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

Abstract

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 leadmore » 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.« less

Authors:
 [1];  [2];  [1];  [3];  [4];  [1];  [5];  [6];  [7];  [3];  [8]
  1. Duke Univ., Durham, NC (United States)
  2. Univ. of Cincinnati, OH (United States)
  3. North Carolina State Univ., Raleigh, NC (United States)
  4. Univ. of North Carolina, Chapel Hill, NC (United States)
  5. Univ. of Cincinnati, Cincinnati, OH (United States), College of Medicine
  6. Univ. of Cincinnati, OH (United States). College of Medicine
  7. Univ. of Cincinnati, Cincinnati, OH (United States). College of Medicine
  8. North Carolina State Univ., Raleigh, NC (United States); Duke Univ., Durham, NC (United States)
Publication Date:
Research Org.:
North Carolina State University, Raleigh, NC (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1395575
Grant/Contract Number:  
FG02-10ER64931; SC0003778
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Health Perspectives
Additional Journal Information:
Journal Volume: 124; Journal Issue: 5; Journal ID: ISSN 0091-6765
Publisher:
National Institute of Environmental Health Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

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., and Hoyo, Cathrine. Lead Exposure during Early Human Development and DNA Methylation of Imprinted Gene Regulatory Elements in Adulthood. United States: N. p., 2015. Web. doi:10.1289/ehp.1408577.
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. Lead Exposure during Early Human Development and DNA Methylation of Imprinted Gene Regulatory Elements in Adulthood. United States. https://doi.org/10.1289/ehp.1408577
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., and Hoyo, Cathrine. Fri . "Lead Exposure during Early Human Development and DNA Methylation of Imprinted Gene Regulatory Elements in Adulthood". United States. https://doi.org/10.1289/ehp.1408577. https://www.osti.gov/servlets/purl/1395575.
@article{osti_1395575,
title = {Lead Exposure during Early Human Development and DNA Methylation of Imprinted Gene Regulatory Elements in Adulthood},
author = {Li, Yue and Xie, Changchun and Murphy, Susan K. and Skaar, David and Nye, Monica and Vidal, Adriana C. and Cecil, Kim M. and Dietrich, Kim N. and Puga, Alvaro and Jirtle, Randy L. and Hoyo, Cathrine},
abstractNote = {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.},
doi = {10.1289/ehp.1408577},
journal = {Environmental Health Perspectives},
number = 5,
volume = 124,
place = {United States},
year = {Fri Jun 26 00:00:00 EDT 2015},
month = {Fri Jun 26 00:00:00 EDT 2015}
}

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Works referenced in this record:

The early-life social environment and DNA methylation
journal, February 2012


The role of imprinted genes in humans
journal, July 2013


Loss of imprinting of insulin growth factor II gene: a potential heritable biomarker for colon neoplasia predisposition☆
journal, April 2004


Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive
journal, July 2000


The Genome- and System-Wide Response of DNA Methylation to Early Life Adversity and its Implication on Mental Health
journal, December 2013


Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy
journal, July 2011

  • Hoyo, Cathrine; Murtha, Amy P.; Schildkraut, Joellen M.
  • Epigenetics, Vol. 6, Issue 7
  • DOI: 10.4161/epi.6.7.16263

CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus
journal, May 2000

  • Hark, Amy T.; Schoenherr, Christopher J.; Katz, David J.
  • Nature, Vol. 405, Issue 6785
  • DOI: 10.1038/35013106

Cancer epigenetics takes center stage
journal, January 2001

  • Feinberg, Andrew P.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 2
  • DOI: 10.1073/pnas.98.2.392

Imprint regulatory elements as epigenetic biosensors of exposure in epidemiological studies
journal, August 2009

  • Hoyo, C.; Murphy, S. K.; Jirtle, R. L.
  • Journal of Epidemiology & Community Health, Vol. 63, Issue 9
  • DOI: 10.1136/jech.2009.090803

Decreased Brain Volume in Adults with Childhood Lead Exposure
journal, May 2008


Maternal Genistein Alters Coat Color and Protects A vy Mouse Offspring from Obesity by Modifying the Fetal Epigenome
journal, April 2006

  • Dolinoy, Dana C.; Weidman, Jennifer R.; Waterland, Robert A.
  • Environmental Health Perspectives, Vol. 114, Issue 4
  • DOI: 10.1289/ehp.8700

Exposure to lead and the developmental origin of oxidative DNA damage in the aging brain
journal, April 2006

