DNA Methylation of Imprinted Genes in Mexican–American Newborn Children with Prenatal Phthalate Exposure

References

• 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
• Barker DJ . The origins of the developmental origins theory . J. Intern. Med.261 ( 5 ), 412 – 417 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Baccarelli A , BollatiV . Epigenetics and environmental chemicals . Curr. Opin. Pediatr.21 ( 2 ), 243 – 251 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Feil R , FragaM . Epigenetics and the environment: emerging patterns and implications . Nat. Rev. Genet.13 , 97 – 109 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Foley DL , CraigJM , MorleyRet al. Prospects for epigenetic epidemiology . Am. J. Epidemiol.169 ( 4 ), 389 – 400 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Jaenisch R , BirdA . Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals . Nat. Genet.33 , 245 – 254 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Barlow DP , BartolomeiMS . Genomic imprinting in mammals . Cold Spring Harb. Perspect. Biol.6 ( 2 ), 1 – 20 ( 2014 ).
   Web of Science ®Google Scholar
• Murphy SK , HuangZ , HoyoC . Differentially methylated regions of imprinted genes in prenatal, perinatal and postnatal human tissues . PLoS ONE7 ( 7 ), e40924 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Wilkins JF , UbedaF , Van CleveJ . The evolving landscape of imprinted genes in humans and mice: conflict among alleles, genes, tissues and kin . Bioessays38 , 482 – 489 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Reik W , WalterJ . Genomic imprinting: parental influence on the genome . Nat. Rev. Genet.2 ( 1 ), 21 – 32 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Heijmans BT , TobiEW , SteinADet al. Persistent epigenetic differences associated with prenatal exposure to famine in humans . Proc. Natl Acad. Sci. USA105 ( 44 ), 17046 – 17049 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Hoyo C , MurthaAP , SchildkrautJMet al. Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy . Epigenetics6 ( 7 ), 928 – 936 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Lee HS , Barraza-VillarrealA , BiessyCet al. Dietary supplementation with polyunsaturated fatty acid during pregnancy modulates DNA methylation at IGF2/H19 imprinted genes and growth of infants . Physiol. Genomics46 ( 23 ), 851 – 857 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Qian YY , HuangXL , LiangHet al. Effects of maternal folic acid supplementation on gene methylation and being small for gestational age . J. Hum. Nutr. Diet.29 ( 5 ), 643 – 651 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Murphy SK , AdigunA , HuangZet al. Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke . Gene494 ( 1 ), 36 – 43 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Vidal AC , MurphySK , MurthaAPet al. Associations between antibiotic exposure during pregnancy, birth weight and aberrant methylation at imprinted genes among offspring . Int. J. Obes. (Lond.)37 ( 7 ), 907 – 913 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Vidal AC , SemenovaV , DarrahTet al. Maternal cadmium, iron and zinc levels, DNA methylation and birth weight . BMC Pharmacol. Toxicol.16 , doi:10.1186/s40360-015-0020-2 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Nye MD , HoyoC , MurphySK . In vitro lead exposure changes DNA methylation and expression of IGF2 and PEG1/MEST . Toxicol. In Vitro29 ( 3 ), 544 – 550 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Li Y , XieC , MurphySKet al. Lead exposure during early human development and DNA methylation of imprinted gene regulatory elements in adulthood . Environ. Health Perspect.124 ( 5 ), 666 – 673 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Nye MD , KingKE , DarrahTHet al. Maternal blood lead concentrations, DNA methylation of MEG3 DMR regulating the DLK1/MEG3 imprinted domain and early growth in a multiethnic cohort . Environ. Epigenet.2 ( 1 ), 1 – 8 ( 2016 ).
   Web of Science ®Google Scholar
• Goodrich JM , SanchezBN , DolinoyDCet al. Quality control and statistical modeling for environmental epigenetics: a study on in utero lead exposure and DNA methylation at birth . Epigenetics10 ( 1 ), 19 – 30 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Rojas D , RagerJE , SmeesterLet al. Prenatal arsenic exposure and the epigenome: identifying sites of 5-methylcytosine alterations that predict functional changes in gene expression in newborn cord blood and subsequent birth outcomes . Toxicol. Sci.143 ( 1 ), 97 – 106 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Mansell T , NovakovicB , MeyerBet al. The effects of maternal anxiety during pregnancy on IGF2/H19 methylation in cord blood . Transl. Psychiatry6 , e765 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Vidal AC , Benjamin NeelonSE , LiuYet al. Maternal stress, preterm birth, and DNA methylation at imprint regulatory sequences in humans . Genet. Epigenet.6 , 37 – 44 ( 2014 ).
