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      An epigenetic synopsis of parental substance use

      1 , 1 , 2 , 2 , 3 , 2 , 4
      Epigenomics
      Future Medicine Ltd

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          Abstract

          The rate of substance use is rising, especially among reproductive-age individuals. Emerging evidence suggests that paternal pre-conception and maternal prenatal substance use may alter offspring epigenetic regulation (changes to gene expression without modifying DNA) and outcomes later in life, including neurodevelopment and mental health. However, relatively little is known due to the complexities and limitations of existing studies, making causal interpretations challenging. This review examines the contributions and influence of parental substance use on the gametes and potential transmissibility to the offspring’s epigenome as possible areas to target public health warnings and healthcare provider counseling of individuals or couples in the pre-conception and prenatal periods to ultimately mitigate short- and long-term offspring morbidity and mortality.

          Abstract

          Plain language summary

          More people, especially those of reproductive age, are using substances, and there is growing evidence to suggest that parental substance use before and during pregnancy may adversely affect offspring and result in issues later in life, including mental health challenges. Such relationships have been demonstrated with nicotine, alcohol, cannabis, opioids and illegal drugs (e.g., heroin, cocaine, methamphetamines). Some of these adverse impacts on offspring can potentially be passed down in families even after parents have quit using the substance. Because more individuals are using drugs, especially during the COVID-19 pandemic, it is important that families learn more about the potential impact of substance use on their future offspring before they try to get pregnant.

          Abstract

          Tweetable abstract

          Substance use before and during pregnancy can influence the offspring epigenome and later health outcomes. This is an area to target in public healthcare warnings and healthcare provider counseling to ultimately mitigate offspring morbidity and mortality.

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          Most cited references189

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          An epigenetic biomarker of aging for lifespan and healthspan

          Identifying reliable biomarkers of aging is a major goal in geroscience. While the first generation of epigenetic biomarkers of aging were developed using chronological age as a surrogate for biological age, we hypothesized that incorporation of composite clinical measures of phenotypic age that capture differences in lifespan and healthspan may identify novel CpGs and facilitate the development of a more powerful epigenetic biomarker of aging. Using an innovative two-step process, we develop a new epigenetic biomarker of aging, DNAm PhenoAge, that strongly outperforms previous measures in regards to predictions for a variety of aging outcomes, including all-cause mortality, cancers, healthspan, physical functioning, and Alzheimer's disease. While this biomarker was developed using data from whole blood, it correlates strongly with age in every tissue and cell tested. Based on an in-depth transcriptional analysis in sorted cells, we find that increased epigenetic, relative to chronological age, is associated with increased activation of pro-inflammatory and interferon pathways, and decreased activation of transcriptional/translational machinery, DNA damage response, and mitochondrial signatures. Overall, this single epigenetic biomarker of aging is able to capture risks for an array of diverse outcomes across multiple tissues and cells, and provide insight into important pathways in aging.
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            The diverse roles of DNA methylation in mammalian development and disease

            DNA methylation is of paramount importance for mammalian embryonic development. DNA methylation has numerous functions: it is implicated in the repression of transposons and genes, but is also associated with actively transcribed gene bodies and, in some cases, with gene activation per se. In recent years, sensitive technologies have been developed that allow the interrogation of DNA methylation patterns from a small number of cells. The use of these technologies has greatly improved our knowledge of DNA methylation dynamics and heterogeneity in embryos and in specific tissues. Combined with genetic analyses, it is increasingly apparent that regulation of DNA methylation erasure and (re-)establishment varies considerably between different developmental stages. In this Review, we discuss the mechanisms and functions of DNA methylation and demethylation in both mice and humans at CpG-rich promoters, gene bodies and transposable elements. We highlight the dynamic erasure and re-establishment of DNA methylation in embryonic, germline and somatic cell development. Finally, we provide insights into DNA methylation gained from studying genetic diseases.
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              Persistent epigenetic differences associated with prenatal exposure to famine in humans.

              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
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                Journal
                Epigenomics
                Epigenomics
                Future Medicine Ltd
                1750-1911
                1750-192X
                April 2023
                April 2023
                : 15
                : 7
                : 453-473
                Affiliations
                [1 ]Division of Reproductive & Developmental Sciences, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR 97006, USA; Department of Obstetrics & Gynecology, Maternal Fetal Medicine, Oregon Health & Science University, Portland, OR 97239, USA
                [2 ]Department of Obstetrics & Gynecology, Duke University Medical Center, Durham, NC 27710, USA
                [3 ]Division of Reproductive Endocrinology & Infertility, Department of Obstetrics & Gynecology, Duke University Medical Center, Durham, NC 27710, USA
                [4 ]Division of Reproductive Sciences, Department of Obstetrics & Gynecology, Duke University Medical Center, Durham, NC 27701, USA; Division of Environmental Sciences & Policy, Duke Nicholas School of the Environment, Duke University, Durham, NC 27708, USA; Department of Pathology, Duke University Medical Center, Durham, NC, 27710, USA
                Article
                10.2217/epi-2023-0064
                37282544
                0c91fac8-7a04-42b3-b804-a6288ee4903c
                © 2023
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