Advanced search
Publication Cover
Epigenetics Volume 16, 2021 - Issue 10
Submit an article Journal homepage
1,278
Views
7
CrossRef citations to date
0
Altmetric
Research Paper

Tissue and sex-specific programming of DNA methylation by perinatal lead exposure: implications for environmental epigenetics studies

Laurie K. Svobodaa Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0002-0003-4513View further author information
ORCID Icon,
Kari Neiera Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USAView further author information
,
Kai Wangb Department of Computational Medicine and Bioinformatics, University of Michigan Medical School Palmer Commons, Ann Arbor, MI, USAView further author information
,
Raymond G. Cavalcantec Epigenomics Core, University of Michigan, Medical School, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0002-6986-4283View further author information
ORCID Icon,
Christine A. Rygiela Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0001-7690-8945View further author information
ORCID Icon,
Zing Tsaia Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA;b Department of Computational Medicine and Bioinformatics, University of Michigan Medical School Palmer Commons, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0002-4006-1559View further author information
ORCID Icon,
Tamara R. Jonesa Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USAView further author information
,
Siyu Liub Department of Computational Medicine and Bioinformatics, University of Michigan Medical School Palmer Commons, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0002-5681-7824View further author information
ORCID Icon,
Jaclyn M. Goodricha Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0002-8289-9253View further author information
ORCID Icon,
Claudia Lalancettec Epigenomics Core, University of Michigan, Medical School, Ann Arbor, MI, USAView further author information
,
Justin A. Colacinoa Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA;d Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0002-5882-4569View further author information
ORCID Icon,
Maureen A. Sartorb Department of Computational Medicine and Bioinformatics, University of Michigan Medical School Palmer Commons, Ann Arbor, MI, USA;e Department of Biostatistics, University of Michigan, School of Public Health, Ann Arbor, MI, USAORCID Iconhttps://orcid.org/0000-0001-6155-5702View further author information
ORCID Icon &
Dana C. Dolinoya Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA;d Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USACorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-3304-2456View further author information
ORCID Icon show all
Pages 1102-1122 | Received 17 May 2020, Accepted 07 Oct 2020, Published online: 08 Nov 2020

