Lead Exposure during Early Human Development and DNA Methylation of Imprinted Gene Regulatory Elements in Adulthood

Li, Yue; Xie, Changchun; Murphy, Susan K.; Skaar, David; Nye, Monica; Vidal, Adriana C.; Cecil, Kim M.; Dietrich, Kim N.; Puga, Alvaro; Jirtle, Randy L.; Hoyo, Cathrine

doi:10.1289/ehp.1408577

Title: Lead Exposure during Early Human Development and DNA Methylation of Imprinted Gene Regulatory Elements in Adulthood

Journal Article · Fri Jun 26 00:00:00 EDT 2015 · Environmental Health Perspectives

DOI:https://doi.org/10.1289/ehp.1408577· OSTI ID:1395575

Li, Yue ^[1]; Xie, Changchun ^[2]; Murphy, Susan K. ^[1]; Skaar, David ^[3]; Nye, Monica ^[4]; Vidal, Adriana C. ^[1]; Cecil, Kim M. ^[5]; Dietrich, Kim N. ^[6]; Puga, Alvaro ^[7]; Jirtle, Randy L. ^[3]; Hoyo, Cathrine ^[8]

Duke Univ., Durham, NC (United States)
Univ. of Cincinnati, OH (United States)
North Carolina State Univ., Raleigh, NC (United States)
Univ. of North Carolina, Chapel Hill, NC (United States)
Univ. of Cincinnati, Cincinnati, OH (United States), College of Medicine
Univ. of Cincinnati, OH (United States). College of Medicine
Univ. of Cincinnati, Cincinnati, OH (United States). College of Medicine
North Carolina State Univ., Raleigh, NC (United States); Duke Univ., Durham, NC (United States)

Here, lead exposure during early development causes neurodevelopmental disorders by unknown mechanisms. Epidemiologic studies have focused recently on determining associations between lead exposure and global DNA methylation; however, such approaches preclude the identification of loci that may alter human disease risk. The objective of this study was to determine whether maternal, postnatal, and early childhood lead exposure can alter the differentially methylated regions (DMRs) that control the monoallelic expression of imprinted genes involved in metabolism, growth, and development. Questionnaire data and serial blood lead levels were obtained from 105 participants (64 females, 41 males) of the Cincinnati Lead Study from birth to 78 months. When participants were adults, we used Sequenom EpiTYPER assays to test peripheral blood DNA to quantify CpG methylation in peripheral blood leukocytes at DMRs of 22 human imprinted genes. Statistical analyses were conducted using linear regression. Mean blood lead concentration from birth to 78 months was associated with a significant decrease in PEG3 DMR methylation (β = –0.0014; 95% CI: –0.0023, –0.0005, p = 0.002), stronger in males (β = –0.0024; 95% CI: –0.0038, –0.0009, p = 0.003) than in females (β = –0.0009; 95% CI: –0.0020, 0.0003, p = 0.1). Elevated mean childhood blood lead concentration was also associated with a significant decrease in IGF2/H19 (β = –0.0013; 95% CI: –0.0023, –0.0003, p = 0.01) DMR methylation, but primarily in females, (β = –0.0017; 95% CI: –0.0029, –0.0006, p = 0.005) rather than in males, (β = –0.0004; 95% CI: –0.0023, 0.0015, p = 0.7). Elevated blood lead concentration during the neonatal period was associated with higher PLAGL1/HYMAI DMR methylation regardless of sex (β = 0.0075; 95% CI: 0.0018, 0.0132, p = 0.01). The magnitude of associations between cumulative lead exposure and CpG methylation remained unaltered from 30 to 78 months. Our findings provide evidence that early childhood lead exposure results in sexdependent and gene-specific DNA methylation differences in the DMRs of PEG3, IGF2/H19, and PLAGL1/HYMAI in adulthood.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: North Carolina State University, Raleigh, NC (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FG02-10ER64931; SC0003778

OSTI ID:: 1395575

Journal Information:: Environmental Health Perspectives, Vol. 124, Issue 5; ISSN 0091-6765

Publisher:: National Institute of Environmental Health SciencesCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 39 works

