4,764
Views
6
CrossRef citations to date
0
Altmetric
Research Article

The Biological Embedding of Early-Life Socioeconomic Status and Family Adversity in Children’s Genome-Wide DNA Methylation

, , , , , , , & show all
Pages 1445-1461 | Received 27 Jun 2018, Accepted 27 Jul 2018, Published online: 23 Oct 2018

References

  • Adler NE , StewartJ . Health disparities across the lifespan: meaning, methods, and mechanisms . Ann. NY Acad. Sci.1186 , 5 – 23 ( 2010 ).
  • Braveman P , EgerterS . Overcoming obstacles to health: a report to the Robert Wood Johnson Foundation Commission to Build a Healthier America . Robert Wood Johnson Foundation , Princeton, NJ, USA , 1 – 80 ( 2008 ).
  • Cohen S , DoyleWJ , TurnerRB , AlperCM , SkonerDP . Childhood socioeconomic status and host resistance to infectious illness in adulthood . Psychosom. Med.66 ( 4 ), 553 – 558 ( 2004 ).
  • Miller G , ChenE . Unfavorable socioeconomic conditions in early life presage expression of proinflammatory phenotype in adolescence . Psychosom. Med.69 ( 5 ), 402 – 409 ( 2007 ).
  • Hertzman C . The biological embedding of early experience and its effects on health in adulthood . Ann. NY Acad. Sci.896 , 85 – 95 ( 1999 ).
  • Miller GE , ChenE , FokAKet al. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling . Proc. Natl Acad. Sci. USA106 ( 34 ), 14716 – 14721 ( 2009 ).
  • Noble KG , HoustonSM , BritoNHet al. Family income, parental education and brain structure in children and adolescents . Nat. Neurosci.18 ( 5 ), 773 – 778 ( 2015 ).
  • Bush NR , BoyceWT . The contributions of early experience to biological development and sensitivity to context . In : Handbook of Developmental Psychopathology . LewisM , RudolphKD ( Eds ). Springer , NY, USA , 287 – 309 ( 2014 ).
  • Hertzman C , BoyceWT . How experience gets under the skin to create gradients in developmental health . Ann. Rev. Public Health31 , 329 – 347 ( 2010 ).
  • Miller GE , ChenE , ParkerKJ . Psychological stress in childhood and susceptibility to the chronic diseases of aging: moving toward a model of behavioral and biological mechanisms . Psychol. Bull.137 ( 6 ), 959 – 997 ( 2011 ).
  • Farah MJ , SheraDM , SavageJHet al. Childhood poverty: specific associations with neurocognitive development . Brain Res.1110 ( 1 ), 166 – 174 ( 2006 ).
  • Sheridan MA , SarsourK , JutteD , D’espositoM , BoyceWT . The impact of social disparity on prefrontal function in childhood . PLoS ONE7 ( 4 ), e35744 ( 2012 ).
  • Chen E , CohenS , MillerGE . How low socioeconomic status affects 2-year hormonal trajectories in children . Psychol. Sci.21 ( 1 ), 31 – 37 ( 2010 ).
  • Shonkoff JP , GarnerAS , The Committee on Psychosocial Aspects of Child and Family Healthet al.The lifelong effects of early childhood adversity and toxic stress . Pediatrics129 ( 1 ), e232 – e246 ( 2012 ).
  • Alkon A , BoyceWT , TranL , HarleyKG , NeuhausJ , EskenaziB . Prenatal adversities and Latino children’s autonomic nervous system reactivity trajectories from 6 months to 5 years of age . PLoS ONE9 ( 1 ), e86283 ( 2014 ).
  • Bush NR , ObradovicJ , AdlerN , BoyceWT . Kindergarten stressors and cumulative adrenocortical activation: the “first straws” of allostatic load?Dev. Psychopathol.23 ( 4 ), 1089 – 1106 ( 2011 ).
  • Blair C , RaverCC , GrangerD , Mills-KoonceR , HibelL . Allostasis and allostatic load in the context of poverty in early childhood . Dev. Psychopathol.23 ( Special Issue 03 ), 845 – 857 ( 2011 ).
  • Ly M , HaynesMR , BarterJW , WeinbergerDR , ZinkCF . Subjective socioeconomic status predicts human ventral striatal responses to social status information . Curr. Biol.21 ( 9 ), 794 – 797 ( 2011 ).
  • Meaney MJ . Epigenetics and the biological definition of gene X environment interactions . Child Dev.81 ( 1 ), 41 – 79 ( 2010 ).
  • Boyce WT , KoborMS . Development and the epigenome: the ‘synapse’ of gene–environment interplay . Dev. Sci.18 ( 1 ), 1 – 23 ( 2015 ).
  • 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 ).
  • Borghol N , SudermanM , McArdleWet al. Associations with early-life socio-economic position in adult DNA methylation . Int. J. Epidemiol.41 ( 1 ), 62 – 74 ( 2012 ).