References

  • Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13(7):484–492.
  • Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293(5532):1089–1093.
  • Lopez V, Fernandez AF, Fraga MF. The role of 5-hydroxymethylcytosine in development, aging and age-related diseases. Ageing Res Rev. 2017;37:28–38.
  • Kochmanski JJ, Marchlewicz EH, Cavalcante RG, et al. Longitudinal effects of developmental bisphenol a exposure on epigenome-wide DNA hydroxymethylation at imprinted loci in mouse blood. Environ Health Perspect. 2018;126(7):077006.
  • Ringh MV, Hagemann-Jensen M, Needhamsen M, et al. Tobacco smoking induces changes in true DNA methylation, hydroxymethylation and gene expression in bronchoalveolar lavage cells. EBioMedicine. 2019;46:290–304.
  • Huang Y, Lin S, Jin L, et al. Decreased global DNA hydroxymethylation in neural tube defects: association with polycyclic aromatic hydrocarbons. Epigenetics. 2019;1–11.
  • Zhai H, Chen C, Wang N, et al. Blood lead level is associated with non-alcoholic fatty liver disease in the Yangtze river delta region of China in the context of rapid urbanization. Environ Health. 2017;16(1):93. .
  • Cave M, Appana S, Patel M, et al. Polychlorinated biphenyls, lead, and mercury are associated with liver disease in American adults: NHANES 2003-2004. Environ Health Perspect. 2010;118(12):1735–1742.
  • Bener A, Obineche E, Gillett M, et al. Association between blood levels of lead, blood pressure and risk of diabetes and heart disease in workers. Int Arch Occup Environ Health. 2001;74(5):375–378.
  • Park YJ, Jung Y, Oh CU. Relations between the blood lead level and metabolic syndrome risk factors. Public Health Nurs. 2019;36(2):118–125.
  • Nye MD, King KE, Darrah TH, et 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. 2016;2(1):1. .
  • Faulk C, Barks A, Liu K, et al. Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice. Epigenomics. 2013;5(5):487–500.
  • Faulk C, Barks A, Sanchez BN, et al. Perinatal lead (Pb) exposure results in sex-specific effects on food intake, fat, weight, and insulin response across the murine life-course. PLoS One. 2014;9(8):e104273. .
  • Wu J, Wen XW, Faulk C, et al. Perinatal lead exposure alters gut microbiota composition and results in sex-specific bodyweight increases in adult mice. Toxicol Sci. 2016;151(2):324–333. .
  • Leasure JL, Giddabasappa A, Chaney S, et al. Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice. Environ Health Perspect. 2008;116(3):355–361. .
  • Sun H, Wang N, Nie X, et al. Lead Exposure Induces Weight Gain in Adult Rats, accompanied by DNA hypermethylation. PLoS One. 2017;12(1):e0169958. .
  • Xia J, Lu L, Jin C, et al. Effects of short term lead exposure on gut microbiota and hepatic metabolism in adult zebrafish. Comp Biochem Physiol C Toxicol Pharmacol. 2018;209:1–8.
  • Xia J, Jin C, Pan Z, et al. Chronic exposure to low concentrations of lead induces metabolic disorder and dysbiosis of the gut microbiota in mice. Sci Total Environ. 2018;631-632:439–448.
  • Wang T, Pehrsson EC, Purushotham D, et al. The NIEHS TaRGET II Consortium and environmental epigenomics. Nat Biotechnol. 2018;36(3):225–227. .
  • Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol. 2003;23(15):5293–5300.
  • Weinhouse C, Anderson OS, Bergin IL, et al. Dose-dependent incidence of hepatic tumors in adult mice following perinatal exposure to bisphenol A. Environ Health Perspect. 2014;122(5):485–491. .
  • Akalin A, Kormaksson M, Li S, et al. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 2012;13(10):R87. .
  • Garrett-Bakelman FE, Sheridan CK, Kacmarczyk TJ, et al. Enhanced reduced representation bisulfite sequencing for assessment of DNA methylation at base pair resolution. J Vis Exp. 2015;96:e52246.
  • Koster J, Rahmann S. Snakemake–a scalable bioinformatics workflow engine. Bioinformatics. 2012;28(19):2520–2522.
  • Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–1572.
  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359.
  • Park Y, Figueroa ME, Rozek LS, et al. MethylSig: a whole genome DNA methylation analysis pipeline. Bioinformatics. 2014;30(17):2414–2422.
  • Park Y, Wu H. Differential methylation analysis for BS-seq data under general experimental design. Bioinformatics. 2016;32(10):1446–1453.
  • Cavalcante RG, Sartor MA. annotatr: genomic regions in context. Bioinformatics. 2017;33(15):2381–2383.
  • Sugathan A, Waxman DJ. Genome-wide analysis of chromatin states reveals distinct mechanisms of sex-dependent gene regulation in male and female mouse liver. Mol Cell Biol. 2013;33(18):3594–3610.
  • Lee CT, Cavalcante RG, Lee C, et al. Poly-Enrich: count-based methods for gene set enrichment testing with genomic regions. NAR Genom Bioinform. 2020;2(1):lqaa006.
