282
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Early Life Lead Exposure Causes Gender-Specific Changes in the DNA Methylation Profile of DNA Extracted from Dried Blood Spots

, , , , , , , & show all
Pages 379-393 | Published online: 16 Jun 2015

References

  • Glorennec P , BemrahN , TardA , RobinA , Le BotB , BardD . Probabilistic modeling of young children’s overall lead exposure in France: integrated approach for various exposure media . Environ. Int.33 ( 7 ), 937 – 945 ( 2007 ).
  • Jakubowski M . Low-level environmental lead exposure and intellectual impairment in children – the current concepts of risk assessment . Int. J. Occup. Med. Environ. health24 ( 1 ), 1 – 7 ( 2011 ).
  • Christie NT , CostaM . In vitro assessment of the toxicity of metal compounds: IV. disposition of metals in cells: interactions with membranes, glutathione, metallothionein, and DNA . Biol. Trace Elem. Res.6 ( 2 ), 139 – 158 ( 1984 ).
  • Farant JP , WigfieldDC . Biomonitoring lead exposure with delta-aminolevulinate dehydratase (ALA-D) activity ratios . Int. Arch. Occup. Environ. Health51 ( 1 ), 15 – 24 ( 1982 ).
  • Bakulski KM , RozekLS , DolinoyDC , PaulsonHL , HuH . Alzheimer’s disease and environmental exposure to lead: the epidemiologic evidence and potential role of epigenetics . Curr. Alzheimer Res.9 ( 5 ), 563 – 573 ( 2012 ).
  • Altmann L , GutowskiM , WiegandH . Effects of maternal lead exposure on functional plasticity in the visual cortex and hippocampus of immature rats . Brain Res. Dev. Brain Res.81 ( 1 ), 50 – 56 ( 1994 ).
  • Wolff MS , BrittonJA , BoguskiLet al. Environmental exposures and puberty in inner-city girls . Environ. Res.107 ( 3 ), 393 – 400 ( 2008 ).
  • Lawrence DA , MccabeMJJr . Immunomodulation by metals . Int. Immunopharmacol.2 ( 2–3 ), 293 – 302 ( 2002 ).
  • Hirsch HV , MercerJ , SambaziotisHet al. Behavioral effects of chronic exposure to low levels of lead in Drosophila melanogaster . Neurotoxicology24 ( 3 ), 435 – 442 ( 2003 ).
  • Schneider JS , TalsaniaK , MettilW , AndersonDW . Genetic diversity influences the response of the brain to developmental lead exposure . Toxicol. Sci. ( 2014 ).
  • Sobin C , ParisiN , SchaubT , GutierrezM , OrtegaAX . delta-Aminolevulinic acid dehydratase single nucleotide polymorphism 2 and peptide transporter 2*2 haplotype may differentially mediate lead exposure in male children . Arch. Environ. Contam. Toxicol.61 ( 3 ), 521 – 529 ( 2011 ).
  • Kulis M , QueirosAC , BeekmanR , Martin-SuberoJI . Intragenic DNA methylation in transcriptional regulation, normal differentiation and cancer . Biochim. Biophys. Acta1829 ( 11 ), 1161 – 1174 ( 2013 ).
  • Tate PH , BirdAP . Effects of DNA methylation on DNA-binding proteins and gene expression . Curr. Opin. Genet. Dev.3 ( 2 ), 226 – 231 ( 1993 ).
  • Jaenisch R , BirdA . Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals . Nat. Genet.33 ( Suppl. ), 245 – 254 ( 2003 ).
  • Hendrich B , BirdA . Identification and characterization of a family of mammalian methyl-CpG binding proteins . Mol. Cell. Biol.18 ( 11 ), 6538 – 6547 ( 1998 ).
  • Hendrich B , TweedieS . The methyl-CpG binding domain and the evolving role of DNA methylation in animals . Trends Genet.19 ( 5 ), 269 – 277 ( 2003 ).
  • Arand J , SpielerD , KariusTet al. In vivo control of CpG and non-CpG DNA methylation by DNA methyltransferases . PLoS Genet.8 ( 6 ), e1002750 ( 2012 ).
  • Jones PA . Functions of DNA methylation: islands, start sites, gene bodies and beyond . Nat. Rev. Genet.13 ( 7 ), 484 – 492 ( 2012 ).
  • Cingolani P , CaoX , KhetaniRet al. Intronic non-CG DNA hydroxymethylation and alternative mRNA splicing in honey bees . BMC Genomics14 ( 1 ), 666 ( 2013 ).
  • Yoder JA , WalshCP , BestorTH . Cytosine methylation and the ecology of intragenomic parasites . Trends Genet.13 ( 8 ), 335 – 340 ( 1997 ).
