Sex- and Tissue-Specific Effects of Binge-Level Prenatal Alcohol Consumption on DNA Methylation at Birth

References

• May PA , BlankenshipJ , MaraisASet al. Maternal alcohol consumption producing fetal alcohol spectrum disorders (FASD): quantity, frequency, and timing of drinking. Drug. Alcohol Depend.133(2), 502–512 (2013).
   PubMed Web of Science ®Google Scholar
• Reid N . Fetal alcohol spectrum disorder in Australia: what is the current state of affairs?Drug. Alcohol Rev.37(7), 827–830 (2018).
   PubMed Web of Science ®Google Scholar
• Bower C , WatkinsRE , MutchRCet al. Fetal alcohol spectrum disorder and youth justice: a prevalence study among young people sentenced to detention in Western Australia. BMJ Open8(2), e019605 (2018).
   PubMed Web of Science ®Google Scholar
• O’Keeffe LM , KearneyPM , GreeneRAet al. Maternal alcohol use during pregnancy and offspring trajectories of height and weight: a prospective cohort study. Drug Alcohol Depend.153, 323–329 (2015).
   PubMed Web of Science ®Google Scholar
• O’Leary C , JacobyP , D’AntoineHet al. Heavy prenatal alcohol exposure and increased risk of stillbirth. BJOG119(8), 945–952 (2012).
   PubMed Web of Science ®Google Scholar
• Fan J , JacobsonSW , TaylorPAet al. White matter deficits mediate effects of prenatal alcohol exposure on cognitive development in childhood. Hum. Brain Mapp.37(8), 2943–2958 (2016).
   PubMed Web of Science ®Google Scholar
• O’Leary CM , WatsonL , D’AntoineHet al. Heavy maternal alcohol consumption and cerebral palsy in the offspring. Dev. Med. Child Neurol.54(3), 224–230 (2012).
   PubMed Web of Science ®Google Scholar
• Muggli E , O’LearyC , ForsterDet al. Study protocol: Asking QUestions about Alcohol in pregnancy (AQUA): a longitudinal cohort study of fetal effects of low to moderate alcohol exposure. BMC Pregnancy Childbirth14, 302 (2014).
   PubMed Web of Science ®Google Scholar
• Muggli E , O’LearyC , DonathSet al. ‘Did you ever drink more?’ A detailed description of pregnant women’s drinking patterns. BMC Public Health16, 683 (2016).
   PubMed Web of Science ®Google Scholar
• Borsani E , DellaVedova AM , RezzaniRet al. Correlation between human nervous system development and acquisition of fetal skills: an overview. Brain Dev.41(3), 225–233 (2019).
   PubMed Web of Science ®Google Scholar
• Muggli E , MatthewsH , PeningtonAet al. Association between prenatal alcohol exposure and craniofacial shape of children at 12 months of age. JAMA Pediatr.171(8), 771–780 (2017).
   PubMed Web of Science ®Google Scholar
• Halliday JL , MuggliE , LewisSet al. Alcohol consumption in a general antenatal population and child neurodevelopment at 2 years. J. Epidemiol. Community Health71(10), 990–998 (2017).
   PubMed Web of Science ®Google Scholar
• Kilburn TR , EriksenHL , UnderbjergMet al. Low to moderate average alcohol consumption and binge drinking in early pregnancy: effects on choice reaction time and information processing time in five-year-old children. PLoS ONE10(9), e0138611 (2015).
   PubMed Web of Science ®Google Scholar
• Nulman I , RovetJ , KennedyDet al. Binge alcohol consumption by non-alcohol-dependent women during pregnancy affects child behaviour, but not general intellectual functioning; a prospective controlled study. Arch. Womens Ment. Health7(3), 173–181 (2004).
   PubMedGoogle Scholar
• Godfrey KM , CostelloPM , LillycropKA. The developmental environment, epigenetic biomarkers and long-term health. J. Dev. Orig. Health Dis.6(5), 399–406 (2015).
   PubMed Web of Science ®Google Scholar
• Waterland RA , MichelsKB. Epigenetic epidemiology of the developmental origins hypothesis. Annu. Rev. Nutr.27, 363–388 (2007).
   PubMed Web of Science ®Google Scholar
• Bianco-Miotto T , CraigJM , GasserYPet al. Epigenetics and DOHaD: from basics to birth and beyond. J. Dev. Orig. Health Dis.8(5), 513–519 (2017).
   PubMed Web of Science ®Google Scholar
• Portales-Casamar E , LussierAA , JonesMJet al. DNA methylation signature of human fetal alcohol spectrum disorder. Epigenetics Chromatin9, 25 (2016).
