Environmental chemicals and DNA methylation in adults: a systematic review of the epidemiologic evidence

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Abstract

Current evidence supports the notion that environmental exposures are associated with DNA-methylation and expression changes that can impact human health. Our objective was to conduct a systematic review of epidemiologic studies evaluating the association between environmental chemicals with DNA methylation levels in adults. After excluding arsenic, recently evaluated in a systematic review, we identified a total of 17 articles (6 on cadmium, 4 on lead, 2 on mercury, 1 on nickel, 1 on antimony, 1 on tungsten, 5 on persistent organic pollutants and perfluorinated compounds, 1 on bisphenol A, and 3 on polycyclic aromatic hydrocarbons). The selected articles reported quantitative methods to determine DNA methylation including immunocolorimetric assays for total content of genomic DNA methylation, and microarray technologies, methylation-specific quantitative PCR, Luminometric Methylation Assay (LUMA), and bisulfite pyrosequencing for DNA methylation content of genomic sites such as gene promoters, LINE-1, Alu elements, and others. Considering consistency, temporality, strength, dose-response relationship, and biological plausibility, we concluded that the current evidence is not sufficient to provide inference because differences across studies and limited samples sizes make it difficult to compare across studies and to evaluate sources of heterogeneity. Important questions for future research include the need for larger and longitudinal studies, the validation of findings, and the systematic evaluation of the dose-response relationships. Future studies should also consider the evaluation of epigenetic marks recently in the research spotlight such as DNA hydroxymethylation and the role of underlying genetic variants.

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The online version of this article (doi:10.1186/s13148-015-0055-7) contains supplementary material, which is available to authorized users.

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Most cited references 106

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Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution.

Michael J Booth, Miguel R Branco, Gabriella Ficz … (2012)

5-Methylcytosine can be converted to 5-hydroxymethylcytosine (5hmC) in mammalian DNA by the ten-eleven translocation (TET) enzymes. We introduce oxidative bisulfite sequencing (oxBS-Seq), the first method for quantitative mapping of 5hmC in genomic DNA at single-nucleotide resolution. Selective chemical oxidation of 5hmC to 5-formylcytosine (5fC) enables bisulfite conversion of 5fC to uracil. We demonstrate the utility of oxBS-Seq to map and quantify 5hmC at CpG islands (CGIs) in mouse embryonic stem (ES) cells and identify 800 5hmC-containing CGIs that have on average 3.3% hydroxymethylation. High levels of 5hmC were found in CGIs associated with transcriptional regulators and in long interspersed nuclear elements, suggesting that these regions might undergo epigenetic reprogramming in ES cells. Our results open new questions on 5hmC dynamics and sequence-specific targeting by TETs.

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Lead Exposure and Cardiovascular Disease—A Systematic Review

Ana Navas-Acien, Eliseo Guallar, Ellen Silbergeld … (2006)

Objective This systematic review evaluates the evidence on the association between lead exposure and cardiovascular end points in human populations. Methods We reviewed all observational studies from database searches and citations regarding lead and cardiovascular end points. Results A positive association of lead exposure with blood pressure has been identified in numerous studies in different settings, including prospective studies and in relatively homogeneous socioeconomic status groups. Several studies have identified a dose–response relationship. Although the magnitude of this association is modest, it may be underestimated by measurement error. The hypertensive effects of lead have been confirmed in experimental models. Beyond hypertension, studies in general populations have identified a positive association of lead exposure with clinical cardiovascular outcomes (cardiovascular, coronary heart disease, and stroke mortality; and peripheral arterial disease), but the number of studies is small. In some studies these associations were observed at blood lead levels < 5 μg/dL. Conclusions We conclude that the evidence is sufficient to infer a causal relationship of lead exposure with hypertension. We conclude that the evidence is suggestive but not sufficient to infer a causal relationship of lead exposure with clinical cardiovascular outcomes. There is also suggestive but insufficient evidence to infer a causal relationship of lead exposure with heart rate variability. Public Health Implications These findings have immediate public health implications. Current occupational safety standards for blood lead must be lowered and a criterion for screening elevated lead exposure needs to be established in adults. Risk assessment and economic analyses of lead exposure impact must include the cardiovascular effects of lead. Finally, regulatory and public health interventions must be developed and implemented to further prevent and reduce lead exposure.

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A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements.

