Exploring the evidence for epigenetic regulation of environmental influences on child health across generations

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Abstract

Environmental exposures, psychosocial stressors and nutrition are all potentially important influences that may impact health outcomes directly or via interactions with the genome or epigenome over generations. While there have been clear successes in large-scale human genetic studies in recent decades, there is still a substantial amount of missing heritability to be elucidated for complex childhood disorders. Mounting evidence, primarily in animals, suggests environmental exposures may generate or perpetuate altered health outcomes across one or more generations. One putative mechanism for these environmental health effects is via altered epigenetic regulation. This review highlights the current epidemiologic literature and supporting animal studies that describe intergenerational and transgenerational health effects of environmental exposures. Both maternal and paternal exposures and transmission patterns are considered, with attention paid to the attendant ethical, legal and social implications.

Abstract

Carrie Breton and colleagues review the literature supporting evidence for transgenerational health effects of environmental exposures by epigenetic mechanisms. This Review summarizes current knowledge based on animal and human cohort studies, and discusses the ethical, legal, and social implications of epigenetic research in humans

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Integrative analysis of 111 reference human epigenomes

Anshul Kundaje, Wouter Meuleman, Jason Ernst … (2016)

The reference human genome sequence set the stage for studies of genetic variation and its association with human disease, but a similar reference has lacked for epigenomic studies. To address this need, the NIH Roadmap Epigenomics Consortium generated the largest collection to-date of human epigenomes for primary cells and tissues. Here, we describe the integrative analysis of 111 reference human epigenomes generated as part of the program, profiled for histone modification patterns, DNA accessibility, DNA methylation, and RNA expression. We establish global maps of regulatory elements, define regulatory modules of coordinated activity, and their likely activators and repressors. We show that disease and trait-associated genetic variants are enriched in tissue-specific epigenomic marks, revealing biologically-relevant cell types for diverse human traits, and providing a resource for interpreting the molecular basis of human disease. Our results demonstrate the central role of epigenomic information for understanding gene regulation, cellular differentiation, and human disease.

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Chromatin remodelling during development.

Lena Ho, Gerald R Crabtree (2010)

New methods for the genome-wide analysis of chromatin are providing insight into its roles in development and their underlying mechanisms. Current studies indicate that chromatin is dynamic, with its structure and its histone modifications undergoing global changes during transitions in development and in response to extracellular cues. In addition to DNA methylation and histone modification, ATP-dependent enzymes that remodel chromatin are important controllers of chromatin structure and assembly, and are major contributors to the dynamic nature of chromatin. Evidence is emerging that these chromatin-remodelling enzymes have instructive and programmatic roles during development. Particularly intriguing are the findings that specialized assemblies of ATP-dependent remodellers are essential for establishing and maintaining pluripotent and multipotent states in cells.

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Persistent epigenetic differences associated with prenatal exposure to famine in humans.

B. Heijmans, E. Tobi, A. Stein … (2008)

Extensive epidemiologic studies have suggested that adult disease risk is associated with adverse environmental conditions early in development. Although the mechanisms behind these relationships are unclear, an involvement of epigenetic dysregulation has been hypothesized. Here we show that individuals who were prenatally exposed to famine during the Dutch Hunger Winter in 1944-45 had, 6 decades later, less DNA methylation of the imprinted IGF2 gene compared with their unexposed, same-sex siblings. The association was specific for periconceptional exposure, reinforcing that very early mammalian development is a crucial period for establishing and maintaining epigenetic marks. These data are the first to contribute empirical support for the hypothesis that early-life environmental conditions can cause epigenetic changes in humans that persist throughout life.

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Author and article information

Contributors

Carrie V. Breton:

ORCID: http://orcid.org/0000-0002-6082-4066

breton@usc.edu

Journal

Journal ID (nlm-ta): Commun Biol

Journal ID (iso-abbrev): Commun Biol

Title: Communications Biology

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2399-3642

Publication date (Electronic): 22 June 2021

Publication date PMC-release: 22 June 2021

Publication date Collection: 2021

Volume: 4

Electronic Location Identifier: 769

Affiliations

[1 ]GRID grid.42505.36, ISNI 0000 0001 2156 6853, Department of Preventive Medicine, Keck School of Medicine, , University of Southern California, ; Los Angeles, CA USA

[2 ]GRID grid.137628.9, ISNI 0000 0004 1936 8753, Department of Pediatrics, , NYU Grossman School of Medicine, ; New York, NY USA

[3 ]GRID grid.2515.3, ISNI 0000 0004 0378 8438, Department of Psychiatry, , Boston Children’s Hospital and Harvard Medical School, ; Boston, MA USA

[4 ]GRID grid.40263.33, ISNI 0000 0004 1936 9094, Department of Epidemiology, , Brown University School of Public Health, ; Providence, RI USA