   PubMed Web of Science ®Google Scholar
• Cobben JM , KrzyzewskaIM , VenemaAet al. DNA methylation abundantly associates with fetal alcohol spectrum disorder and its subphenotypes. Epigenomics11(7), 767–785 (2019).
   PubMed Web of Science ®Google Scholar
• Laufer BI , Chater-DiehlEJ , KapalangaJ , SinghSM. Long-term alterations to DNA methylation as a biomarker of prenatal alcohol exposure: from mouse models to human children with fetal alcohol spectrum disorders. Alcohol60, 67–75 (2017).
   PubMed Web of Science ®Google Scholar
• Laufer BI , KapalangaJ , CastellaniCA , DiehlEJ , YanL , SinghSM. Associative DNA methylation changes in children with prenatal alcohol exposure. Epigenomics7(8), 1259–1274 (2015).
   PubMed Web of Science ®Google Scholar
• Lussier AA , MorinAM , MacisaacJLet al. DNA methylation as a predictor of fetal alcohol spectrum disorder. Clin. Epigenetics10, 5 (2018).
   PubMed Web of Science ®Google Scholar
• Rogic S , WongA , PavlidisP. Meta-analysis of gene expression patterns in animal models of prenatal alcohol exposure suggests role for protein synthesis inhibition and chromatin remodeling. Alcohol Clin. Exp. Res.40(4), 717–727 (2016).
   PubMed Web of Science ®Google Scholar
• Okazaki S , OtsukaI , ShinkoYet al. Epigenetic clock analysis in children with fetal alcohol spectrum disorder. Alcohol Clin. Exp. Res.45(2), 329–337 (2021).
   PubMedGoogle Scholar
• Nguyen VB , ProbynME , CampbellFet al. Low-dose maternal alcohol consumption: effects in the hearts of offspring in early life and adulthood. Physiol. Rep.2(7), (2014).
   Google Scholar
• Kleiber ML , DiehlEJ , LauferBIet al. Long-term genomic and epigenomic dysregulation as a consequence of prenatal alcohol exposure: a model for fetal alcohol spectrum disorders. Front. Genet.5, 161 (2014).
   PubMed Web of Science ®Google Scholar
• Gangisetty O , WynneO , JabbarSet al. Fetal alcohol exposure reduces dopamine receptor D2 and Increases pituitary weight and prolactin production via epigenetic mechanisms. PLoS ONE10(10), e0140699 (2015).
   PubMed Web of Science ®Google Scholar
• Boschen KE , McKeownSE , RothTL , KlintsovaAY. Impact of exercise and a complex environment on hippocampal dendritic morphology, Bdnf gene expression, and DNA methylation in male rat pups neonatally exposed to alcohol. Dev. Neurobiol.77(6), 708–725 (2017).
   PubMed Web of Science ®Google Scholar
• Probyn ME , LockEK , AndersonSTet al. The effect of low-to-moderate-dose ethanol consumption on rat mammary gland structure and function and early postnatal growth of offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol.304(10), R791–798 (2013).
   PubMed Web of Science ®Google Scholar
• Gardebjer EM , AndersonST , PantaleonMet al. Maternal alcohol intake around the time of conception causes glucose intolerance and insulin insensitivity in rat offspring, which is exacerbated by a postnatal high-fat diet. FASEB J29(7), 2690–2701 (2015).
   PubMed Web of Science ®Google Scholar
• Loke YJ , MuggliE , NguyenLet al. Time- and sex-dependent associations between prenatal alcohol exposure and placental global DNA methylation. Epigenomics10(7), 981–991 (2018).
   PubMedGoogle Scholar
• Sharp GC , ArathimosR , ReeseSEet al. Maternal alcohol consumption and offspring DNA methylation: findings from six general population-based birth cohorts. Epigenomics10(1), 27–42 (2018).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMedGoogle Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Kalisch-Smith JI , SteaneSE , SimmonsDGet al. Periconceptional alcohol exposure causes female-specific perturbations to trophoblast differentiation and placental formation in the rat. Development146(11), (2019).
   PubMed Web of Science ®Google Scholar
• Terasaki LS , GomezJ , SchwarzJM. An examination of sex differences in the effects of early-life opiate and alcohol exposure. Philos. Trans. R. Soc. Lond. B Biol. Sci.371(1688), 20150123 (2016).
   PubMed Web of Science ®Google Scholar
• Treit S , ChenZ , ZhouDet al. Sexual dimorphism of volume reduction but not cognitive deficit in fetal alcohol spectrum disorders: a combined diffusion tensor imaging, cortical thickness and brain volume study. Neuroimage Clin.15, 284–297 (2017).