   PubMedGoogle Scholar
• LaRocca J , BinderAM , McElrathTF , MichelsKB . The impact of first trimester phthalate and phenol exposure on IGF2/H19 genomic imprinting and birth outcomes . Environ. Res.133 , 396 – 406 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Goodrich JM , DolinoyDG , SanchezBNet al. Adolescent epigenetic profiles and environmental exposures from early life through peri-adolscence . Environ. Epigenet.2 ( 3 ), 1 – 11 ( 2016 ).
   Google Scholar
• Zhao Y , ChenJ , WangX , SongQ , XuHH , ZhangYH . Third trimester phthalate exposure is associated with DNA methylation of growth-related genes in human placenta . Sci. Rep.6 , 33449 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Silva MJ , BarrDB , ReidyJAet al. Urinary levels of seven phthalate metabolites in the US population from the National Health and Nutrition Examination Survey (NHANES) 1999–2000 . Environ. Health Perspect.112 ( 3 ), 331 – 338 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Woodruff TJ , ZotaAR , SchwartzJM . Environmental chemicals in pregnant women in the United States: NHANES 2003–2004 . Environ. Health Perspect.119 ( 6 ), 878 – 885 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• CDC, Fourth national report on human exposure to environmental chemicals . www.cdc.gov/exposurereport/pdf/FourthReport.pdf ( 2009 ).
   Google Scholar
• Smarr MM , GrantzKL , SundaramR , MaisogJM , KannanK , LouisGM . Parental urinary biomarkers of preconception exposure to bisphenol A and phthalates in relation to birth outcomes . Environ. Health14 , 1 – 11 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Zhang Y , LinL , CaoY , ChenB , ZhengL , GeRS . Phthalate levels and low birth weight: a nested case–control study of Chinese newborns . J. Pediatr.155 ( 4 ), 500 – 504 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• de Cock M , De BoerMR , LamoreeM , LeglerJ , Van De BorM . Prenatal exposure to endocrine disrupting chemicals and birth weight – a prospective cohort study . J. Environ. Sci. Health A Tox. Hazard Subst. Environ. Eng.51 ( 2 ), 178 – 185 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Whyatt RM , AdibiJJ , CalafatAMet al. Prenatal di(2-ethylhexyl)phthalate exposure and length of gestation among an inner-city cohort . Pediatrics124 ( 6 ), e1213 – e1220 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Weinberger B , VetranoAM , ArcherFEet al. Effects of maternal exposure to phthalates and bisphenol A during pregnancy on gestational age . J. Matern. Fetal Neonatal Med.27 ( 4 ), 323 – 327 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Ferguson KK , McElrathTF , MeekerJD . Environmental phthalate exposure and preterm birth . JAMA Pediatr.168 ( 1 ), 61 – 67 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Meeker JD , HuH , CantonwineDEet al. Urinary phthalate metabolites in relation to preterm birth in Mexico city . Environ. Health Perspect.117 ( 10 ), 1587 – 1592 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Valvi D , CasasM , RomagueraDet al. Prenatal phthalate exposure and childhood growth and blood pressure: evidence from the Spanish INMA-Sabadell birth cohort study . Environ. Health Perspect.123 ( 10 ), 1022 – 1029 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Kim Y , HaEH , KimEJet al. Prenatal exposure to phthalates and infant development at 6 months: prospective Mothers and Children’s Environmental Health (MOCEH) study . Environ. Health Perspect.119 ( 10 ), 1495 – 1500 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Engel SM , MiodovnikA , CanfieldRLet al. Prenatal phthalate exposure is associated with childhood behavior and executive functioning . Environ. Health Perspect.118 ( 4 ), 565 – 571 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Whyatt RM , PerzanowskiMS , JustACet al. Asthma in inner-city children at 5–11 years of age and prenatal exposure to phthalates: the Columbia Center for Children’s Environmental Health Cohort . Environ. Health Perspect.122 ( 10 ), 1141 – 1146 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Kostka G , Urbanek-OlejnikK , WiadrowskaB . Di-butyl phthalate-induced hypomethylation of the c-myc gene in rat liver . Toxicol. Ind. Health26 ( 7 ), 407 – 416 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Martinez-Arguelles DB , PapadopoulosV . Identification of hot spots of DNA methylation in the adult male adrenal in response to in utero exposure to the ubiquitous endocrine disruptor plasticizer di-(2-ethylhexyl) phthalate . Endocrinology156 ( 1 ), 124 – 133 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Pogribny IP , TryndyakVP , BoureikoAet al. Mechanisms of peroxisome proliferator-induced DNA hypomethylation in rat liver . Mutat. Res.644 ( 1–2 ), 17 – 23 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Wu S , ZhuJ , LiYet al. Dynamic epigenetic changes involved in testicular toxicity induced by di-2-(ethylhexyl) phthalate in mice . Basic Clin. Pharmacol. Toxicol.106 ( 2 ), 118 – 123 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Huen K , CalafatAM , BradmanA , YousefiP , EskenaziB , HollandN . Maternal phthalate exposure during pregnancy is associated with DNA methylation of LINE-1 and Alu repetitive elements in Mexican–American children . Environ. Res.148 , 55 – 62 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Solomon O , YousefiP , HuenKet al. Prenatal phthalate exposure and altered patterns of DNA methylation in cord blood . Environ. Mol. Mutagen.58 ( 6 ), 398 – 410 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Eskenazi B , KogutK , HuenKet al. Organophosphate pesticide exposure, PON1, and neurodevelopment in school-age children from the CHAMACOS study . Environ. Res.134 , 149 – 157 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Holland N , HuenK , TranVet al. Urinary phthalate metabolites and biomarkers of oxidative stress in a Mexican–American cohort: variability in early and late pregnancy . Toxics4 ( 1 ), ( 2016 ).
   PubMedGoogle Scholar
• Holland N , FurlongC , BastakiMet al. Paraoxonase polymorphisms, haplotypes, and enzyme activity in Latino mothers and newborns . Environ. Health Perspect.114 ( 7 ), 985 – 991 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Silva MJ , SamandarE , PreauJLJr , ReidyJA , NeedhamLL , CalafatAM . Quantification of 22 phthalate metabolites in human urine . J. Chromatogr. B Analyt. Technol. Biomed. Life. Sci.860 ( 1 ), 106 – 112 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Harley KG , BergerK , RauchSet al. Association of prenatal urinary phthalate metabolite concentrations and childhood BMI and obesity . Pediatr. Res.82 ( 3 ), 405 – 415 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Parlett LE , CalafatAM , SwanSH . Women’s exposure to phthalates in relation to use of personal care products . J. Expo. Sci. Environ. Epidemiol.23 ( 2 ), 197 – 206 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lubin JH , ColtJS , CamannDet al. Epidemiologic evaluation of measurement data in the presence of detection limits . Environ. Health Perspect.112 ( 17 ), 1691 – 1696 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Zota AR , CalafatAM , WoodruffTJ . Temporal trends in phthalate exposures: findings from the National Health and Nutrition Examination Survey, 2001–2010 . Environ. Health Perspect.122 ( 3 ), 235 – 241 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Nye MD , HoyoC , HuangZet al. Associations between methylation of paternally expressed gene 3 (PEG3), cervical intraepithelial neoplasia and invasive cervical cancer . PLoS ONE8 ( 2 ), e56325 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Zhao J , DahleD , ZhouY , ZhangX , KlibanskiA . Hypermethylation of the promoter region is associated with the loss of MEG3 gene expression in human pituitary tumors . J. Clin. Endocrinol. Metab.90 ( 4 ), 2179 – 2186 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Gejman R , BatistaDL , ZhongYet al. Selective loss of MEG3 expression and intergenic differentially methylated region hypermethylation in the MEG3/DLK1 locus in human clinically nonfunctioning pituitary adenomas . J. Clin. Endocrinol. Metab.93 ( 10 ), 4119 – 4125 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Otsuka S , MaegawaS , TakamuraAet al. Aberrant promoter methylation and expression of the imprinted PEG3 gene in glioma . Proc. Jpn Acad. Ser. B Phys. Biol. Sci.85 ( 4 ), 157 – 165 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Rezvani G , LuiJC , BarnesKM , BaronJ . A set of imprinted genes required for normal body growth also promotes growth of rhabdomyosarcoma cells . Pediatr. Res.71 ( 1 ), 32 – 38 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Soubry A , GuoL , HuangZet al. Obesity-related DNA methylation at imprinted genes in human sperm: results from the TIEGER study . Clin. Epigenetics8 , 1 – 11 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Yousefi P , HuenK , QuachHet al. Estimation of blood cellular heterogeneity in newborns and children for epigenome-wide association studies . Environ. Mol. Mutagen.56 ( 9 ), 751 – 758 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Houseman EA , AccomandoWP , KoestlerDCet al. DNA methylation arrays as surrogate measures of cell mixture distribution . BMC Bioinformatics13 , 1 – 16 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Bakulski KM , FeinbergJI , AndrewsSVet al. DNA methylation of cord blood cell types: applications for mixed cell birth studies . Epigenetics11 ( 5 ), 354 – 362 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Yousefi P , HuenK , Aguilar SchallRet al. Considerations for normalization of DNA methylation data by Illumina 450K BeadChip assay in population studies . Epigenetics8 ( 11 ), 1141 – 1152 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Du P , ZhangX , HuangCCet al. Comparison of beta-value and M-value methods for quantifying methylation levels by microarray analysis . BMC Bioinformatics11 , 1 – 9 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Wasserman L . Multiple testing . In : All of Statistics: A Concise Course in Statistical Inference . Springer , NY, USA , 165 – 168 ( 2004 ).