Citation information provided by
Web of Science

References (77)

The early-life social environment and DNA methylation Szyf, M. Clinical Genetics, Vol. 81, Issue 4 https://doi.org/10.1111/j.1399-0004.2012.01843.x	journal	February 2012
The role of imprinted genes in humans Ishida, Miho; Moore, Gudrun E. Molecular Aspects of Medicine, Vol. 34, Issue 4 https://doi.org/10.1016/j.mam.2012.06.009	journal	July 2013
Regulation of Maternal Behavior and Offspring Growth by Paternally Expressed Peg3 Li, L. Science, Vol. 284, Issue 5412 https://doi.org/10.1126/science.284.5412.330	journal	April 1999
Loss of imprinting of insulin growth factor II gene: a potential heritable biomarker for colon neoplasia predisposition☆ Cruz-Correa, Marcia; Cui, Hengmi; Giardiello, Francis M. Gastroenterology, Vol. 126, Issue 4 https://doi.org/10.1053/j.gastro.2003.12.051	journal	April 2004
Interpreting and Managing Blood Lead Levels of Less Than 10 g/dL in Children and Reducing Childhood Exposure to Lead: Recommendations of the Centers for Disease Control and Prevention Advisory Committee on Childhood Lead Poisoning Prevention Binns, H. J.; Campbell, C.; Brown, M. J. PEDIATRICS, Vol. 120, Issue 5 https://doi.org/10.1542/peds.2005-1770	journal	November 2007
Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive Kanduri, Chandrasekhar; Pant, Vinod; Loukinov, Dmitri Current Biology, Vol. 10, Issue 14 https://doi.org/10.1016/s0960-9822(00)00597-2	journal	July 2000
The Genome- and System-Wide Response of DNA Methylation to Early Life Adversity and its Implication on Mental Health Szyf, Moshe The Canadian Journal of Psychiatry, Vol. 58, Issue 12 https://doi.org/10.1177/070674371305801208	journal	December 2013
Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy Hoyo, Cathrine; Murtha, Amy P.; Schildkraut, Joellen M. Epigenetics, Vol. 6, Issue 7 https://doi.org/10.4161/epi.6.7.16263	journal	July 2011
Large scale mapping of methylcytosines in CTCF-binding sites in the human H19 promoter and aberrant hypomethylation in human bladder cancer Takai, D. Human Molecular Genetics, Vol. 10, Issue 23 https://doi.org/10.1093/hmg/10.23.2619	journal	November 2001
CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus Hark, Amy T.; Schoenherr, Christopher J.; Katz, David J. Nature, Vol. 405, Issue 6785 https://doi.org/10.1038/35013106	journal	May 2000
Cancer epigenetics takes center stage Feinberg, Andrew P. Proceedings of the National Academy of Sciences, Vol. 98, Issue 2 https://doi.org/10.1073/pnas.98.2.392	journal	January 2001
Imprint regulatory elements as epigenetic biosensors of exposure in epidemiological studies Hoyo, C.; Murphy, S. K.; Jirtle, R. L. Journal of Epidemiology & Community Health, Vol. 63, Issue 9 https://doi.org/10.1136/jech.2009.090803	journal	August 2009
Decreased Brain Volume in Adults with Childhood Lead Exposure Cecil, Kim M.; Brubaker, Christopher J.; Adler, Caleb M. PLoS Medicine, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pmed.0050112	journal	May 2008
Maternal Genistein Alters Coat Color and Protects A ^vy Mouse Offspring from Obesity by Modifying the Fetal Epigenome Dolinoy, Dana C.; Weidman, Jennifer R.; Waterland, Robert A. Environmental Health Perspectives, Vol. 114, Issue 4 https://doi.org/10.1289/ehp.8700	journal	April 2006
Exposure to lead and the developmental origin of oxidative DNA damage in the aging brain Bolin, Celeste M.; Basha, Riyaz; Cox, David The FASEB Journal, Vol. 20, Issue 6 https://doi.org/10.1096/fj.05-5091fje	journal	April 2006
Adaptive radiation-induced epigenetic alterations mitigated by antioxidants Bernal, Autumn J.; Dolinoy, Dana C.; Huang, Dale The FASEB Journal, Vol. 27, Issue 2 https://doi.org/10.1096/fj.12-220350	journal	February 2013