  • Kile ML , BaccarelliA , HoffmanEet al. Prenatal arsenic exposure and DNA methylation in maternal and umbilical cord blood leukocytes . Environ. Health Perspect.120 ( 7 ), 1061 – 1066 ( 2012 ).
  • Wright RO , SchwartzJ , WrightRJet al. Biomarkers of lead exposure and DNA methylation within retrotransposons . Environ. Health Perspect.118 ( 6 ), 790 – 795 ( 2010 ).
  • Dosunmu R , AlashwalH , ZawiaNH . Genome-wide expression and methylation profiling in the aged rodent brain due to early-life Pb exposure and its relevance to aging . Mech. Ageing Dev.133 ( 6 ), 435 – 443 ( 2012 ).
  • Koestler DC , Avissar-WhitingM , HousemanEA , KaragasMR , MarsitCJ . Differential DNA methylation in umbilical cord blood of infants exposed to low levels of arsenic in utero . Environ. Health Perspect.121 ( 8 ), 971 – 977 ( 2013 ).
  • Hanna CW , BloomMS , RobinsonWPet al. DNA methylation changes in whole blood is associated with exposure to the environmental contaminants, mercury, lead, cadmium and bisphenol A, in women undergoing ovarian stimulation for IVF . Hum. Reprod.27 ( 5 ), 1401 – 1410 ( 2012 ).
  • Brubaker CJ , DietrichKN , LanphearBP , CecilKM . The influence of age of lead exposure on adult gray matter volume . Neurotoxicology31 ( 3 ), 259 – 266 ( 2010 ).
  • Jedrychowski W , PereraF , JankowskiJet al. Gender specific differences in neurodevelopmental effects of prenatal exposure to very low-lead levels: the prospective cohort study in three-year olds . Early Hum. Dev.85 ( 8 ), 503 – 510 ( 2009 ).
  • 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 ).
  • Jin P , WarrenST . New insights into fragile X syndrome: from molecules to neurobehaviors . Trends Biochem. Sci.28 ( 3 ), 152 – 158 ( 2003 ).
  • Sofer T , SchifanoED , HoppinJA , HouL , BaccarelliAA . A-clustering: a novel method for the detection of co-regulated methylation regions, and regions associated with exposure . Bioinformatics29 ( 22 ), 2884 – 2891 ( 2013 ).
  • Petronis KR , AnthonyJC . Social epidemiology, intra-neighbourhood correlation, and generalised estimating equations . J. Epidemiol. Community Health57 ( 11 ), 914 ( 2003 ).
  • Jurkowska RZ , JurkowskiTP , JeltschA . Structure and function of mammalian DNA methyltransferases . Chembiochem12 ( 2 ), 206 – 222 ( 2011 ).
  • Bibikova M , BarnesB , TsanCet al. High density DNA methylation array with single CpG site resolution . Genomics98 ( 4 ), 288 – 295 ( 2011 ).
  • Du P , ZhangX , HuangCCet al. Comparison of beta-value and M-value methods for quantifying methylation levels by microarray analysis . BMC Bioinformatics11 , 587 ( 2010 ).
  • 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 ).
  • Touleimat N , TostJ . Complete pipeline for Infinium((R)) Human Methylation 450K BeadChip data processing using subset quantile normalization for accurate DNA methylation estimation . Epigenomics4 ( 3 ), 325 – 341 ( 2012 ).
  • Johnson WE , LiC , RabinovicA . Adjusting batch effects in microarray expression data using empirical Bayes methods . Biostatistics8 ( 1 ), 118 – 127 ( 2007 ).
  • Barfield RT , KilaruV , SmithAK , ConneelyKN . CpGassoc: an R function for analysis of DNA methylation microarray data . Bioinformatics28 ( 9 ), 1280 – 1281 ( 2012 ).
  • Wessely F , EmesRD . Identification of DNA methylation biomarkers from Infinium arrays . Front. Genet.3 , 161 ( 2012 ).
  • Felsenfeld G . A brief history of epigenetics . Cold Spring Harbor Perspect. Biol.6 ( 1 ), ( 2014 ).
  • Barker DJ , ErikssonJG , ForsenT , OsmondC . Fetal origins of adult disease: strength of effects and biological basis . Int. J. Epidemiol.31 ( 6 ), 1235 – 1239 ( 2002 ).
  • Haworth KE , FarrellWE , EmesRDet al. Combined influence of gene-specific cord blood methylation and maternal smoking habit on birth weight . Epigenomics5 ( 1 ), 37 – 49 ( 2013 ).
  • Hsiung DT , MarsitCJ , HousemanEAet al. Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma . Cancer Epidemiol. Biomarkers Prev.16 ( 1 ), 108 – 114 ( 2007 ).