[5 ]GRID grid.17088.36, ISNI 0000 0001 2150 1785, Department of Food Science and Human Nutrition, , Michigan State University, ; East Lansing, MI USA

[6 ]GRID grid.413734.6, ISNI 0000 0000 8499 1112, Department of Psychiatry, Vagelos College of Physicians and Surgeons, , Columbia University Irving Medical Center and New York State Psychiatric Institute, ; New York, NY USA

[7 ]GRID grid.21925.3d, ISNI 0000 0004 1936 9000, Department of Psychiatry, , University of Pittsburgh, ; Pittsburgh, PA USA

[8 ]GRID grid.27860.3b, ISNI 0000 0004 1936 9684, Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, California National Primate Research Center, , University of California, Davis, ; Davis, CA USA

[9 ]GRID grid.27860.3b, ISNI 0000 0004 1936 9684, Department of Medical Microbiology and Immunology, MIND Institute, Genome Center, , University of California, Davis, ; Davis, CA USA

[10 ]GRID grid.59734.3c, ISNI 0000 0001 0670 2351, Icahn School of Medicine at Mount Sinai, ; New York, NY USA

[11 ]GRID grid.21107.35, ISNI 0000 0001 2171 9311, Department of Mental Health, , Johns Hopkins Bloomberg School of Public Health, ; Baltimore, MD USA

[12 ]GRID grid.27860.3b, ISNI 0000 0004 1936 9684, Department of Public Health Sciences, , UC Davis School of Medicine, ; Davis, CA USA

[13 ]GRID grid.189967.8, ISNI 0000 0001 0941 6502, Department of Epidemiology, , Emory University, ; Atlanta, GA USA

[14 ]GRID grid.42505.36, ISNI 0000 0001 2156 6853, Department of Biochemistry and Molecular Medicine, , University of Southern California, ; Los Angeles, CA USA

[15 ]GRID grid.266102.1, ISNI 0000 0001 2297 6811, Division of Research, Kaiser Permanente Northern California and Department of Epidemiology and Biostatistics, , University of California, San Francisco, ; Oakland, CA USA

[16 ]GRID grid.10698.36, ISNI 0000000122483208, Department of Environmental Sciences and Engineering, , Gillings School of Global Public Health, UNC Chapel Hill, ; Chapel Hill, NC USA

Author information

Carrie V. Breton http://orcid.org/0000-0002-6082-4066

Linda G. Kahn http://orcid.org/0000-0002-6512-6160

Hong Ji http://orcid.org/0000-0002-9558-0620

Janine M. LaSalle http://orcid.org/0000-0002-3480-2031

Rebecca Schmidt http://orcid.org/0000-0003-1582-2747

Shakira F. Suglia http://orcid.org/0000-0002-5634-9290

Article

Publisher ID: 2316

DOI: 10.1038/s42003-021-02316-6

PMC ID: 8219763

PubMed ID: 34158610

SO-VID: cad6e8cb-68c7-4684-988f-611234004c5b

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 23 September 2020

Date accepted : 3 June 2021

Funding

Funded by: FundRef https://doi.org/10.13039/100000052, U.S. Department of Health & Human Services | NIH | NIH Office of the Director (OD);

Award ID: U2COD023375

Award ID: U24OD023382

Award ID: UH3OD023287

Award ID: UH3OD023305

Award ID: UH3OD023337

Award ID: UH3OD023313

Award ID: UH3OD023285

Award ID: UH3OD023328

Award ID: UH3OD023244

Award ID: UH3OD023342

Award ID: UH3OD023365

Award ID: UH3OD023282

Award ID: UH3OD023289

Award ID: UH3OD023348

Award Recipient : Carrie V. Breton

Funded by: U.S. Department of Health & Human Services | NIH | NIH Office of the Director (OD)

Funded by: FundRef https://doi.org/10.13039/100000002, U.S. Department of Health & Human Services | National Institutes of Health (NIH);

Award ID: 5K99ES030403

Award ID: R01MH121070

Award ID: R01AI141569-1A1

Award ID: P30ES023513-supported EHSC scholar fund

Award ID: R01ES029213

Award ID: R01HD093643

Award ID: R01HL125761

Award ID: T32AA00745

Award ID: K01DK120807

Award Recipient : Carrie V. Breton

Funded by: U.S. Department of Health & Human Services | National Institutes of Health (NIH)

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Keywords: epigenetics,population genetics

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Keywords: epigenetics, population genetics

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Exploring the evidence for epigenetic regulation of environmental influences on child health across generations

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G3: Genes|Genomes|Genetics

Most cited references 255

Integrative analysis of 111 reference human epigenomes

Chromatin remodelling during development.

Persistent epigenetic differences associated with prenatal exposure to famine in humans.

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Cited by 42

Most referenced authors 4,542