   Google Scholar
• Soubry A , MurphySK , WangFet al. Newborns of obese parents have altered DNA methylation patterns at imprinted genes . Int. J. Obes. (Lond.)39 ( 4 ), 650 – 657 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Hoyo C , DaltveitAK , IversenEet al. Erythrocyte folate concentrations, CpG methylation at genomically imprinted domains, and birth weight in a multiethnic newborn cohort . Epigenetics9 ( 8 ), 1120 – 1130 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Kappil MA , GreenBB , ArmstrongDAet al. Placental expression profile of imprinted genes impacts birth weight . Epigenetics10 ( 9 ), 842 – 849 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• McMinn J , WeiM , SchupfNet al. Unbalanced placental expression of imprinted genes in human intrauterine growth restriction . Placenta27 ( 6–7 ), 540 – 549 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Zhang X , GejmanR , MahtaAet al. Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression . Cancer Res.70 ( 6 ), 2350 – 2358 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Kawakami T , ChanoT , MinamiK , OkabeH , OkadaY , OkamotoK . Imprinted DLK1 is a putative tumor suppressor gene and inactivated by epimutation at the region upstream of GTL2 in human renal cell carcinoma . Hum. Mol. Genet.15 ( 6 ), 821 – 830 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Benetatos L , DasoulaA , HatzimichaelE , GeorgiouI , SyrrouM , BourantasKL . Promoter hypermethylation of the MEG3 (DLK1/MEG3) imprinted gene in multiple myeloma . Clin. Lymphoma Myeloma8 ( 3 ), 171 – 175 ( 2008 ).
   PubMedGoogle Scholar
• Benetatos L , HatzimichaelE , DasoulaAet al. CpG methylation analysis of the MEG3 and SNRPN imprinted genes in acute myeloid leukemia and myelodysplastic syndromes . Leuk. Res.34 ( 2 ), 148 – 153 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Astuti D , LatifF , WagnerKet al. Epigenetic alteration at the DLK1-GTL2 imprinted domain in human neoplasia: analysis of neuroblastoma, phaeochromocytoma and Wilms’ tumour . Br. J. Cancer92 ( 8 ), 1574 – 1580 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Kameswaran V , KaestnerKH . The missing lnc(RNA) between the pancreatic beta-cell and diabetes . Front. Genet.5 , 200 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Kameswaran V , BramswigNC , McKennaLBet al. Epigenetic regulation of the DLK1-MEG3 microRNA cluster in human type 2 diabetic islets . Cell. Metab.19 ( 1 ), 135 – 145 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• You L , WangN , YinDet al. Downregulation of long noncoding RNA Meg3 affects insulin synthesis and secretion in mouse pancreatic beta cells . J. Cell. Physiol.231 ( 4 ), 852 – 862 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Martin EM , FryRC . A cross-study analysis of prenatal exposures to environmental contaminants and the epigenome: support for stress-responsive transcription factor occupancy as a mediator of gene-specific CpG methylation patterning . Environ. Epigenet.2 ( 1 ), 1 – 9 ( 2016 ).
   Google Scholar