  • Risso D, Ngai J, Speed TP, et al. Normalization of RNA-seq data using factor analysis of control genes or samples. Nat Biotechnol. 2014;32(9):896–902.
  • Chen A, Chen D, Chen Y. Advances of DNase-seq for mapping active gene regulatory elements across the genome in animals. Gene. 2018;667:83–94.
  • Faulk C, Liu K, Barks A, et al. Longitudinal epigenetic drift in mice perinatally exposed to lead. Epigenetics. 2014;9(7):934–941.
  • Williamson CMBA, Thomas S, Beechey CV, et al. World wide web site - mouse imprinting data and references. 2013. http://www.har.mrc.ac.uk/research/genomic_imprinting/
  • Banerjee S, Melnyk SB, Krager KJ, et al. Trifluoperazine inhibits acetaminophen-induced hepatotoxicity and hepatic reactive nitrogen formation in mice and in freshly isolated hepatocytes. Toxicol Rep. 2017;4:134–142.
  • Li Y, Duan F, Zhou X, et al. Differential responses of GC1 spermatogonia cells to high and low doses of bisphenol A. Mol Med Rep. 2018;18(3):3034–3040.
  • Reed ML, Leff SE. Maternal imprinting of human SNRPN, a gene deleted in Prader-Willi syndrome. Nat Genet. 1994;6(2):163–167.
  • Nilsson E, Matte A, Perfilyev A, et al. Epigenetic alterations in human liver from subjects with type 2 diabetes in parallel with reduced folate levels. J Clin Endocrinol Metab. 2015;100(11):E1491–1501. .
  • Seale P. Transcriptional regulatory circuits controlling brown fat development and activation. Diabetes. 2015;64(7):2369–2375.
  • Abbas S, Raza ST, Ahmed F, et al. Association of genetic polymorphism of PPARgamma-2, ACE, MTHFR, FABP-2 and FTO genes in risk prediction of type 2 diabetes mellitus. J Biomed Sci. 2013;20(1):80.
  • Speakman JR. The ‘fat mass and obesity related’ (FTO) gene: mechanisms of impact on obesity and energy balance. Curr Obes Rep. 2015;4(1):73–91.
  • Hua HW, Jiang F, Huang Q, et al. MicroRNA-153 promotes Wnt/beta-catenin activation in hepatocellular carcinoma through suppression of WWOX. Oncotarget. 2015;6(6):3840–3847.
  • Conforto TL, Waxman DJ. Sex-specific mouse liver gene expression: genome-wide analysis of developmental changes from pre-pubertal period to young adulthood. Biol Sex Differ. 2012;3(1):9.
  • Lau-Corona D, Bae WK, Hennighausen L, et al. Sex-biased genetic programs in liver metabolism and liver fibrosis are controlled by EZH1 and EZH2. PLoS Genet. 2020;16(5):e1008796.
  • Niessen LW, Mohan D, Akuoku JK, et al. Tackling socioeconomic inequalities and non-communicable diseases in low-income and middle-income countries under the Sustainable Development agenda. Lancet. 2018;391(10134):2036–2046. .
  • Sen A, Heredia N, Senut MC, et al. Early life lead exposure causes gender-specific changes in the DNA methylation profile of DNA extracted from dried blood spots. Epigenomics. 2015;7(3):379–393. .
  • Mizuno K, Ueno Y. Autonomic Nervous System and the Liver. Hepatol Res. 2017;47(2):160–165.
  • Field RB, Kruse DH, Redman RS. Immunohistochemical localization and mRNA detection of Rab3D and/or Rab3B in rat von Ebner’s glands, parotid gland, pancreas, and liver. Histochem J. 2001;33(2):71–77.
  • Delbro DS, Hallsberg L, Wallin M, et al. Expression of the non-neuronal cholinergic system in rat liver. APMIS. 2011;119(3):227–228.
  • Loo JM, Scherl A, Nguyen A, et al. Extracellular metabolic energetics can promote cancer progression. Cell. 2015;160(3):393–406. .
  • Zhan H, Jiang J, Sun Q, et al. Whole-exome sequencing-based mutational profiling of hepatitis B virus-related early-stage hepatocellular carcinoma. Gastroenterol Res Pract. 2017;2017:2029315.
  • Ammerpohl O, Pratschke J, Schafmayer C, et al. Distinct DNA methylation patterns in cirrhotic liver and hepatocellular carcinoma. Int J Cancer. 2012;130(6):1319–1328. .
  • Song J, Xie C, Jiang L, et al. Transcription factor AP-4 promotes tumorigenic capability and activates the Wnt/beta-catenin pathway in hepatocellular carcinoma. Theranostics. 2018;8(13):3571–3583. .
  • Barlow DP, Bartolomei MS. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol. 2014;6(2):2.
  • Okae H, Chiba H, Hiura H, et al. Genome-wide analysis of DNA methylation dynamics during early human development. PLoS Genet. 2014;10(12):e1004868. .
  • Bansal A, Rashid C, Xin F, et al. Sex- and Dose-Specific Effects of Maternal Bisphenol A Exposure on Pancreatic Islets of First- and Second-Generation Adult Mice Offspring. Environ Health Perspect. 2017;125(9):097022. .
  • Susiarjo M, Sasson I, Mesaros C, et al. Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet. 2013;9(4):e1003401.
  • Skaar DA, Li Y, Bernal AJ, et al. The human imprintome: regulatory mechanisms, methods of ascertainment, and roles in disease susceptibility. Ilar J. 2012;53(3–4):341–358.
