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Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation

Genomic imprinting, parent-of-origin-specific gene expression, is controlled by differential epigenetic status of the parental chromosomes. While DNA methylation and suppressive histone modifications established during gametogenesis suppress imprinted genes on the inactive allele, how and when the e...

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Autores principales: Ishihara, Teruhito, Griffith, Oliver W., Suzuki, Shunsuke, Renfree, Marilyn B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8960379/
https://www.ncbi.nlm.nih.gov/pubmed/35359448
http://dx.doi.org/10.3389/fcell.2022.838684
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author Ishihara, Teruhito
Griffith, Oliver W.
Suzuki, Shunsuke
Renfree, Marilyn B.
author_facet Ishihara, Teruhito
Griffith, Oliver W.
Suzuki, Shunsuke
Renfree, Marilyn B.
author_sort Ishihara, Teruhito
collection PubMed
description Genomic imprinting, parent-of-origin-specific gene expression, is controlled by differential epigenetic status of the parental chromosomes. While DNA methylation and suppressive histone modifications established during gametogenesis suppress imprinted genes on the inactive allele, how and when the expressed allele gains its active status is not clear. In this study, we asked whether the active histone-3 lysine-4 trimethylation (H3K4me3) marks remain at paternally expressed genes (PEGs) in sperm and embryos before and after fertilization using published data. Here we show that mouse sperm had the active H3K4me3 at more than half of known PEGs, and these genes were present even after fertilization. Using reciprocal cross data, we identified 13 new transient PEGs during zygotic genome activation. Next, we confirmed that the 12 out of the 13 new transient PEGs were associated with the paternal H3K4me3 in sperm. Nine out of the 12 genes were associated with the paternal H3K4me3 in zygotes. Our results show that paternal H3K4me3 marks escape inactivation during the histone-to-protamine transition that occurs during sperm maturation and are present in embryos from early zygotic stages up to implantation.
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spelling pubmed-89603792022-03-30 Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation Ishihara, Teruhito Griffith, Oliver W. Suzuki, Shunsuke Renfree, Marilyn B. Front Cell Dev Biol Cell and Developmental Biology Genomic imprinting, parent-of-origin-specific gene expression, is controlled by differential epigenetic status of the parental chromosomes. While DNA methylation and suppressive histone modifications established during gametogenesis suppress imprinted genes on the inactive allele, how and when the expressed allele gains its active status is not clear. In this study, we asked whether the active histone-3 lysine-4 trimethylation (H3K4me3) marks remain at paternally expressed genes (PEGs) in sperm and embryos before and after fertilization using published data. Here we show that mouse sperm had the active H3K4me3 at more than half of known PEGs, and these genes were present even after fertilization. Using reciprocal cross data, we identified 13 new transient PEGs during zygotic genome activation. Next, we confirmed that the 12 out of the 13 new transient PEGs were associated with the paternal H3K4me3 in sperm. Nine out of the 12 genes were associated with the paternal H3K4me3 in zygotes. Our results show that paternal H3K4me3 marks escape inactivation during the histone-to-protamine transition that occurs during sperm maturation and are present in embryos from early zygotic stages up to implantation. Frontiers Media S.A. 2022-03-10 /pmc/articles/PMC8960379/ /pubmed/35359448 http://dx.doi.org/10.3389/fcell.2022.838684 Text en Copyright © 2022 Ishihara, Griffith, Suzuki and Renfree. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Ishihara, Teruhito
Griffith, Oliver W.
Suzuki, Shunsuke
Renfree, Marilyn B.
Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation
title Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation
title_full Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation
title_fullStr Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation
title_full_unstemmed Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation
title_short Presence of H3K4me3 on Paternally Expressed Genes of the Paternal Genome From Sperm to Implantation
title_sort presence of h3k4me3 on paternally expressed genes of the paternal genome from sperm to implantation
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8960379/
https://www.ncbi.nlm.nih.gov/pubmed/35359448
http://dx.doi.org/10.3389/fcell.2022.838684
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