Symmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei

Abstract Paternal genome reprogramming, such as protamine–histone exchange and global DNA demethylation, is crucial for the development of fertilised embryos. Previously, our study showed that one of histone arginine methylation, asymmetrically dimethylated histone H3R17 (H3R17me2a), is necessary fo...

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Autores principales: Kohtaro Morita, Yuki Hatanaka, Shunya Ihashi, Masahide Asano, Kei Miyamoto, Kazuya Matsumoto
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:fcf3c10f47fa40f084b91b050f1310a62021-12-02T15:55:04ZSymmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei10.1038/s41598-021-89334-w2045-2322https://doaj.org/article/fcf3c10f47fa40f084b91b050f1310a62021-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-89334-whttps://doaj.org/toc/2045-2322Abstract Paternal genome reprogramming, such as protamine–histone exchange and global DNA demethylation, is crucial for the development of fertilised embryos. Previously, our study showed that one of histone arginine methylation, asymmetrically dimethylated histone H3R17 (H3R17me2a), is necessary for epigenetic reprogramming in the mouse paternal genome. However, roles of histone arginine methylation in reprogramming after fertilisation are still poorly understood. Here, we report that H3R2me2s promotes global transcription at the 1-cell stage, referred to as minor zygotic genome activation (ZGA). The inhibition of H3R2me2s by expressing a histone H3.3 mutant H3.3R2A prevented embryonic development from the 2-cell to 4-cell stages and significantly reduced global RNA synthesis and RNA polymerase II (Pol II) activity. Consistent with this result, the expression levels of MuERV-L as minor ZGA transcripts were decreased by forced expression of H3.3R2A. Furthermore, treatment with an inhibitor and co-injection of siRNA to PRMT5 and PRMT7 also resulted in the attenuation of transcriptional activities with reduction of H3R2me2s in the pronuclei of zygotes. Interestingly, impairment of H3K4 methylation by expression of H3.3K4M resulted in a decrease of H3R2me2s in male pronuclei. Our findings suggest that H3R2me2s together with H3K4 methylation is involved in global transcription during minor ZGA in mice.Kohtaro MoritaYuki HatanakaShunya IhashiMasahide AsanoKei MiyamotoKazuya MatsumotoNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-14 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Kohtaro Morita
Yuki Hatanaka
Shunya Ihashi
Masahide Asano
Kei Miyamoto
Kazuya Matsumoto
Symmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei
description Abstract Paternal genome reprogramming, such as protamine–histone exchange and global DNA demethylation, is crucial for the development of fertilised embryos. Previously, our study showed that one of histone arginine methylation, asymmetrically dimethylated histone H3R17 (H3R17me2a), is necessary for epigenetic reprogramming in the mouse paternal genome. However, roles of histone arginine methylation in reprogramming after fertilisation are still poorly understood. Here, we report that H3R2me2s promotes global transcription at the 1-cell stage, referred to as minor zygotic genome activation (ZGA). The inhibition of H3R2me2s by expressing a histone H3.3 mutant H3.3R2A prevented embryonic development from the 2-cell to 4-cell stages and significantly reduced global RNA synthesis and RNA polymerase II (Pol II) activity. Consistent with this result, the expression levels of MuERV-L as minor ZGA transcripts were decreased by forced expression of H3.3R2A. Furthermore, treatment with an inhibitor and co-injection of siRNA to PRMT5 and PRMT7 also resulted in the attenuation of transcriptional activities with reduction of H3R2me2s in the pronuclei of zygotes. Interestingly, impairment of H3K4 methylation by expression of H3.3K4M resulted in a decrease of H3R2me2s in male pronuclei. Our findings suggest that H3R2me2s together with H3K4 methylation is involved in global transcription during minor ZGA in mice.
format article
author Kohtaro Morita
Yuki Hatanaka
Shunya Ihashi
Masahide Asano
Kei Miyamoto
Kazuya Matsumoto
author_facet Kohtaro Morita
Yuki Hatanaka
Shunya Ihashi
Masahide Asano
Kei Miyamoto
Kazuya Matsumoto
author_sort Kohtaro Morita
title Symmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei
title_short Symmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei
title_full Symmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei
title_fullStr Symmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei
title_full_unstemmed Symmetrically dimethylated histone H3R2 promotes global transcription during minor zygotic genome activation in mouse pronuclei
title_sort symmetrically dimethylated histone h3r2 promotes global transcription during minor zygotic genome activation in mouse pronuclei
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/fcf3c10f47fa40f084b91b050f1310a6
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AT yukihatanaka symmetricallydimethylatedhistoneh3r2promotesglobaltranscriptionduringminorzygoticgenomeactivationinmousepronuclei
AT shunyaihashi symmetricallydimethylatedhistoneh3r2promotesglobaltranscriptionduringminorzygoticgenomeactivationinmousepronuclei
AT masahideasano symmetricallydimethylatedhistoneh3r2promotesglobaltranscriptionduringminorzygoticgenomeactivationinmousepronuclei
AT keimiyamoto symmetricallydimethylatedhistoneh3r2promotesglobaltranscriptionduringminorzygoticgenomeactivationinmousepronuclei
AT kazuyamatsumoto symmetricallydimethylatedhistoneh3r2promotesglobaltranscriptionduringminorzygoticgenomeactivationinmousepronuclei
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