  • Bolin, Celeste M.; Basha, Riyaz; Cox, David
  • The FASEB Journal, Vol. 20, Issue 6
  • DOI: 10.1096/fj.05-5091fje

Adaptive radiation-induced epigenetic alterations mitigated by antioxidants
journal, February 2013

  • Bernal, Autumn J.; Dolinoy, Dana C.; Huang, Dale
  • The FASEB Journal, Vol. 27, Issue 2
  • DOI: 10.1096/fj.12-220350

Early exposure to lead and juvenile delinquency
journal, November 2001


Genomic Imprinting: A Mammalian Epigenetic Discovery Model
journal, December 2011


Lead exposure in consumers of culled invasive alien mammals in El Palmar National Park, Argentina
journal, April 2021

  • Tammone, Agostina; Caselli, Andrea Elsa; Condorí, Walter Ezequiel
  • Environmental Science and Pollution Research, Vol. 28, Issue 31
  • DOI: 10.1007/s11356-021-13654-7

Anodic stripping voltammetry procedure modified for improved accuracy of blood lead analysis.
journal, March 1988


The role of imprinted genes in humans
journal, January 2011


Neurotoxic Effects and Biomarkers of Lead Exposure: A Review
journal, January 2009


Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation
journal, June 2003


Epigenotype-phenotype correlations in Beckwith-Wiedemann syndrome
journal, December 2000


Persistent epigenetic differences associated with prenatal exposure to famine in humans
journal, October 2008

  • Heijmans, B. T.; Tobi, E. W.; Stein, A. D.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 44
  • DOI: 10.1073/pnas.0806560105

Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice
journal, October 2013

  • Faulk, Christopher; Barks, Amanda; Liu, Kevin
  • Epigenomics, Vol. 5, Issue 5
  • DOI: 10.2217/epi.13.49

A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting
journal, May 1990

  • DeChiara, Thomas M.; Efstratiadis, Argiris; Robertsen, Elizabeth J.
  • Nature, Vol. 345, Issue 6270
  • DOI: 10.1038/345078a0

The Human Imprintome: Regulatory Mechanisms, Methods of Ascertainment, and Roles in Disease Susceptibility
journal, December 2012


An imprinted gene network that controls mammalian somatic growth is down-regulated during postnatal growth deceleration in multiple organs
journal, July 2008

  • Lui, Julian C.; Finkielstain, Gabriela P.; Barnes, Kevin M.
  • American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 295, Issue 1
  • DOI: 10.1152/ajpregu.00182.2008

Temporal stability and age-related prevalence of loss of imprinting of the insulin-like growth factor-2 gene
journal, February 2009

  • Cruz-Correa, Marcia; Zhao, Ronghua; Oveido, Myriam
  • Epigenetics, Vol. 4, Issue 2
  • DOI: 10.4161/epi.4.2.7954

Parental Socioeconomic Status and Risk of Offspring Autism Spectrum Disorders in a Swedish Population-Based Study
journal, May 2012

  • Rai, Dheeraj; Lewis, Glyn; Lundberg, Michael
  • Journal of the American Academy of Child & Adolescent Psychiatry, Vol. 51, Issue 5
  • DOI: 10.1016/j.jaac.2012.02.012

Loss of IGF2 Imprinting: A Potential Marker of Colorectal Cancer Risk
journal, March 2003


Imprinting evolution and the price of silence
journal, May 2003


Association of cord blood methylation fractions at imprinted insulin-like growth factor 2 (IGF2), plasma IGF2, and birth weight
journal, March 2012


Hypothalamic expression of Peg3 gene is associated with maternal care differences between SM/J and LG/J mouse strains : Maternal Care and
journal, May 2012

  • Chiavegatto, Silvana; Sauce, Bruno; Ambar, Guilherme
  • Brain and Behavior, Vol. 2, Issue 4
  • DOI: 10.1002/brb3.58

Quantitative analysis of DNA methylation at all human imprinted regions reveals preservation of epigenetic stability in adult somatic tissue
journal, January 2011

  • Woodfine, Kathryn; Huddleston, Joanna E.; Murrell, Adele
  • Epigenetics & Chromatin, Vol. 4, Issue 1
  • DOI: 10.1186/1756-8935-4-1

Low-level lead-induced neurotoxicity in children: an update on central nervous system effects
journal, July 1998


