 , 102 ( 2014 ).
  • Uphoff EP , PickettKE , CabiesesB , SmallN , WrightJ . A systematic review of the relationships between social capital and socioeconomic inequalities in health: a contribution to understanding the psychosocial pathway of health inequalities . Int. J. Equity Health12 , 54 ( 2013 ).
  • Fisher PA , GunnarMR , ChamberlainP , ReidJB . Preventive intervention for maltreated preschool children: impact on children’s behavior, neuroendocrine activity, and foster parent functioning . J. Am. Acad. Child Adolesc. Psychiatry39 ( 11 ), 1356 – 1364 ( 2000 ).
  • Evans GW , KimP , TingAH , TesherHB , ShannisD . Cumulative risk, maternal responsiveness, and allostatic load among young adolescents . Dev. Psychol.43 ( 2 ), 341 – 351 ( 2007 ).
  • Chen E , MillerGE , KoborMS , ColeSW . Maternal warmth buffers the effects of low early-life socioeconomic status on pro-inflammatory signaling in adulthood . Mol. Psychiatry16 ( 7 ), 729 – 737 ( 2011 ).
  • Miller GE , BrodyGH , YuT , ChenE . A family-oriented psychosocial intervention reduces inflammation in low-SES African American youth . Proc. Natl Acad. Sci. USA111 ( 31 ), 11287 – 11292 ( 2014 ).
  • Hostinar CE , SullivanRM , GunnarMR . Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development . Psychol. Bull.140 ( 1 ), 256 – 282 ( 2014 ).
  • Borghol N , SudermanM , McArdleWet al. Associations with early-life socio-economic position in adult DNA methylation . Int. J. Epidemiol.41 ( 1 ), 62 – 74 ( 2012 ).
  • Lam LL , EmberlyE , FraserHBet al. Factors underlying variable DNA methylation in a human community cohort . Proc. Natl Acad. Sci. USA109 ( Suppl. 2 ), 17253 – 17260 ( 2012 ).
  • McGuinness D , McGlynnLM , JohnsonPCet al. Socio-economic status is associated with epigenetic differences in the pSoBid cohort . Int. J. Epidemiol.41 ( 1 ), 151 – 160 ( 2012 ).
  • Suderman M , PappasJJ , BorgholNet al. Lymphoblastoid cell lines reveal associations of adult DNA methylation with childhood and current adversity that are distinct from whole blood associations . Int. J. Epidemiol.44 ( 4 ), 1331 – 1340 ( 2015 ).
  • Needham BL , SmithJA , ZhaoWet al. Life course socioeconomic status and DNA methylation in genes related to stress reactivity and inflammation: the multi-ethnic study of atherosclerosis . Epigenetics10 ( 10 ), 958 – 969 ( 2015 ).
  • Stringhini S , PolidoroS , SacerdoteCet al. Life-course socioeconomic status and DNA methylation of genes regulating inflammation . Int. J. Epidemiol.44 ( 4 ), 1320 – 1330 ( 2015 ).
  • Fryers T , MelzerD , JenkinsR , BrughaT . The distribution of the common mental disorders: social inequalities in Europe . Clin. Pract. Epidemiol. Ment. Health1 , 14 ( 2005 ).
  • Swartz JR , HaririAR , WilliamsonDE . An epigenetic mechanism links socioeconomic status to changes in depression-related brain function in high-risk adolescents . Mol. Psychiatry doi:10.1038/mp.2016.82 ( 2016 ) ( Epub ahead of print ).
  • Beach SR , BrodyGH , TodorovAA , GunterTD , PhilibertRA . Methylation at SLC6A4 is linked to family history of child abuse: an examination of the Iowa Adoptee sample . Am. J. Med. Genet. B Neuropsychiatr. Genet.153b ( 2 ), 710 – 713 ( 2010 ).
  • Beach SR , BrodyGH , LeiMK , KimS , CuiJ , PhilibertRA . Is serotonin transporter genotype associated with epigenetic susceptibility or vulnerability? Examination of the impact of socioeconomic status risk on African American youth . Dev. Psychopathol.26 ( 2 ), 289 – 304 ( 2014 ).
  • Zhao J , GoldbergJ , BremnerJD , VaccarinoV . Association between promoter methylation of serotonin transporter gene and depressive symptoms: a monozygotic twin study . Psychosom. Med.75 ( 6 ), 523 – 529 ( 2013 ).
  • Nikolova YS , KoenenKC , GaleaSet al. Beyond genotype: serotonin transporter epigenetic modification predicts human brain function . Nat. Neurosci.17 ( 9 ), 1153 – 1155 ( 2014 ).
  • Swartz JR , KnodtAR , RadtkeSR , HaririAR . A neural biomarker of psychological vulnerability to future life stress . Neuron85 ( 3 ), 505 – 511 ( 2015 ).
  • Swartz JR , WilliamsonDE , HaririAR . Developmental change in amygdala reactivity during adolescence: effects of family history of depression and stressful life events . Am. J. Psychiatry172 ( 3 ), 276 – 283 ( 2015 ).
  • Beach SR , LeiMK , BrodyGHet al. Parenting, socioeconomic status risk, and later young adult health: exploration of opposing indirect effects via DNA methylation . Child Dev.87 ( 1 ), 111 – 121 ( 2016 ).
