Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes

Abstract L-ascorbic acid (Vitamin C) can enhance the meiotic maturation and developmental competence of porcine oocytes, but the underlying molecular mechanism remains obscure. Here we show the role of ascorbic acid in regulating epigenetic status of both nucleic acids and chromatin to promote oocyt...

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Autores principales: Xiao-Xia Yu, Yun-Hua Liu, Xiao-Man Liu, Pei-Chao Wang, Shuai Liu, Jia-Kun Miao, Zhi-Qiang Du, Cai-Xia Yang
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Publicado: Nature Portfolio 2018
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Acceso en línea:https://doaj.org/article/9c6bcaaac00a46d1b2edd0ae9f7c5c51
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spelling oai:doaj.org-article:9c6bcaaac00a46d1b2edd0ae9f7c5c512021-12-02T15:08:25ZAscorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes10.1038/s41598-018-24395-y2045-2322https://doaj.org/article/9c6bcaaac00a46d1b2edd0ae9f7c5c512018-04-01T00:00:00Zhttps://doi.org/10.1038/s41598-018-24395-yhttps://doaj.org/toc/2045-2322Abstract L-ascorbic acid (Vitamin C) can enhance the meiotic maturation and developmental competence of porcine oocytes, but the underlying molecular mechanism remains obscure. Here we show the role of ascorbic acid in regulating epigenetic status of both nucleic acids and chromatin to promote oocyte maturation and development in pigs. Supplementation of 250 μM L-ascorbic acid 2-phosphate sesquimagnesium salt hydrate (AA2P) during in vitro maturation significantly enhanced the nuclear maturation (as indicated by higher rate of first polar body extrusion and increased Bmp15 mRNA level), reduced level of reactive oxygen species, and promoted developmental potency (higher cleavage and blastocyst rates of parthenotes, and decreased Bax and Caspase3 mRNA levels in blastocysts) of pig oocytes. AA2P treatment caused methylation erasure in mature oocytes on nucleic acids (5-methylcytosine (5 mC) and N 6 -methyladenosine (m6A)) and histones (Histone H3 trimethylations at lysines 27, H3K27me3), but establishment of histone H3 trimethylations at lysines 4 (H3K4me3) and 36 (H3K36me3). During the global methylation reprogramming process, levels of TET2 (mRNA and protein) and Dnmt3b (mRNA) were significantly elevated, but simultaneously DNMT3A (mRNA and protein), and also Hif-1α, Hif-2α, Tet3, Mettl14, Kdm5b and Eed (mRNA) were significantly inhibited. Our findings support that ascorbic acid can reprogram the methylation status of not only DNA and histone, but also RNA, to improve pig oocyte maturation and developmental competence.Xiao-Xia YuYun-Hua LiuXiao-Man LiuPei-Chao WangShuai LiuJia-Kun MiaoZhi-Qiang DuCai-Xia YangNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 8, Iss 1, Pp 1-12 (2018)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Xiao-Xia Yu
Yun-Hua Liu
Xiao-Man Liu
Pei-Chao Wang
Shuai Liu
Jia-Kun Miao
Zhi-Qiang Du
Cai-Xia Yang
Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes
description Abstract L-ascorbic acid (Vitamin C) can enhance the meiotic maturation and developmental competence of porcine oocytes, but the underlying molecular mechanism remains obscure. Here we show the role of ascorbic acid in regulating epigenetic status of both nucleic acids and chromatin to promote oocyte maturation and development in pigs. Supplementation of 250 μM L-ascorbic acid 2-phosphate sesquimagnesium salt hydrate (AA2P) during in vitro maturation significantly enhanced the nuclear maturation (as indicated by higher rate of first polar body extrusion and increased Bmp15 mRNA level), reduced level of reactive oxygen species, and promoted developmental potency (higher cleavage and blastocyst rates of parthenotes, and decreased Bax and Caspase3 mRNA levels in blastocysts) of pig oocytes. AA2P treatment caused methylation erasure in mature oocytes on nucleic acids (5-methylcytosine (5 mC) and N 6 -methyladenosine (m6A)) and histones (Histone H3 trimethylations at lysines 27, H3K27me3), but establishment of histone H3 trimethylations at lysines 4 (H3K4me3) and 36 (H3K36me3). During the global methylation reprogramming process, levels of TET2 (mRNA and protein) and Dnmt3b (mRNA) were significantly elevated, but simultaneously DNMT3A (mRNA and protein), and also Hif-1α, Hif-2α, Tet3, Mettl14, Kdm5b and Eed (mRNA) were significantly inhibited. Our findings support that ascorbic acid can reprogram the methylation status of not only DNA and histone, but also RNA, to improve pig oocyte maturation and developmental competence.
format article
author Xiao-Xia Yu
Yun-Hua Liu
Xiao-Man Liu
Pei-Chao Wang
Shuai Liu
Jia-Kun Miao
Zhi-Qiang Du
Cai-Xia Yang
author_facet Xiao-Xia Yu
Yun-Hua Liu
Xiao-Man Liu
Pei-Chao Wang
Shuai Liu
Jia-Kun Miao
Zhi-Qiang Du
Cai-Xia Yang
author_sort Xiao-Xia Yu
title Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes
title_short Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes
title_full Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes
title_fullStr Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes
title_full_unstemmed Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes
title_sort ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes
publisher Nature Portfolio
publishDate 2018
url https://doaj.org/article/9c6bcaaac00a46d1b2edd0ae9f7c5c51
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