  • Tehranifar P , WuHC , FanXet al. Early life socioeconomic factors and genomic DNA methylation in mid-life . Epigenetics8 ( 1 ), 23 – 27 ( 2013 ).
  • Mcdade TW , RyanC , JonesMJet al. Social and physical environments early in development predict DNA methylation of inflammatory genes in young adulthood . Proc. Natl Acad. Sci. USA114 ( 29 ), 7611 – 7616 ( 2017 ).
  • Stringhini S , PolidoroS , SacerdoteCet al. Life-course socioeconomic status and DNA methylation of genes regulating inflammation . Int. J. Epidemiol.44 ( 4 ), 1320 – 1330 ( 2015 ).
  • Smith AK , KilaruV , KlengelTet al. DNA extracted from saliva for methylation studies of psychiatric traits: evidence tissue specificity and relatedness to brain . Am. J. Med. Genet. B Neuropsychiatr. Genet.168B ( 1 ), 36 – 44 ( 2015 ).
  • Adler N , BushNR , PantellMS . Rigor, vigor, and the study of health disparities . Proc. Natl Acad. Sci. USA109 ( Suppl. 2 ), 17154 – 17159 ( 2012 ).
  • Lengua LJ , BushNR , LongAC , KovacsEA , TrancikAM . Effortful control as a moderator of the relation between contextual risk factors and growth in adjustment problems . Dev. Psychopathol.20 ( 2 ), 509 – 528 ( 2008 ).
  • Sheikh MA , AbelsenB , OlsenJA . Clarifying associations between childhood adversity, social support, behavioral factors, and mental health, health, and well-being in adulthood: a population-based study . Front. Psychol.7 , 727 ( 2016 ).
  • Essex MJ , BoyceWT , HertzmanCet al. Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence . Child Dev.84 ( 1 ), 58 – 75 ( 2013 ).
  • Fraser HB , LamLL , NeumannSM , KoborMS . Population-specificity of human DNA methylation . Genome Biol.13 ( 2 ), R8 ( 2012 ).
  • Heyn H , MoranS , Hernando-HerraezIet al. DNA methylation contributes to natural human variation . Genome Res.23 ( 9 ), 1363 – 1372 ( 2013 ).
  • 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 ).
  • Birney E , SmithGD , GreallyJM . Epigenome-wide association studies and the interpretation of disease -omics . PLoS Genet.12 ( 6 ), e1006105 ( 2016 ).
  • Mersha TB , AbebeT . Self-reported race/ethnicity in the age of genomic research: its potential impact on understanding health disparities . Hum. Genomics9 ( 1 ), 1 ( 2015 ).
  • Galanter JM , GignouxCR , OhSSet al. Differential methylation between ethnic sub-groups reflects the effect of genetic ancestry and environmental exposures . eLife6 , e20532 ( 2017 ).
  • Jones MJ , FarréP , McEwenLMet al. Distinct DNA methylation patterns of cognitive impairment and trisomy 21 in down syndrome . BMC Med. Genomics6 , 58 ( 2013 ).
  • Benjamini Y , HochbergY . Controlling the false discovery rate: a practical and powerful approach to multiple testing . J. R. Stat. Soc. Series B (Methodol.)57 ( 1 ), 289 – 300 ( 1995 ).
  • Martin P , MartinM . Proximal and distal influences on development: the model of developmental adaptation . Dev. Rev.22 ( 1 ), 78 – 96 ( 2002 ).
  • The Gene Ontology Consortium . Gene Ontology Consortium: going forward . Nucl. Acids Res.43 ( database issue ), D1049 – D1056 ( 2015 ).
  • Hackman DA , GallopR , EvansGW , FarahMJ . Socioeconomic status and executive function: developmental trajectories and mediation . Dev. Sci.18 ( 5 ), 686 – 702 ( 2015 ).
  • Friedman EM , KarlamanglaA , GruenewaldT , KoretzB , SeemanT . Early life adversity and adult biological risk profiles . Psychosom. Med.77 ( 2 ), 176 – 185 ( 2015 ).
  • Williams DR , MohammedSA , LeavellJ , CollinsC . Race, socioeconomic status, and health: complexities, ongoing challenges, and research opportunities . Ann. NY Acad. Sci.1186 ( 1 ), 69 – 101 ( 2010 ).
  • Kuzawa CW , SweetE . Epigenetics and the embodiment of race: developmental origins of US racial disparities in cardiovascular health . Am. J. Hum. Biol.21 ( 1 ), 2 – 15 ( 2009 ).
  • Florez JC , PriceAL , CampbellDet al. Strong association of socioeconomic status and genetic ancestry in Latinos: implications for admixture studies of type 2 diabetes . In : Racial Identities, Genetic Ancestry, and Health in South America: Argentina, Brazil, Colombia, and Uruguay . GibbonS , SantosRV , SansM ( Eds ). Palgrave Macmillan , NY, USA , 137 – 153 ( 2011 ).