Early exposure to lead and juvenile delinquency Dietrich, Kim N.; Douglas, Ris M.; Succop, Paul A. Neurotoxicology and Teratology, Vol. 23, Issue 6 https://doi.org/10.1016/s0892-0362(01)00184-2	journal	November 2001
Association of maternal and nutrient supply line factors with DNA methylation at the imprinted IGF2/H19 locus in multiple tissues of newborn twins Loke, Yuk Jing; Galati, John C.; Morley, Ruth Epigenetics, Vol. 8, Issue 10 https://doi.org/10.4161/epi.25908	journal	October 2013
Genomic Imprinting: A Mammalian Epigenetic Discovery Model Barlow, Denise P. Annual Review of Genetics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-genet-110410-132459	journal	December 2011
Lead exposure in consumers of culled invasive alien mammals in El Palmar National Park, Argentina Tammone, Agostina; Caselli, Andrea Elsa; Condorí, Walter Ezequiel Environmental Science and Pollution Research, Vol. 28, Issue 31 https://doi.org/10.1007/s11356-021-13654-7	journal	April 2021
Anodic stripping voltammetry procedure modified for improved accuracy of blood lead analysis. Roda, S. M.; Greenland, R. D.; Bornschein, R. L. Clinical Chemistry, Vol. 34, Issue 3 https://doi.org/10.1093/clinchem/34.3.563	journal	March 1988
The role of imprinted genes in humans Moore, Gudrun; Oakey, Rebecca Genome Biology, Vol. 12, Issue 3 https://doi.org/10.1186/gb-2011-12-3-106	journal	January 2011
Neurotoxic Effects and Biomarkers of Lead Exposure: A Review Sanders, T.; Liu, Y.; Buchner, V. Reviews on Environmental Health, Vol. 24, Issue 1 https://doi.org/10.1515/REVEH.2009.24.1.15	journal	January 2009
Children’s blood lead and standardized test performance response as indicators of neurotoxicity in metropolitan New Orleans elementary schools Zahran, S.; Mielke, H. W.; Weiler, S. NeuroToxicology, Vol. 30, Issue 6 https://doi.org/10.1016/j.neuro.2009.07.017	journal	November 2009
Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation Takiguchi, Masufumi; Achanzar, William E.; Qu, Wei Experimental Cell Research, Vol. 286, Issue 2 https://doi.org/10.1016/s0014-4827(03)00062-4	journal	June 2003
Epigenotype-phenotype correlations in Beckwith-Wiedemann syndrome Engel, J. R. Journal of Medical Genetics, Vol. 37, Issue 12 https://doi.org/10.1136/jmg.37.12.921	journal	December 2000
Persistent epigenetic differences associated with prenatal exposure to famine in humans Heijmans, B. T.; Tobi, E. W.; Stein, A. D. Proceedings of the National Academy of Sciences, Vol. 105, Issue 44 https://doi.org/10.1073/pnas.0806560105	journal	October 2008
Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice Faulk, Christopher; Barks, Amanda; Liu, Kevin Epigenomics, Vol. 5, Issue 5 https://doi.org/10.2217/epi.13.49	journal	October 2013
A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting DeChiara, Thomas M.; Efstratiadis, Argiris; Robertsen, Elizabeth J. Nature, Vol. 345, Issue 6270 https://doi.org/10.1038/345078a0	journal	May 1990
The Human Imprintome: Regulatory Mechanisms, Methods of Ascertainment, and Roles in Disease Susceptibility Skaar, D. A.; Li, Y.; Bernal, A. J. ILAR Journal, Vol. 53, Issue 3-4 https://doi.org/10.1093/ilar.53.3-4.341	journal	December 2012
An imprinted gene network that controls mammalian somatic growth is down-regulated during postnatal growth deceleration in multiple organs Lui, Julian C.; Finkielstain, Gabriela P.; Barnes, Kevin M. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 295, Issue 1 https://doi.org/10.1152/ajpregu.00182.2008	journal	July 2008