Metabolic Flexibility Assists Reprograming of Central and Peripheral Innate Immunity During Neurodevelopment
journal, October 2020


Zac1 Regulates an Imprinted Gene Network Critically Involved in the Control of Embryonic Growth
journal, November 2006


Genomic imprinting: parental influence on the genome
journal, January 2001

  • Reik, Wolf; Walter, Jörn
  • Nature Reviews Genetics, Vol. 2, Issue 1
  • DOI: 10.1038/35047554

The evolution of imprinting: chromosomal mapping of orthologues of mammalian imprinted domains in monotreme and marsupial mammals
journal, January 2007

  • Edwards, Carol A.; Rens, Willem; Clarke, Oliver
  • BMC Evolutionary Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1471-2148-7-157

Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions
journal, October 2006

  • Zhao, Zhihu; Tavoosidana, Gholamreza; Sjölinder, Mikael
  • Nature Genetics, Vol. 38, Issue 11
  • DOI: 10.1038/ng1891

Imprinting Weaves Its Web
journal, November 2006


Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke
journal, February 2012


Impaired glucose homeostasis in transgenic mice expressing the human transient neonatal diabetes mellitus locus, TNDM
journal, August 2004

  • Ma, Dan; Shield, Julian P. H.; Dean, Wendy
  • Journal of Clinical Investigation, Vol. 114, Issue 3
  • DOI: 10.1172/jci200419876

Biomarkers of Lead Exposure and DNA Methylation within Retrotransposons
journal, June 2010

  • Wright, Robert O.; Schwartz, Joel; Wright, Rosalind J.
  • Environmental Health Perspectives, Vol. 118, Issue 6
  • DOI: 10.1289/ehp.0901429

Deregulation of an imprinted gene network in prostate cancer
journal, February 2014

  • Ribarska, Teodora; Goering, Wolfgang; Droop, Johanna
  • Epigenetics, Vol. 9, Issue 5
  • DOI: 10.4161/epi.28006

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
journal, January 2001

  • Nakagawa, H.; Chadwick, R. B.; Peltomaki, P.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 2
  • DOI: 10.1073/pnas.98.2.591

Longitudinal Analyses of Prenatal and Postnatal Lead Exposure and Early Cognitive Development
journal, April 1987

  • Bellinger, David; Leviton, Alan; Waternaux, Christine
  • New England Journal of Medicine, Vol. 316, Issue 17
  • DOI: 10.1056/nejm198704233161701

Differentially Methylated Regions of Imprinted Genes in Prenatal, Perinatal and Postnatal Human Tissues
journal, July 2012


The early-life social environment and DNA methylation
journal, February 2012


Impaired glucose homeostasis in transgenic mice expressing the human transient neonatal diabetes mellitus locus, TNDM
journal, August 2004

  • Ma, Dan; Shield, Julian P. H.; Dean, Wendy
  • Journal of Clinical Investigation, Vol. 114, Issue 3
  • DOI: 10.1172/JCI19876

Influence of Prenatal Lead Exposure on Genomic Methylation of Cord Blood DNA
journal, January 2009


Exposure to lead and the developmental origin of oxidative DNA damage in the aging brain
journal, April 2006

  • Bolin, Celeste M.; Basha, Riyaz; Cox, David
  • The FASEB Journal, Vol. 20, Issue 6
  • DOI: 10.1096/fj.05-5091fje

Deprivation, ethnicity and the prevalence of intellectual and developmental disabilities
journal, October 2010


Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions
journal, October 2006

  • Zhao, Zhihu; Tavoosidana, Gholamreza; Sjölinder, Mikael
  • Nature Genetics, Vol. 38, Issue 11
  • DOI: 10.1038/ng1891

Neuropsychological studies in children with elevated tooth-lead concentrations: II. Extended Study
journal, March 1983

  • Winneke, G.; Kr�mer, U.; Brockhaus, A.
  • International Archives of Occupational and Environmental Health, Vol. 51, Issue 3
  • DOI: 10.1007/bf00377755

Peg3/Pw1 Is a Mediator between p53 and Bax in DNA Damage-induced Neuronal Death
journal, April 2002

  • Johnson, Mark D.; Wu, Xiangwei; Aithmitti, Nadia
  • Journal of Biological Chemistry, Vol. 277, Issue 25
  • DOI: 10.1074/jbc.m201907200

DNA hypomethylation and human diseases
journal, January 2007

  • Wilson, Ann S.; Power, Barbara E.; Molloy, Peter L.
  • Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, Vol. 1775, Issue 1
  • DOI: 10.1016/j.bbcan.2006.08.007

