Genome-wide DNA methylation of the liver reveals delayed effects of early-life exposure to 17-α-ethinylestradiol in the self-fertilizing mangrove rivulus

Voisin, Anne‐Sophie; Ulloa, Victoria Suarez; Stockwell, Peter A.; Chatterjee, Aniruddha; Silvestre, Frédéric

doi:10.1080/15592294.2021.1921337

Cited by 7 publications

(8 citation statements)

References 101 publications

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“…We found most of the differential methylation in intergenic regions and on introns (Figure 2C,D,F,G). Although differential methylation of noncoding regions has been reported, 16–24 little is known about its biological functions. Initially, we used HOMER to determine motif enrichment in hypo‐ and hyper‐DMSs, and found motifs supporting our model and phenotype.…”

Section: Discussionmentioning

confidence: 99%

“…[13][14][15] To date, most studies have focused on probing the alterations in DNA methylation near genes and promoters, which are easier to mechanistically link to changes in gene expression. Nonetheless, there is a growing body of literature from different animal models, tissues, and cell types reporting on prevailing differential methylation in intergenic regions, introns, and other noncoding DNA regions, [16][17][18][19][20][21][22][23][24] following the contextual and environmental stimulus. These areas in the genome may harbor cis-and trans-regulatory elements of transcription, also known as enhancers.…”

Section: Introductionmentioning

confidence: 99%

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Embryonic heat conditioning in chicks induces transgenerational heat/immunological resilience via methylation on regulatory elements

et al. 2022

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The question of whether behavioral traits are heritable is under debate. An obstacle in demonstrating transgenerational inheritance in mammals originates from the maternal environment's effect on offspring phenotype. Here, we used in ovo embryonic heat conditioning (EHC) of first-generation chicks, demonstrating heredity of both heat and immunological resilience, confirmed by a reduced fibril response in their untreated offspring to either heat or LPS challenge. Concordantly, transcriptome analysis confirmed that EHC induces changes in gene expression in the anterior preoptic hypothalamus (APH) that contribute to these phenotypes in the offspring.To study the association between epigenetic mechanisms and trait heritability, DNAmethylation patterns in the APH of offspring of control versus EHC fathers were evaluated. Genome-wide analysis revealed thousands of differentially methylated sites (DMSs), which were highly enriched in enhancers and CCCTC-binding factor (CTCF) sites. Overlap analysis revealed 110 differentially expressed genes that were associated with altered methylation, predominantly on enhancers. Gene-ontology analysis shows pathways associated with immune response, chaperone-mediated protein folding, and stress response. For the proof of concept, we focused on HSP25 and SOCS3, modulators of heat and immune responses, respectively. Chromosome conformational capture (3C) assay identified interactions between their promoters and methylated enhancers, with the strongest frequency on CTCF binding sites.Furthermore, gene expression corresponded with the differential methylation patterns, and presented increased CTCF binding in both hyper-and hypomethylated DMSs. Collectively, we demonstrate that EHC induces transgenerational thermalThis is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Embryonic heat conditioning in chicks induces transgenerational heat/immunological resilience via methylation on regulatory elements

et al. 2022

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“…Unlike genetic variation, DNA methylation can be rapidly influenced by environmental variation, particularly when the organism is in the early developmental stages [ 109 ]. Some studies have investigated the influence of the environment in shaping the epigenome under different laboratory settings (e.g., temperature [ 110 ], diet [ 111 ], behavior [ 112 ], and chemicals [ 113 ]. However, they may not reflect the epigenetic processes that occur under field conditions with natural levels of environmental heterogeneity and complexity.…”

Section: Epigenetic Dynamics In Natural Animal Populationsmentioning

confidence: 99%

Population Epigenetics: The Extent of DNA Methylation Variation in Wild Animal Populations