Temporal stability and age-related prevalence of loss of imprinting of the insulin-like growth factor-2 gene Cruz-Correa, Marcia; Zhao, Ronghua; Oveido, Myriam Epigenetics, Vol. 4, Issue 2 https://doi.org/10.4161/epi.4.2.7954	journal	February 2009
Parental Socioeconomic Status and Risk of Offspring Autism Spectrum Disorders in a Swedish Population-Based Study Rai, Dheeraj; Lewis, Glyn; Lundberg, Michael Journal of the American Academy of Child & Adolescent Psychiatry, Vol. 51, Issue 5 https://doi.org/10.1016/j.jaac.2012.02.012	journal	May 2012
Loss of IGF2 Imprinting: A Potential Marker of Colorectal Cancer Risk Cui, H. Science, Vol. 299, Issue 5613 https://doi.org/10.1126/science.1080902	journal	March 2003
Imprinting evolution and the price of silence Murphy, Susan K.; Jirtle, Randy L. BioEssays, Vol. 25, Issue 6 https://doi.org/10.1002/bies.10277	journal	May 2003
Association of cord blood methylation fractions at imprinted insulin-like growth factor 2 (IGF2), plasma IGF2, and birth weight Hoyo, Cathrine; Fortner, Kimberly; Murtha, Amy P. Cancer Causes & Control, Vol. 23, Issue 4 https://doi.org/10.1007/s10552-012-9932-y	journal	March 2012
ZAC, LIT1 (KCNQ1OT1) and p57KIP2 (CDKN1C) are in an imprinted gene network that may play a role in Beckwith-Wiedemann syndrome Arima, T. Nucleic Acids Research, Vol. 33, Issue 8 https://doi.org/10.1093/nar/gki555	journal	April 2005
Hypothalamic expression of Peg3 gene is associated with maternal care differences between SM/J and LG/J mouse strains : Maternal Care and Chiavegatto, Silvana; Sauce, Bruno; Ambar, Guilherme Brain and Behavior, Vol. 2, Issue 4 https://doi.org/10.1002/brb3.58	journal	May 2012
Associations between Methylation of Paternally Expressed Gene 3 (PEG3), Cervical Intraepithelial Neoplasia and Invasive Cervical Cancer Nye, Monica D.; Hoyo, Cathrine; Huang, Zhiqing PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0056325	journal	February 2013
Quantitative analysis of DNA methylation at all human imprinted regions reveals preservation of epigenetic stability in adult somatic tissue Woodfine, Kathryn; Huddleston, Joanna E.; Murrell, Adele Epigenetics & Chromatin, Vol. 4, Issue 1 https://doi.org/10.1186/1756-8935-4-1	journal	January 2011
Low-level lead-induced neurotoxicity in children: an update on central nervous system effects Finkelstein, Y. Brain Research Reviews, Vol. 27, Issue 2 https://doi.org/10.1016/s0165-0173(98)00011-3	journal	July 1998
Metabolic Flexibility Assists Reprograming of Central and Peripheral Innate Immunity During Neurodevelopment Cruz-Carrillo, Gabriela; Camacho-Morales, Alberto Molecular Neurobiology, Vol. 58, Issue 2 https://doi.org/10.1007/s12035-020-02154-3	journal	October 2020
Zac1 Regulates an Imprinted Gene Network Critically Involved in the Control of Embryonic Growth Varrault, Annie; Gueydan, Charlotte; Delalbre, Annie Developmental Cell, Vol. 11, Issue 5 https://doi.org/10.1016/j.devcel.2006.09.003	journal	November 2006
Genomic imprinting: parental influence on the genome Reik, Wolf; Walter, Jörn Nature Reviews Genetics, Vol. 2, Issue 1 https://doi.org/10.1038/35047554	journal	January 2001
The evolution of imprinting: chromosomal mapping of orthologues of mammalian imprinted domains in monotreme and marsupial mammals Edwards, Carol A.; Rens, Willem; Clarke, Oliver BMC Evolutionary Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2148-7-157	journal	January 2007
Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions Zhao, Zhihu; Tavoosidana, Gholamreza; Sjölinder, Mikael Nature Genetics, Vol. 38, Issue 11 https://doi.org/10.1038/ng1891	journal	October 2006