Epigenetic histone modification regulates developmental lead exposure induced hyperactivity in rats
journal, February 2014


Phenotypic plasticity and the epigenetics of human disease
journal, May 2007


A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting
journal, May 1990

  • DeChiara, Thomas M.; Efstratiadis, Argiris; Robertsen, Elizabeth J.
  • Nature, Vol. 345, Issue 6270
  • DOI: 10.1038/345078a0

Parental Socioeconomic Status and Risk of Offspring Autism Spectrum Disorders in a Swedish Population-Based Study
journal, May 2012

  • Rai, Dheeraj; Lewis, Glyn; Lundberg, Michael
  • Journal of the American Academy of Child & Adolescent Psychiatry, Vol. 51, Issue 5
  • DOI: 10.1016/j.jaac.2012.02.012

Maternal and child undernutrition: consequences for adult health and human capital
journal, January 2008


Season of Conception in Rural Gambia Affects DNA Methylation at Putative Human Metastable Epialleles
journal, December 2010


Deregulation of an imprinted gene network in prostate cancer
journal, February 2014

  • Ribarska, Teodora; Goering, Wolfgang; Droop, Johanna
  • Epigenetics, Vol. 9, Issue 5
  • DOI: 10.4161/epi.28006

Influence of Prenatal Lead Exposure on Genomic Methylation of Cord Blood DNA
journal, September 2009

  • Pilsner, J. Richard; Hu, Howard; Ettinger, Adrienne
  • Environmental Health Perspectives, Vol. 117, Issue 9
  • DOI: 10.1289/ehp.0800497

Epigenotype-phenotype correlations in Beckwith-Wiedemann syndrome
journal, December 2000


Persistent epigenetic differences associated with prenatal exposure to famine in humans
journal, October 2008

  • Heijmans, B. T.; Tobi, E. W.; Stein, A. D.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 44
  • DOI: 10.1073/pnas.0806560105

An Extensive Genetic Program Occurring during Postnatal Growth in Multiple Tissues
journal, April 2009

  • Finkielstain, Gabriela P.; Forcinito, Patricia; Lui, Julian C. K.
  • Endocrinology, Vol. 150, Issue 4
  • DOI: 10.1210/en.2008-0868

Association of Prenatal and Childhood Blood Lead Concentrations with Criminal Arrests in Early Adulthood
journal, May 2008


Transposable Elements: Targets for Early Nutritional Effects on Epigenetic Gene Regulation
journal, August 2003


Genomic imprinting: parental influence on the genome
journal, January 2001

  • Reik, Wolf; Walter, Jörn
  • Nature Reviews Genetics, Vol. 2, Issue 1
  • DOI: 10.1038/35047554

Biomarkers of Lead Exposure and DNA Methylation within Retrotransposons
journal, June 2010

  • Wright, Robert O.; Schwartz, Joel; Wright, Rosalind J.
  • Environmental Health Perspectives, Vol. 118, Issue 6
  • DOI: 10.1289/ehp.0901429

Phenotypic plasticity and the epigenetics of human disease
journal, May 2007


Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke
journal, February 2012


Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development
journal, August 2007

  • Dolinoy, D. C.; Huang, D.; Jirtle, R. L.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 32
  • DOI: 10.1073/pnas.0703739104

Quantitative analysis of DNA methylation at all human imprinted regions reveals preservation of epigenetic stability in adult somatic tissue
journal, January 2011

  • Woodfine, Kathryn; Huddleston, Joanna E.; Murrell, Adele
  • Epigenetics & Chromatin, Vol. 4, Issue 1
  • DOI: 10.1186/1756-8935-4-1

The evolution of imprinting: chromosomal mapping of orthologues of mammalian imprinted domains in monotreme and marsupial mammals
journal, January 2007

  • Edwards, Carol A.; Rens, Willem; Clarke, Oliver
  • BMC Evolutionary Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1471-2148-7-157

CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus
journal, May 2000

  • Hark, Amy T.; Schoenherr, Christopher J.; Katz, David J.
  • Nature, Vol. 405, Issue 6785
  • DOI: 10.1038/35013106

Imprinting evolution and the price of silence
journal, May 2003


Adaptive radiation-induced epigenetic alterations mitigated by antioxidants
journal, February 2013