Chapelle

Silvestre

2022

Epigenomes

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Population epigenetics explores the extent of epigenetic variation and its dynamics in natural populations encountering changing environmental conditions. In contrast to population genetics, the basic concepts of this field are still in their early stages, especially in animal populations. Epigenetic variation may play a crucial role in phenotypic plasticity and local adaptation as it can be affected by the environment, it is likely to have higher spontaneous mutation rate than nucleotide sequences do, and it may be inherited via non-mendelian processes. In this review, we aim to bring together natural animal population epigenetic studies to generate new insights into ecological epigenetics and its evolutionary implications. We first provide an overview of the extent of DNA methylation variation and its autonomy from genetic variation in wild animal population. Second, we discuss DNA methylation dynamics which create observed epigenetic population structures by including basic population genetics processes. Then, we highlight the relevance of DNA methylation variation as an evolutionary mechanism in the extended evolutionary synthesis. Finally, we suggest new research directions by highlighting gaps in the knowledge of the population epigenetics field. As for our results, DNA methylation diversity was found to reveal parameters that can be used to characterize natural animal populations. Some concepts of population genetics dynamics can be applied to explain the observed epigenetic structure in natural animal populations. The set of recent advancements in ecological epigenetics, especially in transgenerational epigenetic inheritance in wild animal population, might reshape the way ecologists generate predictive models of the capacity of organisms to adapt to changing environments.

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“…Besides the effects on metabolic functions as mentioned above, hepatotoxicity can occur at any life stage in wildlife and humans since DBDPE is widespread in environmental and biological media. For one thing, organisms are sensitive to exogenous pollutants during early developmental stages. , Abnormalities of liver development in early life may adversely affect metabolic function in adulthood and even in offspring and increase the risk of metabolic system disorders. , For another, as the main defensive organ against endogenous and environmental stresses, the liver possesses an amazing regenerative ability. , When the normal liver is injured, hepatocytes are activated from a quiescent state into the cell cycle to proliferate for recovery of liver size and function. , If the ability to repair and regenerate is impaired, the toxic effects of pollutants on the liver will occur or be occurred or exacerbated. There are research gaps in the effects and mechanisms of DBDPE on liver development and regeneration, which limit the evaluation of hepatotoxicity and the prediction of health risks.…”

Section: Introductionmentioning

confidence: 99%

“…16,17 Abnormalities of liver development in early life may adversely affect metabolic function in adulthood and even in offspring and increase the risk of metabolic system disorders. 18,19 For another, as the main defensive organ against endogenous and environmental stresses, the liver possesses an amazing regenerative ability. 20,21 When the normal liver is injured, hepatocytes are activated from a quiescent state into the cell cycle to proliferate for recovery of liver size and function.…”

Section: Introductionmentioning

confidence: 99%

Evidence for Adverse Effects on Liver Development and Regeneration in Zebrafish by Decabromodiphenyl Ethane

Li,

Song,

Wang

et al. 2023

Environ. Sci. Technol.

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Decabromodiphenyl ethane (DBDPE), a ubiquitous emerging pollutant, could be enriched in the liver of organisms, but its effects and mechanisms on liver development and regeneration remain largely unknown. In the present study, we first investigated the adverse effects on liver development and found decreased area and intensity of fluorescence in transgenic zebrafish larvae exposed to DBDPE; further results in wild-type zebrafish larvae revealed a possible mechanism involving disturbed MAPK/Fox O signaling pathways and cell cycle arrest as indicated by decreased transcription of growth arrest and DNA-damage-inducible beta a (gadd45ba). Subsequently, an obstructed recovery process of liver tissue after partial hepatectomy was characterized by the changing profiles of ventral lobe-to-intestine ratio in transgenic female adults upon DBDPE exposure; further results confirmed the adverse effects on liver regeneration by the alterations of the hepatic somatic index and proliferating cell nuclear antigen expression in wild-type female adults and also pointed out a potential role of a disturbed signaling pathway involving cell cycles and glycerolipid metabolism. Our results not only provided novel evidence for the hepatotoxicity and underlying mechanism of DBDPE but also were indicative of subsequent ecological and health risk assessment.

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Genome-wide DNA methylation of the liver reveals delayed effects of early-life exposure to 17-α-ethinylestradiol in the self-fertilizing mangrove rivulus

Cited by 7 publications

References 101 publications

Embryonic heat conditioning in chicks induces transgenerational heat/immunological resilience via methylation on regulatory elements

Embryonic heat conditioning in chicks induces transgenerational heat/immunological resilience via methylation on regulatory elements

Population Epigenetics: The Extent of DNA Methylation Variation in Wild Animal Populations

Evidence for Adverse Effects on Liver Development and Regeneration in Zebrafish by Decabromodiphenyl Ethane

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