Imprinting Weaves Its Web Smits, Guillaume; Kelsey, Gavin Developmental Cell, Vol. 11, Issue 5 https://doi.org/10.1016/j.devcel.2006.10.013	journal	November 2006
Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke Murphy, Susan K.; Adigun, Abayomi; Huang, Zhiqing Gene, Vol. 494, Issue 1 https://doi.org/10.1016/j.gene.2011.11.062	journal	February 2012
Impaired glucose homeostasis in transgenic mice expressing the human transient neonatal diabetes mellitus locus, TNDM Ma, Dan; Shield, Julian P. H.; Dean, Wendy Journal of Clinical Investigation, Vol. 114, Issue 3 https://doi.org/10.1172/jci200419876	journal	August 2004
Biomarkers of Lead Exposure and DNA Methylation within Retrotransposons Wright, Robert O.; Schwartz, Joel; Wright, Rosalind J. Environmental Health Perspectives, Vol. 118, Issue 6 https://doi.org/10.1289/ehp.0901429	journal	June 2010
Deregulation of an imprinted gene network in prostate cancer Ribarska, Teodora; Goering, Wolfgang; Droop, Johanna Epigenetics, Vol. 9, Issue 5 https://doi.org/10.4161/epi.28006	journal	February 2014
Loss of imprinting of the insulin-like growth factor II gene occurs by biallelic methylation in a core region of H19-associated CTCF-binding sites in colorectal cancer Nakagawa, H.; Chadwick, R. B.; Peltomaki, P. Proceedings of the National Academy of Sciences, Vol. 98, Issue 2 https://doi.org/10.1073/pnas.98.2.591	journal	January 2001
Longitudinal Analyses of Prenatal and Postnatal Lead Exposure and Early Cognitive Development Bellinger, David; Leviton, Alan; Waternaux, Christine New England Journal of Medicine, Vol. 316, Issue 17 https://doi.org/10.1056/nejm198704233161701	journal	April 1987
Differentially Methylated Regions of Imprinted Genes in Prenatal, Perinatal and Postnatal Human Tissues Murphy, Susan K.; Huang, Zhiqing; Hoyo, Cathrine PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0040924	journal	July 2012
Impaired glucose homeostasis in transgenic mice expressing the human transient neonatal diabetes mellitus locus, TNDM Ma, Dan; Shield, Julian P. H.; Dean, Wendy Journal of Clinical Investigation, Vol. 114, Issue 3 https://doi.org/10.1172/JCI19876	journal	August 2004
Influence of Prenatal Lead Exposure on Genomic Methylation of Cord Blood DNA Pilsner, Rick; Hu, Howard; Ettinger, Adrienne Epidemiology, Vol. 20 https://doi.org/10.1097/01.ede.0000362961.55503.96	journal	January 2009
Deprivation, ethnicity and the prevalence of intellectual and developmental disabilities Emerson, Eric Journal of Epidemiology and Community Health, Vol. 66, Issue 3 https://doi.org/10.1136/jech.2010.111773	journal	October 2010
Imprinted tumor suppressor genesARHI andPEG3 are the most frequently down-regulated in human ovarian cancers by loss of heterozygosity and promoter methylation Feng, Weiwei; Marquez, Rebecca T.; Lu, Zhen Cancer, Vol. 112, Issue 7 https://doi.org/10.1002/cncr.23323	journal	January 2008
Neuropsychological studies in children with elevated tooth-lead concentrations: II. Extended Study Winneke, G.; Kr�mer, U.; Brockhaus, A. International Archives of Occupational and Environmental Health, Vol. 51, Issue 3 https://doi.org/10.1007/bf00377755	journal	March 1983
Peg3/Pw1 Is a Mediator between p53 and Bax in DNA Damage-induced Neuronal Death Johnson, Mark D.; Wu, Xiangwei; Aithmitti, Nadia Journal of Biological Chemistry, Vol. 277, Issue 25 https://doi.org/10.1074/jbc.m201907200	journal	April 2002
Degree of methylation of ZAC1 ( PLAGL1 ) is associated with prenatal and post-natal growth in healthy infants of the EDEN mother child cohort Azzi, Salah; Sas, Theo CJ; Koudou, Yves Epigenetics, Vol. 9, Issue 3 https://doi.org/10.4161/epi.27387	journal	December 2013