Allen Yang, Marcos R H Estécio, Ketan Doshi … (2004)

We report a method for studying global DNA methylation based on using bisulfite treatment of DNA and simultaneous PCR of multiple DNA repetitive elements, such as Alu elements and long interspersed nucleotide elements (LINE). The PCR product, which represents a pool of approximately 15 000 genomic loci, could be used for direct sequencing, selective restriction digestion or pyrosequencing, in order to quantitate DNA methylation. By restriction digestion or pyrosequencing, the assay was reproducible with a standard deviation of only 2% between assays. Using this method we found that almost two-thirds of the CpG methylation sites in Alu elements are mutated, but of the remaining methylation target sites, 87% were methylated. Due to the heavy methylation of repetitive elements, this assay was especially useful in detecting decreases in DNA methylation, and this assay was validated by examining cell lines treated with the methylation inhibitor 5-aza-2'deoxycytidine (DAC), where we found a 1-16% decrease in Alu element and 18-60% LINE methylation within 3 days of treatment. This method can be used as a surrogate marker of genome-wide methylation changes. In addition, it is less labor intensive and requires less DNA than previous methods of assessing global DNA methylation.

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Author and article information

Contributors

Adrian Ruiz-Hernandez: anruhe@gmail.com

Chin-Chi Kuo: chinchik@gmail.com

Pilar Rentero-Garrido: Pilar.Rentero@uv.es

Wan-Yee Tang: wtang10@jhu.edu

Josep Redon: josep.redon@uv.es

Jose M Ordovas: jose.ordovas@tufts.edu

Ana Navas-Acien: anavas1@jhu.edu

Maria Tellez-Plaza: maria.tellez@uv.es

Journal

Journal ID (nlm-ta): Clin Epigenetics

Journal ID (iso-abbrev): Clin Epigenetics

Title: Clinical Epigenetics

Publisher: BioMed Central (London )

ISSN (Print): 1868-7075

ISSN (Electronic): 1868-7083

Publication date (Electronic): 29 April 2015

Publication date PMC-release: 29 April 2015

Publication date Collection: 2015

Volume: 7

Issue: 1

Electronic Location Identifier: 55

Affiliations

[ ]Department of Internal Medicine, Hospital Clínico de Valencia, Avenida Blasco Ibañez, 17, 46010 Valencia, Spain

[ ]Area of Cardiometabolic and Renal Risk, Institute for Biomedical Research Hospital Clinic de Valencia INCLIVA, Av. Menendez Pelayo 4, Accesorio, 46010 Valencia, Spain

[ ]Department of Environmental Health Sciences, Johns Hopkins University Bloomberg School of Public Health, 615 North Wolfe Street, Baltimore, MD 21205 USA

[ ]Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Baltimore, MD 21205 USA

[ ]Department of Internal Medicine, Kidney Institute and Division of Nephrology, China Medical University Hospital and College of Medicine, China Medical University, 2 Yude Road, Taichung, 40447 Taiwan

[ ]Genotyping and Genetic Diagnosis Unit, Institute for Biomedical Research INCLIVA, Av. Menendez Pelayo, 4 Accesorio, 46010 Valencia, Spain

[ ]CIBER Physiopathology of Obesity and Nutrition (CIBEROBN), Institute of Health Carlos III, Minister of Health, Madrid, Spain

[ ]Nutrition and Genomics Laboratory, Jean Mayer US Department of Agriculture Human Nutrition Research Center on Aging at Tufts University, 711 Washington St, Boston, MA 02111-1524 USA

[ ]Instituto Madrileño de Estudios Avanzados en Alimentación, Ctra. de Cantoblanco 8, 28049 Madrid, Spain

[ ]Welch Center for Prevention, Epidemiology and Clinical Research, Johns Hopkins Medical Institutions, 2024 E. Monument Street, Baltimore, 21205 MD USA

Article

Publisher ID: 55

DOI: 10.1186/s13148-015-0055-7

PMC ID: 4433069

PubMed ID: 25984247

SO-VID: 3a5b54f6-ab56-43f2-8bff-6d888942ee5f

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 5 November 2014

Date accepted : 9 February 2015

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ScienceOpen disciplines: Genetics

Keywords: systematic review,dna methylation,environmental chemicals,cadmium,lead,mercury,metals,persistent organic pollutants,bisphenol a,polycyclic aromatic hydrocarbons

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ScienceOpen disciplines: Genetics

Keywords: systematic review, dna methylation, environmental chemicals, cadmium, lead, mercury, metals, persistent organic pollutants, bisphenol a, polycyclic aromatic hydrocarbons

Environmental chemicals and DNA methylation in adults: a systematic review of the epidemiologic evidence

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Most cited references 106

Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution.

Lead Exposure and Cardiovascular Disease—A Systematic Review

A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements.

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