   PubMed Web of Science ®Google Scholar
• Converse AK , MooreCF , HoldenJEet al. Moderate-level prenatal alcohol exposure induces sex differences in dopamine d1 receptor binding in adult rhesus monkeys. Alcohol Clin. Exp. Res.38(12), 2934–2943 (2014).
   PubMed Web of Science ®Google Scholar
• Ireland P , JolleyD , GilesGet al. Development of the Melbourne FFQ: a food frequency questionnaire for use in an Australian prospective study involving an ethnically diverse cohort. Asia Pac. J. Clin. Nutr.3(1), 19–31 (1994).
   PubMedGoogle Scholar
• Hodge A , PattersonAJ , BrownWJet al. The Anti Cancer Council of Victoria FFQ: relative validity of nutrient intakes compared with weighed food records in young to middle-aged women in a study of iron supplementation. Aust. N. Z. J. Public Health24(6), 576–583 (2000).
   PubMed Web of Science ®Google Scholar
• Richardson JR , PeacockSJ , HawthorneGet al. Construction of the descriptive system for the Assessment of Quality of Life AQoL-6D utility instrument. Health Qual. Life Outcomes10, 38 (2012).
   PubMed Web of Science ®Google Scholar
• Ollikainen M , SmithKR , JooEJet al. DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum Mol Genet19(21), 4176–4188 (2010).
   PubMed Web of Science ®Google Scholar
• Bibikova M , BarnesB , TsanCet al. High density DNA methylation array with single CpG site resolution. Genomics98(4), 288–295 (2011).
   PubMed Web of Science ®Google Scholar
• Sandoval J , HeynH , MoranSet al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics6(6), 692–702 (2011).
   PubMed Web of Science ®Google Scholar
• Aryee MJ , JaffeAE , Corrada-BravoHet al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics30(10), 1363–1369 (2014).
   PubMed Web of Science ®Google Scholar
• Ritchie ME , PhipsonB , WuDet al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res.43(7), e47 (2015).
   PubMed Web of Science ®Google Scholar
• Phipson B , MaksimovicJ , OshlackA. missMethyl: an R package for analyzing data from Illumina’s HumanMethylation450 platform. Bioinformatics32(2), 286–288 (2016).
   PubMed Web of Science ®Google Scholar
• Leek JT , JohnsonWE , ParkerHSet al. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics28(6), 882–883 (2012).
   PubMed Web of Science ®Google Scholar
• Teschendorff AE , BreezeCE , ZhengSC , BeckS. A comparison of reference-based algorithms for correcting cell-type heterogeneity in Epigenome-Wide Association Studies. BMC Bioinformatics18(1), 105 (2017).
   PubMedGoogle Scholar
• Wu Z , AryeeMJ. Subset quantile normalization using negative control features. J. Comput. Biol.17(10), 1385–1395 (2010).
   PubMed Web of Science ®Google Scholar
• Johnson WE , LiC , RabinovicA. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics8(1), 118–127 (2007).
   PubMed Web of Science ®Google Scholar
• Zheng SC , WebsterAP , DongDet al. A novel cell-type deconvolution algorithm reveals substantial contamination by immune cells in saliva, buccal and cervix. Epigenomics10(7), 925–940 (2018).
   PubMed Web of Science ®Google Scholar
• Saffari A , SilverMJ , ZavattariPet al. Estimation of a significance threshold for epigenome-wide association studies. Genet. Epidemiol.42(1), 20–33 (2018).
   PubMed Web of Science ®Google Scholar
• Dempster EL , PidsleyR , SchalkwykLCet al. Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum Mol Genet20(24), 4786–4796 (2011).
   PubMed Web of Science ®Google Scholar
• Wong CC , MeaburnEL , RonaldAet al. Methylomic analysis of monozygotic twins discordant for autism spectrum disorder and related behavioural traits. Mol. Psychiatry19(4), 495–503 (2014).
   PubMed Web of Science ®Google Scholar
• Wong CC , ParsonsMJ , LesterKJet al. Epigenome-wide DNA methylation analysis of monozygotic twins discordant for diurnal preference. Twin Res. Hum. Genet.18(6), 662–669 (2015).
   PubMed Web of Science ®Google Scholar
• Kushwaha G , DozmorovM , WrenJDet al. Hypomethylation coordinates antagonistically with hypermethylation in cancer development: a case of study of leukemia. Human Genomics10 (2016).
   PubMed Web of Science ®Google Scholar
• Luján S , CaroppoE , NiederbergerCet al. Sperm DNA methylation epimutation biomarkers for male infertility and FSH therapeutic responsiveness. Sci. Rep.9(1), 16786 (2019).
   PubMedGoogle Scholar
• Peters TJ , BuckleyMJ , StathamALet al. De novo identification of differentially methylated regions in the human genome. Epigenetics Chromatin8, 6 (2015).