DNA hypomethylation and human diseases Wilson, Ann S.; Power, Barbara E.; Molloy, Peter L. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, Vol. 1775, Issue 1 https://doi.org/10.1016/j.bbcan.2006.08.007	journal	January 2007
Epigenetic histone modification regulates developmental lead exposure induced hyperactivity in rats Luo, Man; Xu, Yi; Cai, Rong Toxicology Letters, Vol. 225, Issue 1 https://doi.org/10.1016/j.toxlet.2013.11.025	journal	February 2014
Phenotypic plasticity and the epigenetics of human disease Feinberg, Andrew P. Nature, Vol. 447, Issue 7143 https://doi.org/10.1038/nature05919	journal	May 2007
Maternal and child undernutrition: consequences for adult health and human capital Victora, Cesar G.; Adair, Linda; Fall, Caroline The Lancet, Vol. 371, Issue 9609 https://doi.org/10.1016/S0140-6736(07)61692-4	journal	January 2008
Season of Conception in Rural Gambia Affects DNA Methylation at Putative Human Metastable Epialleles Waterland, Robert A.; Kellermayer, Richard; Laritsky, Eleonora PLoS Genetics, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pgen.1001252	journal	December 2010
Influence of Prenatal Lead Exposure on Genomic Methylation of Cord Blood DNA Pilsner, J. Richard; Hu, Howard; Ettinger, Adrienne Environmental Health Perspectives, Vol. 117, Issue 9 https://doi.org/10.1289/ehp.0800497	journal	September 2009
An Extensive Genetic Program Occurring during Postnatal Growth in Multiple Tissues Finkielstain, Gabriela P.; Forcinito, Patricia; Lui, Julian C. K. Endocrinology, Vol. 150, Issue 4 https://doi.org/10.1210/en.2008-0868	journal	April 2009
Association of Prenatal and Childhood Blood Lead Concentrations with Criminal Arrests in Early Adulthood Wright, John Paul; Dietrich, Kim N.; Ris, M. Douglas PLoS Medicine, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pmed.0050101	journal	May 2008
Transposable Elements: Targets for Early Nutritional Effects on Epigenetic Gene Regulation Waterland, R. A.; Jirtle, R. L. Molecular and Cellular Biology, Vol. 23, Issue 15 https://doi.org/10.1128/mcb.23.15.5293-5300.2003	journal	August 2003
Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development Dolinoy, D. C.; Huang, D.; Jirtle, R. L. Proceedings of the National Academy of Sciences, Vol. 104, Issue 32 https://doi.org/10.1073/pnas.0703739104	journal	August 2007
How imprinting centres work Lewis, A.; Reik, W. Cytogenetic and Genome Research, Vol. 113, Issue 1-4 https://doi.org/10.1159/000090818	journal	January 2006
Associations between Methylation of Paternally Expressed Gene 3 (PEG3), Cervical Intraepithelial Neoplasia and Invasive Cervical Cancer Britta, Swai,; Brandi, Vasquez,; Pendo, Mlay, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/vg71-fn43	text	January 2013
Transactivation of Igf2 in a mouse model of Beckwith–Wiedemann syndrome Sun, Fang-Lin; Dean, Wendy L.; Kelsey, Gavin Nature, Vol. 389, Issue 6653 https://doi.org/10.1038/39797	journal	October 1997
Long term low-dose arsenic exposure induces loss of DNA methylation Reichard, John F.; Schnekenburger, Michael; Puga, Alvaro Biochemical and Biophysical Research Communications, Vol. 352, Issue 1 https://doi.org/10.1016/j.bbrc.2006.11.001	journal	January 2007
A critical role for IGF-II in memory consolidation and enhancement Chen, Dillon Y.; Stern, Sarah A.; Garcia-Osta, Ana Nature, Vol. 469, Issue 7331 https://doi.org/10.1038/nature09667	journal	January 2011
Low-Level Fetal Lead Exposure Effect on Neurobehavioral Development in Early Infancy Dietrich, Kim N.; Krafft, Kathleen M.; Bornschein, Robert L. Pediatrics, Vol. 80, Issue 5 https://doi.org/10.1542/peds.80.5.721	journal	November 1987

