Dataset Information

Regulation of Polycomb Repression by O-GlcNAcylation: Linking Nutrition to Epigenetic Reprogramming in Embryonic Development and Cancer.

ABSTRACT: Epigenetic modifications are major actors of early embryogenesis and carcinogenesis and are sensitive to nutritional environment. In recent years, the nutritional sensor O-GlcNAcylation has been recognized as a key regulator of chromatin remodeling. In this review, we summarize and discuss recent clues that OGT and O-GlcNAcylation intimately regulate the functions of the Polycomb group proteins at different levels especially during Drosophila melanogaster embryonic development and in human cancer cell lines. These observations define an additional connection between nutrition and epigenetic reprogramming associated to embryonic development and cancer.

SUBMITTER: Decourcelle A

PROVIDER: S-EPMC6400832 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Publications

Regulation of Polycomb Repression by O-GlcNAcylation: Linking Nutrition to Epigenetic Reprogramming in Embryonic Development and Cancer.

Decourcelle Amélie A Leprince Dominique D Dehennaut Vanessa V

Frontiers in endocrinology 20190227

Epigenetic modifications are major actors of early embryogenesis and carcinogenesis and are sensitive to nutritional environment. In recent years, the nutritional sensor O-GlcNAcylation has been recognized as a key regulator of chromatin remodeling. In this review, we summarize and discuss recent clues that OGT and O-GlcNAcylation intimately regulate the functions of the Polycomb group proteins at different levels especially during Drosophila melanogaster embryonic developme ...[more]

PMID: 30873122

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Project description:BackgroundReactive oxygen species (ROS)-induced oxidative stress is well known to play a major role in male infertility. Sperm are sensitive to ROS damaging effects because as male germ cells form mature sperm they progressively lose the ability to repair DNA damage. However, how oxidative DNA lesions in sperm affect early embryonic development remains elusive.ResultsUsing cattle as model, we show that fertilization using sperm exposed to oxidative stress caused a major developmental arrest at the time of embryonic genome activation. The levels of DNA damage response did not directly correlate with the degree of developmental defects. The early cellular response for DNA damage, γH2AX, is already present at high levels in zygotes that progress normally in development and did not significantly increase at the paternal genome containing oxidative DNA lesions. Moreover, XRCC1, a factor implicated in the last step of base excision repair (BER) pathway, was recruited to the damaged paternal genome, indicating that the maternal BER machinery can repair these DNA lesions induced in sperm. Remarkably, the paternal genome with oxidative DNA lesions showed an impairment of zygotic active DNA demethylation, a process that previous studies linked to BER. Quantitative immunofluorescence analysis and ultrasensitive LC-MS-based measurements revealed that oxidative DNA lesions in sperm impair active DNA demethylation at paternal pronuclei, without affecting 5-hydroxymethylcytosine (5hmC), a 5-methylcytosine modification that has been implicated in paternal active DNA demethylation in mouse zygotes. Thus, other 5hmC-independent processes are implicated in active DNA demethylation in bovine embryos. The recruitment of XRCC1 to damaged paternal pronuclei indicates that oxidative DNA lesions drive BER to repair DNA at the expense of DNA demethylation. Finally, this study highlighted striking differences in DNA methylation dynamics between bovine and mouse zygotes that will facilitate the understanding of the dynamics of DNA methylation in early development.ConclusionsThe data demonstrate that oxidative stress in sperm has an impact not only on DNA integrity but also on the dynamics of epigenetic reprogramming, which may harm the paternal genetic and epigenetic contribution to the developing embryo and affect embryo development and embryo quality.

Dataset Information

Regulation of Polycomb Repression by O-GlcNAcylation: Linking Nutrition to Epigenetic Reprogramming in Embryonic Development and Cancer.

Publications

Regulation of Polycomb Repression by <i>O</i>-GlcNAcylation: Linking Nutrition to Epigenetic Reprogramming in Embryonic Development and Cancer.

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