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

Breton, Carrie V.; Landon, Remy; Kahn, Linda G.; Enlow, Michelle Bosquet; Peterson, Alicia K.; Bastain, Theresa M.; Braun, Joseph M.; Comstock, Sarah S.; Duarte, Cristiane S.; Hipwell, Alison E.; Ji, Hong; LaSalle, Janine M.; Miller, Rachel L.; Musci, Rashelle J.; Posner, Jonathan; Schmidt, Rebecca J.; Suglia, Shakira F.; Tung, Irene; Weisenberger, Daniel J.; Zhu, Yeyi; Fry, Rebecca C.

doi:10.1038/s42003-021-02316-6

Cited by 95 publications

(67 citation statements)

References 262 publications

(294 reference statements)

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“…Epigenetic marks are partly inherited (transmission of epigenetic marks from one generation to another) but are also the signature and reflection of exposure to environments throughout life, particularly the early environment during gestation and lactation, which is a very sensitive period to both internal and external factors. Indeed, epigenetic mechanisms represent a means through which environmental factors can leave long-lasting memory of past experiences ( Kundakovic and Jaric, 2017 ; Cirulli et al, 2020 ; Bellver-Sanchis et al, 2021 ; Breton et al, 2021 ). Although epigenetic modifications are often considered stable over time, epigenetic plasticity exists and may mediate adaptation to drastic environmental changes.…”

Section: Epigenetic Mechanisms Mediate Long-term Influence Of Environ...mentioning

confidence: 99%

Early-Life Environment Influence on Late-Onset Alzheimer’s Disease

Gauvrit

Benderradji

Buée

et al. 2022

Front. Cell Dev. Biol.

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With the expand of the population’s average age, the incidence of neurodegenerative disorders has dramatically increased over the last decades. Alzheimer disease (AD) which is the most prevalent neurodegenerative disease is mostly sporadic and primarily characterized by cognitive deficits and neuropathological lesions such as amyloid -β (Aβ) plaques and neurofibrillary tangles composed of hyper- and/or abnormally phosphorylated Tau protein. AD is considered a complex disease that arises from the interaction between environmental and genetic factors, modulated by epigenetic mechanisms. Besides the well-described cognitive decline, AD patients also exhibit metabolic impairments. Metabolic and cognitive perturbations are indeed frequently observed in the Developmental Origin of Health and Diseases (DOHaD) field of research which proposes that environmental perturbations during the perinatal period determine the susceptibility to pathological conditions later in life. In this review, we explored the potential influence of early environmental exposure to risk factors (maternal stress, malnutrition, xenobiotics, chemical factors … ) and the involvement of epigenetic mechanisms on the programming of late-onset AD. Animal models indicate that offspring exposed to early-life stress during gestation and/or lactation increase both AD lesions, lead to defects in synaptic plasticity and finally to cognitive impairments. This long-lasting epigenetic programming could be modulated by factors such as nutriceuticals, epigenetic modifiers or psychosocial behaviour, offering thus future therapeutic opportunity to protect from AD development.

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Section: Epigenetic Mechanisms Mediate Long-term Influence Of Environ...mentioning

confidence: 99%

Early-Life Environment Influence on Late-Onset Alzheimer’s Disease

Gauvrit

Benderradji

Buée

et al. 2022

Front. Cell Dev. Biol.

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“…This causality acquires an extra level of complexity when associations involved an environmental factor or lifestyle habits. Smoking has been widely associated with epigenetic alterations and increased risk of respiratory diseases (e.g., chronic obstructive pulmonary disease or asthma) or neurodevelopmental disorders (e.g., child attention-deficit/hyperactivity disorder) at a single generation but also in transgenerational inheritance [ 72 , 73 ]. However, studies involving different human cohorts did not allow for conclusions that a causal association between smoking, methylation and disease output exists [ 72 ].…”

