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Review
. 2020 Jan;61(1):176-192.
doi: 10.1002/em.22311. Epub 2019 Jun 20.

The role of environmental exposures and the epigenome in health and disease

Bambarendage P U Perera  1 , Christopher Faulk  2 , Laurie K Svoboda  1 , Jaclyn M Goodrich  1 , Dana C Dolinoy  1   3
Affiliations
Review

The role of environmental exposures and the epigenome in health and disease

Bambarendage P U Perera et al. Environ Mol Mutagen. 2020 Jan.

Abstract

The genetic material of every organism exists within the context of regulatory networks that govern gene expression, collectively called the epigenome. Epigenetics has taken center stage in the study of diseases such as cancer and diabetes, but its integration into the field of environmental health is still emerging. As the Environmental Mutagenesis and Genomics Society (EMGS) celebrates its 50th Anniversary this year, we have come together to review and summarize the seminal advances in the field of environmental epigenomics. Specifically, we focus on the role epigenetics may play in multigenerational and transgenerational transmission of environmentally induced health effects. We also summarize state of the art techniques for evaluating the epigenome, environmental epigenetic analysis, and the emerging field of epigenome editing. Finally, we evaluate transposon epigenetics as they relate to environmental exposures and explore the role of noncoding RNA as biomarkers of environmental exposures. Although the field has advanced over the past several decades, including being recognized by EMGS with its own Special Interest Group, recently renamed Epigenomics, we are excited about the opportunities for environmental epigenetic science in the next 50 years. Environ. Mol. Mutagen. 61:176-192, 2020. © 2019 Wiley Periodicals, Inc.

Keywords: TaRGET II; environmental epigenetics; piRNA; transposons, DNA methylation.

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Conflict of interest statement

CONFLICTS OF INTEREST

The authors declare that there are no conflicts of interest.

Figures

Fig. 1.
Fig. 1.
One-year-old female genetically identical viable yellow agouti mice (Avy). Maternal dietary supplementation with methyl donors such as folic acid, choline, and betaine (Waterland and Jirtle, 2003) or the phytoestrogen, genistein (Dolinoy et al., 2006), shifts the coat color of the offspring from yellow to brown and reduces the incidence of obesity, diabetes, and cancer. Furthermore, these maternal dietary supplements can guard the epigenome from the hypomethylating effects of BPA, a common endocrine disrupting chemical used in the production of polycarbonate plastic and epoxy resins (Dolinoy et al., 2007).
Fig. 2.
Fig. 2.
Direct and indirect effects of exposures across multiple generations. Among mammals, maternal exposures during pregnancy may directly influence the mother (F0) and child (F1). Future grandchildren (F2) may be impacted as the primordial germ cells are also directly exposed. Effects are considered transgenerational when they are observed in generations that were not directly exposed (i.e., F3, F4, and beyond in this human example).
Fig. 3.
Fig. 3.
Conceptual diagram for environmental epigenomics studies. Environmental epigenomics studies utilize surrogate tissues as proxies for epigenetic changes in target tissues and determine whether these changes correlate with disease. Several types of epigenetic changes may represent biomarkers of environmental exposures and adverse health outcomes.
Fig. 4.
Fig. 4.
Targeted epigenome editors. Epigenetic marks represent DNA methylation changes and histone modifications. The open popsicles indicate unmethylated DNA, whereas closed popsicles represent methylated DNA, while the unmodified histone (green open dot), is changed to modified histone (red dot) via epigenetic editing. (A) ZFP-based epigenome editing. (B) TALEN-based epigenome editing. (C) CRISPR/dCas9-based epigenome editing (sgRNA, single guide RNA; dCas9, deactivated Cas9; NGG/NCC, PAM sequence). The effector protein signifies a DNA/histone modifying protein that is responsible for the desired epigenetic change. (D) Potential ncRNA-based epigenetic modification. Based on current research that indicates piRNA presence and activity in somatic tissues (Perera et al., 2019), other ncRNA species may be used as potential candidates for epigenome editing. For instance, mature piRNA that contain a 2′-O-methylation modification at its 3′ end and its associated PIWIL proteins may be used to specifically methylate DNA.
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