Cited By (22)

Lead exposure and child maltreatment as models for how to conceptualize early-in-life risk factors for violence Jaffee, Sara R. Infant Mental Health Journal, Vol. 40, Issue 1 https://doi.org/10.1002/imhj.21756	journal	January 2019
Sex-Dependent Effects of Developmental Lead Exposure on the Brain Singh, Garima; Singh, Vikrant; Sobolewski, Marissa Frontiers in Genetics, Vol. 9 https://doi.org/10.3389/fgene.2018.00089	journal	March 2018
The Genetic Basis for Variation in Sensitivity to Lead Toxicity in Drosophila melanogaster Zhou, Shanshan; Morozova, Tatiana V.; Hussain, Yasmeen N. Environmental Health Perspectives, Vol. 124, Issue 7 https://doi.org/10.1289/ehp.1510513	journal	July 2016
Low-level Gestational Lead Exposure Alters Dendritic Spine Plasticity in the Hippocampus and Reduces Learning and Memory in Rats Zhao, Zai-Hua; Zheng, Gang; Wang, Tao Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-21521-8	journal	February 2018
Genetics of the human placenta: implications for toxicokinetics Gundacker, Claudia; Neesen, Jürgen; Straka, Elisabeth Archives of Toxicology, Vol. 90, Issue 11 https://doi.org/10.1007/s00204-016-1816-6	journal	September 2016
Sleep duration and fragmentation in relation to leukocyte DNA methylation in adolescents Jansen, Erica C.; Dolinoy, Dana C.; O’Brien, Louise M. Sleep, Vol. 42, Issue 9 https://doi.org/10.1093/sleep/zsz121	journal	June 2019
Adolescent epigenetic profiles and environmental exposures from early life through peri-adolescence Goodrich, Jaclyn M.; Dolinoy, Dana C.; Sánchez, Brisa N. Environmental Epigenetics, Vol. 2, Issue 3 https://doi.org/10.1093/eep/dvw018	journal	August 2016
DNA methylation of imprinted genes in Mexican–American newborn children with prenatal phthalate exposure Tindula, Gwen; Murphy, Susan K.; Grenier, Carole Epigenomics, Vol. 10, Issue 7 https://doi.org/10.2217/epi-2017-0178	journal	July 2018
An epigenome‐wide DNA methylation study of workers with an occupational exposure to lead Zhang, Xing‐xu; He, Zhen; Feng, Bin Journal of Applied Toxicology, Vol. 39, Issue 9 https://doi.org/10.1002/jat.3816	journal	May 2019
Cadmium exposure and MEG3 methylation differences between Whites and African Americans in the NEST Cohort House, John S.; Hall, Jonathan; Park, Sarah S. Environmental Epigenetics, Vol. 5, Issue 3 https://doi.org/10.1093/eep/dvz014	journal	July 2019
Ecogenetics of lead toxicity and its influence on risk assessment Mani, Ms; Kabekkodu, Sp; Joshi, Mb Human & Experimental Toxicology, Vol. 38, Issue 9 https://doi.org/10.1177/0960327119851253	journal	May 2019
Epigenetics, obesity and early-life cadmium or lead exposure Park, Sarah S.; Skaar, David A.; Jirtle, Randy L. Epigenomics, Vol. 9, Issue 1 https://doi.org/10.2217/epi-2016-0047	journal	January 2017
Large epigenome-wide association study of childhood ADHD identifies peripheral DNA methylation associated with disease and polygenic risk burden Mooney, Michael A.; Ryabinin, Peter; Wilmot, Beth Translational Psychiatry, Vol. 10, Issue 1 https://doi.org/10.1038/s41398-020-0710-4	journal	January 2020
DNA methylation of imprinted gene control regions in the regression of low-grade cervical lesions: Regression of low-grade cervical lesions Gomih, Ayodele; Smith, Jennifer S.; North, Kari E. International Journal of Cancer, Vol. 143, Issue 3 https://doi.org/10.1002/ijc.31350	journal	March 2018