  • Bernal, Autumn J.; Dolinoy, Dana C.; Huang, Dale
  • The FASEB Journal, Vol. 27, Issue 2
  • DOI: 10.1096/fj.12-220350

How imprinting centres work
journal, January 2006

  • Lewis, A.; Reik, W.
  • Cytogenetic and Genome Research, Vol. 113, Issue 1-4
  • DOI: 10.1159/000090818

Associations between Methylation of Paternally Expressed Gene 3 (PEG3), Cervical Intraepithelial Neoplasia and Invasive Cervical Cancer
text, January 2013

  • Britta, Swai,; Brandi, Vasquez,; Pendo, Mlay,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/vg71-fn43

Hypothalamic expression of Peg3 gene is associated with maternal care differences between SM/J and LG/J mouse strains : Maternal Care and
journal, May 2012

  • Chiavegatto, Silvana; Sauce, Bruno; Ambar, Guilherme
  • Brain and Behavior, Vol. 2, Issue 4
  • DOI: 10.1002/brb3.58

Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice
journal, October 2013

  • Faulk, Christopher; Barks, Amanda; Liu, Kevin
  • Epigenomics, Vol. 5, Issue 5
  • DOI: 10.2217/epi.13.49

Transactivation of Igf2 in a mouse model of Beckwith–Wiedemann syndrome
journal, October 1997

  • Sun, Fang-Lin; Dean, Wendy L.; Kelsey, Gavin
  • Nature, Vol. 389, Issue 6653
  • DOI: 10.1038/39797

Imprint regulatory elements as epigenetic biosensors of exposure in epidemiological studies
journal, August 2009

  • Hoyo, C.; Murphy, S. K.; Jirtle, R. L.
  • Journal of Epidemiology & Community Health, Vol. 63, Issue 9
  • DOI: 10.1136/jech.2009.090803

Long term low-dose arsenic exposure induces loss of DNA methylation
journal, January 2007

  • Reichard, John F.; Schnekenburger, Michael; Puga, Alvaro
  • Biochemical and Biophysical Research Communications, Vol. 352, Issue 1
  • DOI: 10.1016/j.bbrc.2006.11.001

The Genome- and System-Wide Response of DNA Methylation to Early Life Adversity and its Implication on Mental Health
journal, December 2013


Influence of Prenatal Lead Exposure on Genomic Methylation of Cord Blood DNA
journal, January 2009


A critical role for IGF-II in memory consolidation and enhancement
journal, January 2011

  • Chen, Dillon Y.; Stern, Sarah A.; Garcia-Osta, Ana
  • Nature, Vol. 469, Issue 7331
  • DOI: 10.1038/nature09667

An imprinted gene network that controls mammalian somatic growth is down-regulated during postnatal growth deceleration in multiple organs
journal, July 2008

  • Lui, Julian C.; Finkielstain, Gabriela P.; Barnes, Kevin M.
  • American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 295, Issue 1
  • DOI: 10.1152/ajpregu.00182.2008

Temporal stability and age-related prevalence of loss of imprinting of the insulin-like growth factor-2 gene
journal, February 2009

  • Cruz-Correa, Marcia; Zhao, Ronghua; Oveido, Myriam
  • Epigenetics, Vol. 4, Issue 2
  • DOI: 10.4161/epi.4.2.7954

Low-Level Fetal Lead Exposure Effect on Neurobehavioral Development in Early Infancy
journal, November 1987

  • Dietrich, Kim N.; Krafft, Kathleen M.; Bornschein, Robert L.
  • Pediatrics, Vol. 80, Issue 5
  • DOI: 10.1542/peds.80.5.721

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journal, January 2019


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journal, March 2018


The Genetic Basis for Variation in Sensitivity to Lead Toxicity in Drosophila melanogaster
journal, July 2016

  • Zhou, Shanshan; Morozova, Tatiana V.; Hussain, Yasmeen N.
  • Environmental Health Perspectives, Vol. 124, Issue 7
  • DOI: 10.1289/ehp.1510513

Low-level Gestational Lead Exposure Alters Dendritic Spine Plasticity in the Hippocampus and Reduces Learning and Memory in Rats
journal, February 2018


Genetics of the human placenta: implications for toxicokinetics
journal, September 2016

  • Gundacker, Claudia; Neesen, Jürgen; Straka, Elisabeth
  • Archives of Toxicology, Vol. 90, Issue 11
  • DOI: 10.1007/s00204-016-1816-6