  • Brody GH , YuT , ChenE , BeachSR , MillerGE . Family-centered prevention ameliorates the longitudinal association between risky family processes and epigenetic aging . J. Child. Psychol. Psychiatry57 ( 5 ), 566 – 574 ( 2016 ).
  • Brody GH , MillerGE , YuT , BeachSR , ChenE . Supportive family environments ameliorate the link between racial discrimination and epigenetic aging: a replication across two longitudinal cohorts . Psychol. Sci.27 ( 4 ), 530 – 541 ( 2016 ).
  • Hannum G , GuinneyJ , ZhaoLet al. Genome-wide methylation profiles reveal quantitative views of human aging rates . Mol. Cell49 ( 2 ), 359 – 367 ( 2013 ).
  • Horvath S . DNA methylation age of human tissues and cell types . Genome Biol.14 ( 10 ), R115 ( 2013 ).
  • Lahiri DK , MaloneyB , ZawiaNH . The LEARn model: an epigenetic explanation for idiopathic neurobiological diseases . Mol. Psychiatry14 ( 11 ), 992 – 1003 ( 2009 ).
  • Simpkin AJ , HemaniG , SudermanMet al. Prenatal and early life influences on epigenetic age in children: a study of mother-offspring pairs from two cohort studies . Hum. Mol. Genet.25 ( 1 ), 191 – 201 ( 2016 ).
  • Marioni RE , ShahS , McRaeAFet al. The epigenetic clock is correlated with physical and cognitive fitness in the Lothian Birth Cohort 1936 . Int. J. Epidemiol.44 ( 4 ), 1388 – 1396 ( 2015 ).
  • Marioni RE , ShahS , McRaeAFet al. DNA methylation age of blood predicts all-cause mortality in later life . Genome Biol.16 , 25 ( 2015 ).
  • Zannas AS , ArlothJ , Carrillo-RoaTet al. Lifetime stress accelerates epigenetic aging in an urban, African American cohort: relevance of glucocorticoid signaling . Genome Biol.16 , 266 ( 2015 ).
  • Miller GE , YuT , ChenE , BrodyGH . Self-control forecasts better psychosocial outcomes but faster epigenetic aging in low-SES youth . Proc. Natl Acad. Sci. USA112 ( 33 ), 10325 – 10330 ( 2015 ).
  • Castagne R , DelpierreC , Kelly-IrvingMet al. A life course approach to explore the biological embedding of socioeconomic position and social mobility through circulating inflammatory markers . Sci. Rep.6 , 25170 ( 2016 ).
  • Vukojevic V , KolassaIT , FastenrathMet al. Epigenetic modification of the glucocorticoid receptor gene is linked to traumatic memory and post-traumatic stress disorder risk in genocide survivors . J. Neurosci.34 ( 31 ), 10274 – 10284 ( 2014 ).
  • Yehuda R , FloryJD , BiererLMet al. Lower methylation of glucocorticoid receptor gene promoter 1F in peripheral blood of veterans with post-traumatic stress disorder . Biol. Psychiatry77 ( 4 ), 356 – 364 ( 2015 ).
  • Sadeh N , SpielbergJM , LogueMWet al. SKA2 methylation is associated with decreased prefrontal cortical thickness and greater PTSD severity among trauma-exposed veterans . Mol. Psychiatry21 ( 3 ), 357 – 363 ( 2016 ).
  • Boks MP , RuttenBP , GeuzeEet al. SKA2 methylation is involved in cortisol stress reactivity and predicts the development of post-traumatic stress disorder (PTSD) after military deployment . Neuropsychopharmacology41 ( 5 ), 1350 – 1356 ( 2016 ).
  • Guintivano J , BrownT , NewcomerAet al. Identification and replication of a combined epigenetic and genetic biomarker predicting suicide and suicidal behaviors . Am. J. Psychiatry171 ( 12 ), 1287 – 1296 ( 2014 ).
  • Kaminsky Z , WilcoxHC , EatonWWet al. Epigenetic and genetic variation at SKA2 predict suicidal behavior and post-traumatic stress disorder . Transl. Psychiatry5 , e627 ( 2015 ).
  • Vinkers CH , KalafateliAL , RuttenBPet al. Traumatic stress and human DNA methylation: a critical review . Epigenomics7 ( 4 ), 593 – 608 ( 2015 ).
  • Yehuda R , DaskalakisNP , LehrnerAet al. Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring . Am. J. Psychiatry171 ( 8 ), 872 – 880 ( 2014 ).
  • Yehuda R , DaskalakisNP , BiererLMet al. Holocaust exposure induced intergenerational effects on FKBP5 methylation . Biol. Psychiatry80 ( 5 ), 372 – 380 ( 2016 ).
  • Bohacek J , FarinelliM , MiranteOet al. Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress . Mol. Psychiatry20 ( 5 ), 621 – 631 ( 2015 ).
  • Gapp K , BohacekJ , GrossmannJet al. Potential of environmental enrichment to prevent transgenerational effects of paternal trauma . Neuropsychopharmacology41 ( 11 ), 2749 – 2758 ( 2016 ).
  • Gapp K , JawaidA , SarkiesPet al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice . Nat. Neurosci.17 ( 5 ), 667 – 669 ( 2014 ).
  • Short AK , FennellKA , PerreauVMet al. Elevated paternal glucocorticoid exposure alters the small noncoding RNA profile in sperm and modifies anxiety and depressive phenotypes in the offspring . Transl. Psychiatry6 ( 6 ), e837 ( 2016 ).