Sexually Dimorphic Effects of Early-Life Exposures to Endocrine Disruptors: Sex-Specific Epigenetic Reprogramming as a Potential Mechanism McCabe, Carolyn; Anderson, Olivia S.; Montrose, Luke Current Environmental Health Reports, Vol. 4, Issue 4 https://doi.org/10.1007/s40572-017-0170-z	journal	October 2017
Association of blood leukocyte DNA methylation at LINE-1 and growth-related candidate genes with pubertal onset and progression Wu, Yue; Peterson, Karen E.; Sánchez, Brisa N. Epigenetics, Vol. 13, Issue 12 https://doi.org/10.1080/15592294.2018.1556198	journal	December 2018
Perinatal Bisphenol A Exposure and Reprogramming of Imprinted Gene Expression in the Adult Mouse Brain Malloy, Maureen A.; Kochmanski, Joseph J.; Jones, Tamara R. Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00951	journal	October 2019
Different People, Different Outcomes: Assessing Genetic Susceptibility to Lead Exposures Barrett, Julia R. Environmental Health Perspectives, Vol. 124, Issue 7 https://doi.org/10.1289/ehp.124-a131	journal	July 2016
Association of Blood Leukocyte DNA Methylation at LINE-1 and Growth-Related Candidate Genes with Pubertal Onset and Progression Wu, Yue; Peterson, Karen E.; Sánchez, Brisa N. Taylor & Francis https://doi.org/10.6084/m9.figshare.7441991.v1	text	January 2018
Association of blood leukocyte DNA methylation at LINE-1 and growth-related candidate genes with pubertal onset and progression Wu, Yue; Peterson, Karen E.; Sánchez, Brisa N. Taylor & Francis https://doi.org/10.6084/m9.figshare.7441991.v2	text	January 2018
Effects of Cadmium Exposure on DNA Methylation at Imprinting Control Regions and Genome-Wide in Mothers and Newborn Children Cowley, Michael; Skaar, David A.; Jima, Dereje D. Environmental Health Perspectives, Vol. 126, Issue 3 https://doi.org/10.1289/ehp2085	journal	March 2018
Association of blood leukocyte DNA methylation at LINE-1 and growth-related candidate genes with pubertal onset and progression Wu, Yue; Peterson, Karen E.; Sánchez, Brisa N. Taylor & Francis https://doi.org/10.6084/m9.figshare.7441991	text	January 2018

Similar Records

Allele-specific deposition of macroH2A1 in Imprinting Control Regions

Journal Article · Fri Jan 13 00:00:00 EST 2006 · Human Molecular Genetics, vol. 15, no. 5, March 1, 2006, pp. 717-724 · OSTI ID:1395575

Choo, J H; Kim, J D; Chung, J H; +2 more

Maternal blood metal levels and fetal markers of metabolic function

Journal Article · Thu Jan 15 00:00:00 EST 2015 · Environmental Research · OSTI ID:1395575

Ashley-Martin, Jillian; Dodds, Linda; Arbuckle, Tye E.; +8 more

Prenatal and postnatal polybrominated diphenyl ether exposure and visual spatial abilities in children

Journal Article · Wed Feb 15 00:00:00 EST 2017 · Environmental Research · OSTI ID:1395575

Vuong, Ann M.; Braun, Joseph M.; Yolton, Kimberly; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES

Title: Lead Exposure during Early Human Development and DNA Methylation of Imprinted Gene Regulatory Elements in Adulthood

Citation Formats

References (77)

Cited By (22)

Similar Records

Related Subjects