   PubMed Web of Science ®Google Scholar
• Satterthwaite FE . An approximate distribution of estimates of variance components. Biometrics2(6), 110–114 (1946).
   PubMed Web of Science ®Google Scholar
• Benjamini Y , HochbergY. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. Series B (Methodol.)57(1), 289–300 (1995).
   Web of Science ®Google Scholar
• Yadav DK , ShresthaS , LillycropKAet al. Vitamin B12 supplementation influences methylation of genes associated with Type 2 diabetes and its intermediate traits. Epigenomics10(1), 71–90 (2018).
   PubMed Web of Science ®Google Scholar
• Wijchers PJ , FestensteinRJ. Epigenetic regulation of autosomal gene expression by sex chromosomes. Trends Genet.27(4), 132–140 (2011).
   PubMed Web of Science ®Google Scholar
• Hartman RJG , HuismanSE , den RuijterHM. Sex differences in cardiovascular epigenetics – a systematic review. Biol. Sex Differ.9(19), (2018).
   PubMedGoogle Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Lussier AA . Epigenetic signatures of prenatal alcohol exposure[PhD thesis]. University British Columbia, BC, Canada. (2017).
   Google Scholar
• Ziats MN , RennertOM. Aberrant expression of long noncoding RNAs in autistic brain. J. Mol. Neurosci.49(3), 589–593 (2013).
   PubMed Web of Science ®Google Scholar
• Maltby VE , LeaRA , SandersKAet al. Differential methylation at MHC in CD4(+) T cells is associated with multiple sclerosis independently of HLA-DRB1. Clin. Epigenetics9, 71 (2017).
   PubMed Web of Science ®Google Scholar
• Su Q , CaiQ , GerwinC , SmithCL , ShengZH. Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat. Cell. Biol.6(10), 941–953 (2004).
   PubMed Web of Science ®Google Scholar
• Cai Q , GerwinC , ShengZH. Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J. Cell. Biol.170(6), 959–969 (2005).
   PubMed Web of Science ®Google Scholar
• Cai Q , PanPY , ShengZH. Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J. Neurosci.27(27), 7284–7296 (2007).
   PubMed Web of Science ®Google Scholar
• Funakoshi E , HamanoA , FukuiMet al. Molecular cloning of the m-Golsyn gene and its expression in the mouse brain. Gene Expr.13(1), 27–40 (2006).
   PubMed Web of Science ®Google Scholar
• Yue F , ChengY , BreschiAet al. A comparative encyclopedia of DNA elements in the mouse genome. Nature515(7527), 355–364 (2014).
   PubMed Web of Science ®Google Scholar
• Xiong GJ , ChengXT , SunTet al. Defects in syntabulin-mediated synaptic cargo transport associate with autism-like synaptic dysfunction and social behavioral traits. Mol Psychiatry26, 1472–1490 (2020).
   PubMed Web of Science ®Google Scholar
• Bereczki E , BrancaRM , FrancisPTet al. Synaptic markers of cognitive decline in neurodegenerative diseases: a proteomic approach. Brain141(2), 582–595 (2018).
   PubMedGoogle Scholar
• Richmond RC , SimpkinAJ , WoodwardGet al. Prenatal exposure to maternal smoking and offspring DNA methylation across the lifecourse: findings from the Avon Longitudinal Study of Parents and Children (ALSPAC). Hum Mol Genet24(8), 2201–2217 (2015).
   PubMed Web of Science ®Google Scholar
• Joubert BR , HabergSE , NilsenRMet al. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ. Health Perspect.120(10), 1425–1431 (2012).
   PubMed Web of Science ®Google Scholar
• Muggli E , CookB , O’LearyCet al. Increasing accurate self-report in surveys of pregnancy alcohol use. Midwifery31(3), e23–28 (2015).
   PubMed Web of Science ®Google Scholar
• Mohandas N , Bass-StringerS , MaksimovicJet al. Epigenome-wide analysis in newborn blood spots from monozygotic twins discordant for cerebral palsy reveals consistent regional differences in DNA methylation. Clin. Epigenetics10, 25 (2018).
   PubMed Web of Science ®Google Scholar
• Mohandas N , LokeYJ , HopkinsSet al. Evidence for type-specific DNA methylation patterns in epilepsy: a discordant monozygotic twin approach. Epigenomics11(8), 951–968 (2019).
   PubMed Web of Science ®Google Scholar
• Martino D , LokeYJ , GordonLet al. Longitudinal, genome-scale analysis of DNA methylation in twins from birth to 18 months of age reveals rapid epigenetic change in early life and pair-specific effects of discordance. Genome Biol.14(5), R42 (2013).
   PubMed Web of Science ®Google Scholar