  • Liu Y , AryeeMJ , PadyukovLet al. Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis . Nat. Biotechnol.31 ( 2 ), 142 – 147 ( 2013 ).
  • Sun YV , SmithAK , ConneelyKNet al. Epigenomic association analysis identifies smoking-related DNA methylation sites in African Americans . Hum. Genet.132 ( 9 ), 1027 – 1037 ( 2013 ).
  • Houseman EA , AccomandoWP , KoestlerDCet al. DNA methylation arrays as surrogate measures of cell mixture distribution . BMC Bioinformatics13 , 86 ( 2012 ).
  • Pilsner JR , HallMN , LiuXet al. Influence of prenatal arsenic exposure and newborn sex on global methylation of cord blood DNA . PLoS ONE7 ( 5 ), e37147 ( 2012 ).
  • Faulk C , BarksA , LiuK , GoodrichJM , DolinoyDC . Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice . Epigenomics5 ( 5 ), 487 – 500 ( 2013 ).
  • Liu J , MorganM , HutchisonK , CalhounVD . A study of the influence of sex on genome wide methylation . PLoS ONE5 ( 4 ), e10028 ( 2010 ).
  • Penaloza CG , EstevezB , HanDM , NorouziM , LockshinRA , ZakeriZ . Sex-dependent regulation of cytochrome P450 family members Cyp1a1, Cyp2e1, and Cyp7b1 by methylation of DNA . FASEB J.28 ( 2 ), 966 – 977 ( 2014 ).
  • Barrett JR . Children’s health. Sex-specific cognitive effects of lead . Environ. Health Perspect.117 ( 9 ), A393 ( 2009 ).
  • Tretter L , Adam-ViziV . Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress . Philos. Trans. R Soc. Lond. B Biol. Sci.360 ( 1464 ), 2335 – 2345 ( 2005 ).
  • Kohli RM , ZhangY . TET enzymes, TDG and the dynamics of DNA demethylation . Nature502 ( 7472 ), 472 – 479 ( 2013 ).
  • Padilla MA , ElobeidM , RudenDM , AllisonDB . An examination of the association of selected toxic metals with total and central obesity indices: NHANES 99–02 . Int. J. Environ. Res. Public Health7 ( 9 ), 3332 – 3347 ( 2010 ).
  • Selenscig D , RossiA , ChiccoA , LombardoYB . Increased leptin storage with altered leptin secretion from adipocytes of rats with sucrose-induced dyslipidemia and insulin resistance: effect of dietary fish oil . Metabolism59 ( 6 ), 787 – 795 ( 2010 ).
  • Shen W , WangC , XiaLet al. Epigenetic modification of the leptin promoter in diet-induced obese mice and the effects of N-3 polyunsaturated fatty acids . Sci. Rep.4 , 5282 ( 2014 ).
  • Kile ML , HousemanEA , BaccarelliAAet al. Effect of prenatal arsenic exposure on DNA methylation and leukocyte subpopulations in cord blood . Epigenetics9 ( 5 ), 774 – 782 ( 2014 ).
  • Webber BR , IacovinoM , ChoiSH , TolarJ , KybaM , BlazarBR . DNA methylation of Runx1 regulatory regions correlates with transition from primitive to definitive hematopoietic potential in vitro and in vivo . Blood122 ( 17 ), 2978 – 2986 ( 2013 ).
  • Wang CQ , MotodaL , SatakeMet al. Runx3 deficiency results in myeloproliferative disorder in aged mice . Blood122 ( 4 ), 562 – 566 ( 2013 ).
  • Wolff EM , LiangG , CortezCCet al. RUNX3 methylation reveals that bladder tumors are older in patients with a history of smoking . Cancer Res.68 ( 15 ), 6208 – 6214 ( 2008 ).
  • Tian Q , LiT , HouW , ZhengJ , SchrumLW , BonkovskyHL . Lon peptidase 1 (LONP1)-dependent breakdown of mitochondrial 5-aminolevulinic acid synthase protein by heme in human liver cells . J. Biol. Chem.286 ( 30 ), 26424 – 26430 ( 2011 ).
  • Ball MP , LiJB , GaoYet al. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells . Nat. Biotechnol.27 ( 4 ), 361 – 368 ( 2009 ).
  • Chopra P , PapaleLA , WhiteATet al. Array-based assay detects genome-wide 5-mC and 5-hmC in the brains of humans, non-human primates, and mice . BMC Genomics15 , 131 ( 2014 ).
  • Huang Y , PastorWA , ShenY , TahilianiM , LiuDR , RaoA . The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing . PLoS ONE5 ( 1 ), e8888 ( 2010 ).
  • Tahiliani M , KohKP , ShenYet al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 . Science324 ( 5929 ), 930 – 935 ( 2009 ).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.