  • Peralta CA , ZivE , KatzRet al. African ancestry, socioeconomic status, and kidney function in elderly African Americans: a genetic admixture analysis . J. Am. Soc. Nephrol.17 ( 12 ), 3491 – 3496 ( 2006 ).
  • Freedland KE , MillerGE , ShepsDS . The great debate, revisited . Psychosom. Med.68 , 179 – 184 ( 2006 ).
  • Lowe R , GemmaC , BeyanHet al. Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies . Epigenetics8 ( 4 ), 445 – 454 ( 2013 ).
  • Bush NR , LaneRD , McLaughlinKA . Mechanisms underlying the association between early-life adversity and physical health: charting a course for the future . Psychosom. Med.78 ( 9 ), 1114 – 1119 ( 2016 ).
  • Teicher MH , SamsonJA . Annual research review: enduring neurobiological effects of childhood abuse and neglect . J. Child Psychol. Psychiatry57 ( 3 ), 241 – 266 ( 2016 ).
  • Theda C , HwangSH , CzajkoA , LokeYJ , LeongP , CraigJM . Quantitation of the cellular content of saliva and buccal swab samples . Sci. Rep.8 ( 1 ), 6944 ( 2018 ).
  • Berko ER , SuzukiM , BerenFet al. Mosaic epigenetic dysregulation of ectodermal cells in autism spectrum disorder . PLOS Genet.10 ( 5 ), e1004402 ( 2014 ).
  • Hill WD , HagenaarsSP , MarioniREet al. Molecular genetic contributions to social deprivation and household income in UK biobank . Curr. Biol.26 ( 22 ), 3083 – 3089 ( 2016 ).
  • Breton CV , MarsitCJ , FaustmanEet al. Small-magnitude effect sizes in epigenetic end points are important in children’s environmental health studies: the Children’s Environmental Health and Disease Prevention Research Center’s Epigenetics Working Group . Environ. Health Perspect.125 ( 4 ), 511 – 526 ( 2017 ).
  • Bush NR , BoyceWT . Differential sensitivity to context: implications for developmental psychopathology . In : Developmental Psychopathology . CicchettiD ( Ed. ). John Wiley and Sons, Inc. , Hoboken, NJ, USA ( 2016 ).
  • Meaney MJ , SzyfM . Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome . Dialogues Clin. Neurosci.7 ( 2 ), 103 – 123 ( 2005 ).
  • Teh AL , PanH , ChenLet al. The effect of genotype and in utero environment on inter-individual variation in neonate DNA methylomes . Genome Res.24 , 1064 – 1074 ( 2014 ).
  • Shonkoff JP . Leveraging the biology of adversity to address the roots of disparities in health and development . Proc. Natl Acad. Sci. USA109 ( Suppl. 2 ), 17302 – 17307 ( 2012 ).
  • Obradović J , BushNR , StamperdahlJ , AdlerNE , BoyceWT . Biological sensitivity to context: the interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness . Child Dev.81 ( 1 ), 270 – 289 ( 2010 ).
  • Essex MJ , KleinMH , ChoE , KalinNH . Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior . Biol. Psychiatry52 ( 8 ), 776 – 784 ( 2002 ).
  • Purcell S , NealeB , Todd-BrownKet al. PLINK: a tool set for whole-genome association and population-based linkage analyses . Am. J. Hum. Genet.81 ( 3 ), 559 – 575 ( 2007 ).
  • Solovieff N , HartleySW , BaldwinCT , PerlsTT , SteinbergMH , SebastianiP . Clustering by genetic ancestry using genome-wide SNP data . BMC Genet.11 , 108 ( 2010 ).
  • Price ME , CottonAM , LamLLet al. Additional annotation enhances potential for biologically-relevant analysis of the Illumina Infinium HumanMethylation450 BeadChip array . Epigenetics Chromatin6 ( 1 ), 4 ( 2013 ).
  • Teschendorff AE , MarabitaF , LechnerMet al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data . Bioinformatics29 ( 2 ), 189 – 196 ( 2013 ).
  • Johnson WE , LiC , RabinovicA . Adjusting batch effects in microarray expression data using empirical Bayes methods . Biostatistics8 ( 1 ), 118 – 127 ( 2007 ).
  • Bates D , MächlerM , BolkerB , WalkerS . Fitting linear mixed-effects models using lme4 . J. Stat. Softw.67 ( 1 ), 48 ( 2015 ).
  • Gillis J , MistryM , PavlidisP . Gene function analysis in complex data sets using ErmineJ . Nat. Protoc.5 ( 6 ), 1148 – 1159 ( 2010 ).
  • Gillis J , PavlidisP . The impact of multifunctional genes on “guilt by association” analysis . PLoS ONE6 ( 2 ), e17258 ( 2011 ).