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Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos
Histone modifications are critical epigenetic indicators of chromatin state associated with gene expression. Although the reprogramming patterns of H3K4me3 and H3K27me3 have been elucidated in mouse and human preimplantation embryos, the relationship between these marks and zygotic genome activation...
Autores principales: | , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cold Spring Harbor Laboratory Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9435746/ https://www.ncbi.nlm.nih.gov/pubmed/35868641 http://dx.doi.org/10.1101/gr.276207.121 |
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author | Bu, Guowei Zhu, Wei Liu, Xin Zhang, Jingjing Yu, Longtao Zhou, Kai Wang, Shangke Li, Zhekun Fan, Zhengang Wang, Tingting Hu, Taotao Hu, Ruifeng Liu, Zhiting Wang, Tao Wu, Linhui Zhang, Xia Zhao, Shuhong Miao, Yi-Liang |
author_facet | Bu, Guowei Zhu, Wei Liu, Xin Zhang, Jingjing Yu, Longtao Zhou, Kai Wang, Shangke Li, Zhekun Fan, Zhengang Wang, Tingting Hu, Taotao Hu, Ruifeng Liu, Zhiting Wang, Tao Wu, Linhui Zhang, Xia Zhao, Shuhong Miao, Yi-Liang |
author_sort | Bu, Guowei |
collection | PubMed |
description | Histone modifications are critical epigenetic indicators of chromatin state associated with gene expression. Although the reprogramming patterns of H3K4me3 and H3K27me3 have been elucidated in mouse and human preimplantation embryos, the relationship between these marks and zygotic genome activation (ZGA) remains poorly understood. By ultra-low-input native chromatin immunoprecipitation and sequencing, we profiled global H3K4me3 and H3K27me3 in porcine oocytes and in vitro fertilized (IVF) embryos. We observed sharp H3K4me3 peaks in promoters of ZGA genes in oocytes, and these peaks became broader after fertilization and reshaped into sharp peaks again during ZGA. By simultaneous depletion of H3K4me3 demethylase KDM5B and KDM5C, we determined that broad H3K4me3 domain maintenance impaired ZGA gene expression, suggesting its function to prevent premature ZGA entry. In contrast, broad H3K27me3 domains underwent global removal upon fertilization, followed by a re-establishment for H3K4me3/H3K27me3 bivalency in morulae. We also found that bivalent marks were deposited at promoters of ZGA genes, and inhibiting this deposition was correlated with the activation of ZGA genes. It suggests that promoter bivalency contributes to ZGA exit in porcine embryos. Moreover, we demonstrated that aberrant reprogramming of H3K4me3 and H3K27me3 triggered ZGA dysregulation in somatic cell nuclear transfer (SCNT) embryos, whereas H3K27me3-mediated imprinting did not exist in porcine IVF and SCNT embryos. Our findings highlight two previously unknown epigenetic reprogramming modes coordinated with ZGA in porcine preimplantation embryos. Finally, the similarities observed between porcine and human histone modification dynamics suggest that the porcine embryo may also be a useful model for human embryo research. |
format | Online Article Text |
id | pubmed-9435746 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Cold Spring Harbor Laboratory Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-94357462023-02-01 Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos Bu, Guowei Zhu, Wei Liu, Xin Zhang, Jingjing Yu, Longtao Zhou, Kai Wang, Shangke Li, Zhekun Fan, Zhengang Wang, Tingting Hu, Taotao Hu, Ruifeng Liu, Zhiting Wang, Tao Wu, Linhui Zhang, Xia Zhao, Shuhong Miao, Yi-Liang Genome Res Research Histone modifications are critical epigenetic indicators of chromatin state associated with gene expression. Although the reprogramming patterns of H3K4me3 and H3K27me3 have been elucidated in mouse and human preimplantation embryos, the relationship between these marks and zygotic genome activation (ZGA) remains poorly understood. By ultra-low-input native chromatin immunoprecipitation and sequencing, we profiled global H3K4me3 and H3K27me3 in porcine oocytes and in vitro fertilized (IVF) embryos. We observed sharp H3K4me3 peaks in promoters of ZGA genes in oocytes, and these peaks became broader after fertilization and reshaped into sharp peaks again during ZGA. By simultaneous depletion of H3K4me3 demethylase KDM5B and KDM5C, we determined that broad H3K4me3 domain maintenance impaired ZGA gene expression, suggesting its function to prevent premature ZGA entry. In contrast, broad H3K27me3 domains underwent global removal upon fertilization, followed by a re-establishment for H3K4me3/H3K27me3 bivalency in morulae. We also found that bivalent marks were deposited at promoters of ZGA genes, and inhibiting this deposition was correlated with the activation of ZGA genes. It suggests that promoter bivalency contributes to ZGA exit in porcine embryos. Moreover, we demonstrated that aberrant reprogramming of H3K4me3 and H3K27me3 triggered ZGA dysregulation in somatic cell nuclear transfer (SCNT) embryos, whereas H3K27me3-mediated imprinting did not exist in porcine IVF and SCNT embryos. Our findings highlight two previously unknown epigenetic reprogramming modes coordinated with ZGA in porcine preimplantation embryos. Finally, the similarities observed between porcine and human histone modification dynamics suggest that the porcine embryo may also be a useful model for human embryo research. Cold Spring Harbor Laboratory Press 2022-08 /pmc/articles/PMC9435746/ /pubmed/35868641 http://dx.doi.org/10.1101/gr.276207.121 Text en © 2022 Bu et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by-nc/4.0/This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) . |
spellingShingle | Research Bu, Guowei Zhu, Wei Liu, Xin Zhang, Jingjing Yu, Longtao Zhou, Kai Wang, Shangke Li, Zhekun Fan, Zhengang Wang, Tingting Hu, Taotao Hu, Ruifeng Liu, Zhiting Wang, Tao Wu, Linhui Zhang, Xia Zhao, Shuhong Miao, Yi-Liang Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos |
title | Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos |
title_full | Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos |
title_fullStr | Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos |
title_full_unstemmed | Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos |
title_short | Coordination of zygotic genome activation entry and exit by H3K4me3 and H3K27me3 in porcine early embryos |
title_sort | coordination of zygotic genome activation entry and exit by h3k4me3 and h3k27me3 in porcine early embryos |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9435746/ https://www.ncbi.nlm.nih.gov/pubmed/35868641 http://dx.doi.org/10.1101/gr.276207.121 |
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