  • Hanna P, Grybek V, Perez de Nanclares G, et al. Genetic and epigenetic defects at the GNAS locus lead to distinct patterns of skeletal growth but similar early-onset obesity. J Bone Miner Res. 2018;33(8):1480–1488.
  • Soubry A, Hoyo C, Butt CM, et al. Human exposure to flame-retardants is associated with aberrant DNA methylation at imprinted genes in sperm. Environ Epigenet. 2017;3(1):dvx003. .
  • Faulk C, Kim JH, Jones TR, et al. Bisphenol A-associated alterations in genome-wide DNA methylation and gene expression patterns reveal sequence-dependent and non-monotonic effects in human fetal liver. Environ Epigenet. 2015;1(1):1. .
  • Nadal A, Quesada I, Tuduri E, et al. Endocrine-disrupting chemicals and the regulation of energy balance. Nat Rev Endocrinol. 2017;13(9):536–546.
  • Ducker GS, Rabinowitz JD. One-carbon metabolism in health and disease. Cell Metab. 2017;25(1):27–42.
  • Sanchez OF, Lee J, Yu King Hing N, et al. Lead (Pb) exposure reduces global DNA methylation level by non-competitive inhibition and alteration of dnmt expression. Metallomics. 2017;9(2):149–160.
  • Paredes SR, Fukuda H, Kozicki PA, et al. S-adenosyl-L-methionine and lead intoxication: its therapeutic effect varying the route of administration. Ecotoxicol Environ Saf. 1986;12(3):252–260.
  • Cao XJ, Huang SH, Wang M, et al. S-adenosyl-L-methionine improves impaired hippocampal long-term potentiation and water maze performance induced by developmental lead exposure in rats. Eur J Pharmacol. 2008;595(1–3):30–34.
  • Sen A, Cingolani P, Senut MC, et al. Lead exposure induces changes in 5-hydroxymethylcytosine clusters in CpG islands in human embryonic stem cells and umbilical cord blood. Epigenetics. 2015;10(7):607–621. .
  • Wong CC, Qian Y, Yu J. Interplay between epigenetics and metabolism in oncogenesis: mechanisms and therapeutic approaches. Oncogene. 2017;36(24):3359–3374.
  • Basha DC, Basha SS, Reddy GR. Lead-induced cardiac and hematological alterations in aging Wistar male rats: alleviating effects of nutrient metal mixture. Biogerontology. 2012;13(4):359–368.
  • Seddik L, Bah TM, Aoues A, et al. Elucidation of mechanisms underlying the protective effects of olive leaf extract against lead-induced neurotoxicity in Wistar rats. J Toxicol Sci. 2011;36(6):797–809.
  • Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci U S A. 2007;104(32):13056–13061.
  • Kundakovic M, Gudsnuk K, Franks B, et al. Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci U S A. 2013;110(24):9956–9961. .
  • Zeng Y, Chen T. DNA methylation reprogramming during mammalian development. Genes (Basel). 2019;10:4.
  • Abu-Remaileh M, Abu-Remaileh M, Akkawi R, et al. WWOX somatic ablation in skeletal muscles alters glucose metabolism. Mol Metab. 2019;22:132–140.
  • Hui T, Cao Q, Wegrzyn-Woltosz J, et al. High-resolution single-cell DNA methylation measurements reveal epigenetically distinct hematopoietic stem cell subpopulations. Stem Cell Reports. 2018;11(2):578–592. .
  • Jaffe AE, Irizarry RA. Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol. 2014;15(2):R31.
  • Su D, Wang X, Campbell MR, et al. Distinct epigenetic effects of tobacco smoking in whole blood and among leukocyte subtypes. PLoS One. 2016;11(12):e0166486. .
  • Babio N, Ibarrola-Jurado N, Bullo M, et al. White blood cell counts as risk markers of developing metabolic syndrome and its components in the PREDIMED study. PLoS One. 2013;8(3):e58354. .
  • Kelsey G, Stegle O, Reik W. Single-cell epigenomics: recording the past and predicting the future. Science. 2017;358(6359):69–75.
  • Wang Q, Trevino LS, Wong RL, et al. Reprogramming of the epigenome by MLL1 links early-life environmental exposures to prostate cancer risk. Mol Endocrinol. 2016;30(8):856–871. .
  • Trevino LS, Dong J, Kaushal A, et al. Epigenome environment interactions accelerate epigenomic aging and unlock metabolically restricted epigenetic reprogramming in adulthood. Nat Commun. 2020;11(1):2316. .
  • Barry PS. A comparison of concentrations of lead in human tissues. Br J Ind Med. 1975;32(2):119–139.
  • Schroeder HA, Tipton IH. The human body burden of lead. Arch Environ Health. 1968;17(6):965–978.
  • Popovic M, McNeill FE, Chettle DR, et al. Impact of occupational exposure on lead levels in women. Environ Health Perspect. 2005;113(4):478–484.
  • Berkowitz GS, Wolff MS, Lapinski RH, et al. Prospective study of blood and tibia lead in women undergoing surgical menopause. Environ Health Perspect. 2004;112(17):1673–1678.

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:

Order Reprints Request Corporate Permissions

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:

Request Academic Permissions

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.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.