Section: Current Ethical and Social Challenges Raised By Epigeneticsmentioning

confidence: 99%

Ethical implications of epigenetics in the era of personalized medicine

Santaló

Berdasco

2022

Clin Epigenet

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Given the increasing research activity on epigenetics to monitor human diseases and its connection with lifestyle and environmental expositions, the field of epigenetics has attracted a great deal of interest also at the ethical and societal level. In this review, we will identify and discuss current ethical, legal and social issues of epigenetics research in the context of personalized medicine. The review covers ethical aspects such as how epigenetic information should impact patient autonomy and the ability to generate an intentional and voluntary decision, the measures of data protection related to privacy and confidentiality derived from epigenome studies (e.g., risk of discrimination, patient re-identification and unexpected findings) or the debate in the distribution of responsibilities for health (i.e., personal versus public responsibilities). We pay special attention to the risk of social discrimination and stigmatization as a consequence of inferring information related to lifestyle and environmental exposures potentially contained in epigenetic data. Furthermore, as exposures to the environment and individual habits do not affect all populations equally, the violation of the principle of distributive justice in the access to the benefits of clinical epigenetics is discussed. In this regard, epigenetics represents a great opportunity for the integration of public policy measures aimed to create healthier living environments. Whether these public policies will coexist or, in contrast, compete with strategies reinforcing the personalized medicine interventions needs to be considered. The review ends with a reflection on the main challenges in epigenetic research, some of them in a technical dimension (e.g., assessing causality or establishing reference epigenomes) but also in the ethical and social sphere (e.g., risk to add an epigenetic determinism on top of the current genetic one). In sum, integration into life science investigation of social experiences such as exposure to risk, nutritional habits, prejudice and stigma, is imperative to understand epigenetic variation in disease. This pragmatic approach is required to locate clinical epigenetics out of the experimental laboratories and facilitate its implementation into society.

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“…Further, the findings of several studies have indicated that certain environmental exposures may impact the health of individuals for multiple generations following the initial insult (reviewed in Breton et al, 2021 ). Human and animal studies are beginning to examine multigenerational risk factors for ASD, defined here as any factors that are non-genetic but may include demographic/social factors, chemical exposures, medications, and medical conditions in the generations prior to the individual diagnosed with ASD.…”

Section: Introductionmentioning

confidence: 99%

The Promise of DNA Methylation in Understanding Multigenerational Factors in Autism Spectrum Disorders

Mouat

LaSalle

2022

Front. Genet.

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Autism spectrum disorder (ASD) is a group of neurodevelopmental disorders characterized by impairments in social reciprocity and communication, restrictive interests, and repetitive behaviors. Most cases of ASD arise from a confluence of genetic susceptibility and environmental risk factors, whose interactions can be studied through epigenetic mechanisms such as DNA methylation. While various parental factors are known to increase risk for ASD, several studies have indicated that grandparental and great-grandparental factors may also contribute. In animal studies, gestational exposure to certain environmental factors, such as insecticides, medications, and social stress, increases risk for altered behavioral phenotypes in multiple subsequent generations. Changes in DNA methylation, gene expression, and chromatin accessibility often accompany these altered behavioral phenotypes, with changes often appearing in genes that are important for neurodevelopment or have been previously implicated in ASD. One hypothesized mechanism for these phenotypic and methylation changes includes the transmission of DNA methylation marks at individual chromosomal loci from parent to offspring and beyond, called multigenerational epigenetic inheritance. Alternatively, intermediate metabolic phenotypes in the parental generation may confer risk from the original grandparental exposure to risk for ASD in grandchildren, mediated by DNA methylation. While hypothesized mechanisms require further research, the potential for multigenerational epigenetics assessments of ASD risk has implications for precision medicine as the field attempts to address the variable etiology and clinical signs of ASD by incorporating genetic, environmental, and lifestyle factors. In this review, we discuss the promise of multigenerational DNA methylation investigations in understanding the complex etiology of ASD.

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

Cited by 95 publications

References 262 publications

Early-Life Environment Influence on Late-Onset Alzheimer’s Disease

Early-Life Environment Influence on Late-Onset Alzheimer’s Disease

Ethical implications of epigenetics in the era of personalized medicine

The Promise of DNA Methylation in Understanding Multigenerational Factors in Autism Spectrum Disorders

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