Sleep duration and fragmentation in relation to leukocyte DNA methylation in adolescents
journal, June 2019

  • Jansen, Erica C.; Dolinoy, Dana C.; O’Brien, Louise M.
  • Sleep, Vol. 42, Issue 9
  • DOI: 10.1093/sleep/zsz121

Adolescent epigenetic profiles and environmental exposures from early life through peri-adolescence
journal, August 2016

  • Goodrich, Jaclyn M.; Dolinoy, Dana C.; Sánchez, Brisa N.
  • Environmental Epigenetics, Vol. 2, Issue 3
  • DOI: 10.1093/eep/dvw018

DNA methylation of imprinted genes in Mexican–American newborn children with prenatal phthalate exposure
journal, July 2018

  • Tindula, Gwen; Murphy, Susan K.; Grenier, Carole
  • Epigenomics, Vol. 10, Issue 7
  • DOI: 10.2217/epi-2017-0178

An epigenome‐wide DNA methylation study of workers with an occupational exposure to lead
journal, May 2019

  • Zhang, Xing‐xu; He, Zhen; Feng, Bin
  • Journal of Applied Toxicology, Vol. 39, Issue 9
  • DOI: 10.1002/jat.3816

Adolescent epigenetic profiles and environmental exposures from early life through peri-adolescence
journal, August 2016

  • Goodrich, Jaclyn M.; Dolinoy, Dana C.; Sánchez, Brisa N.
  • Environmental Epigenetics, Vol. 2, Issue 3
  • DOI: 10.1093/eep/dvw018

Cadmium exposure and MEG3 methylation differences between Whites and African Americans in the NEST Cohort
journal, July 2019

  • House, John S.; Hall, Jonathan; Park, Sarah S.
  • Environmental Epigenetics, Vol. 5, Issue 3
  • DOI: 10.1093/eep/dvz014

Ecogenetics of lead toxicity and its influence on risk assessment
journal, May 2019


Epigenetics, obesity and early-life cadmium or lead exposure
journal, January 2017

  • Park, Sarah S.; Skaar, David A.; Jirtle, Randy L.
  • Epigenomics, Vol. 9, Issue 1
  • DOI: 10.2217/epi-2016-0047

Large epigenome-wide association study of childhood ADHD identifies peripheral DNA methylation associated with disease and polygenic risk burden
journal, January 2020

  • Mooney, Michael A.; Ryabinin, Peter; Wilmot, Beth
  • Translational Psychiatry, Vol. 10, Issue 1
  • DOI: 10.1038/s41398-020-0710-4

DNA methylation of imprinted gene control regions in the regression of low-grade cervical lesions: Regression of low-grade cervical lesions
journal, March 2018

  • Gomih, Ayodele; Smith, Jennifer S.; North, Kari E.
  • International Journal of Cancer, Vol. 143, Issue 3
  • DOI: 10.1002/ijc.31350

Sexually Dimorphic Effects of Early-Life Exposures to Endocrine Disruptors: Sex-Specific Epigenetic Reprogramming as a Potential Mechanism
journal, October 2017

  • McCabe, Carolyn; Anderson, Olivia S.; Montrose, Luke
  • Current Environmental Health Reports, Vol. 4, Issue 4
  • DOI: 10.1007/s40572-017-0170-z

Association of blood leukocyte DNA methylation at LINE-1 and growth-related candidate genes with pubertal onset and progression
journal, December 2018


Perinatal Bisphenol A Exposure and Reprogramming of Imprinted Gene Expression in the Adult Mouse Brain
journal, October 2019

  • Malloy, Maureen A.; Kochmanski, Joseph J.; Jones, Tamara R.
  • Frontiers in Genetics, Vol. 10
  • DOI: 10.3389/fgene.2019.00951

Different People, Different Outcomes: Assessing Genetic Susceptibility to Lead Exposures
journal, July 2016


Epigenetics, obesity and early-life cadmium or lead exposure
journal, January 2017

  • Park, Sarah S.; Skaar, David A.; Jirtle, Randy L.
  • Epigenomics, Vol. 9, Issue 1
  • DOI: 10.2217/epi-2016-0047

Effects of Cadmium Exposure on DNA Methylation at Imprinting Control Regions and Genome-Wide in Mothers and Newborn Children
journal, March 2018

  • Cowley, Michael; Skaar, David A.; Jima, Dereje D.
  • Environmental Health Perspectives, Vol. 126, Issue 3
  • DOI: 10.1289/ehp2085