A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.

Forming an embryo from a zygote poses an apparent conflict for epigenetic regulation. On the one hand, the de novo induction of cell fate identities requires the establishment and subsequent maintenance of epigenetic information to harness developmental gene expression. On the other hand, the embryo...

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Autores principales:	Daniil Pokrovsky, Ignasi Forné, Tobias Straub, Axel Imhof, Ralph A W Rupp
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/fb46f09e89a54444ba25fcaa7b86a912
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spelling	oai:doaj.org-article:fb46f09e89a54444ba25fcaa7b86a9122021-12-02T19:54:37ZA systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.1544-91731545-788510.1371/journal.pbio.3001377https://doaj.org/article/fb46f09e89a54444ba25fcaa7b86a9122021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001377https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Forming an embryo from a zygote poses an apparent conflict for epigenetic regulation. On the one hand, the de novo induction of cell fate identities requires the establishment and subsequent maintenance of epigenetic information to harness developmental gene expression. On the other hand, the embryo depends on cell proliferation, and every round of DNA replication dilutes preexisting histone modifications by incorporation of new unmodified histones into chromatin. Here, we investigated the possible relationship between the propagation of epigenetic information and the developmental cell proliferation during Xenopus embryogenesis. We systemically inhibited cell proliferation during the G1/S transition in gastrula embryos and followed their development until the tadpole stage. Comparing wild-type and cell cycle-arrested embryos, we show that the inhibition of cell proliferation is principally compatible with embryo survival and cellular differentiation. In parallel, we quantified by mass spectrometry the abundance of a large set of histone modification states, which reflects the developmental maturation of the embryonic epigenome. The arrested embryos developed abnormal stage-specific histone modification profiles (HMPs), in which transcriptionally repressive histone marks were overrepresented. Embryos released from the cell cycle block during neurulation reverted toward normality on morphological, molecular, and epigenetic levels. These results suggest that the cell cycle block by HUA alters stage-specific HMPs. We propose that this influence is strong enough to control developmental decisions, specifically in cell populations that switch between resting and proliferating states such as stem cells.Daniil PokrovskyIgnasi FornéTobias StraubAxel ImhofRalph A W RuppPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 9, p e3001377 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Daniil Pokrovsky Ignasi Forné Tobias Straub Axel Imhof Ralph A W Rupp A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.
description	Forming an embryo from a zygote poses an apparent conflict for epigenetic regulation. On the one hand, the de novo induction of cell fate identities requires the establishment and subsequent maintenance of epigenetic information to harness developmental gene expression. On the other hand, the embryo depends on cell proliferation, and every round of DNA replication dilutes preexisting histone modifications by incorporation of new unmodified histones into chromatin. Here, we investigated the possible relationship between the propagation of epigenetic information and the developmental cell proliferation during Xenopus embryogenesis. We systemically inhibited cell proliferation during the G1/S transition in gastrula embryos and followed their development until the tadpole stage. Comparing wild-type and cell cycle-arrested embryos, we show that the inhibition of cell proliferation is principally compatible with embryo survival and cellular differentiation. In parallel, we quantified by mass spectrometry the abundance of a large set of histone modification states, which reflects the developmental maturation of the embryonic epigenome. The arrested embryos developed abnormal stage-specific histone modification profiles (HMPs), in which transcriptionally repressive histone marks were overrepresented. Embryos released from the cell cycle block during neurulation reverted toward normality on morphological, molecular, and epigenetic levels. These results suggest that the cell cycle block by HUA alters stage-specific HMPs. We propose that this influence is strong enough to control developmental decisions, specifically in cell populations that switch between resting and proliferating states such as stem cells.
format	article
author	Daniil Pokrovsky Ignasi Forné Tobias Straub Axel Imhof Ralph A W Rupp
author_facet	Daniil Pokrovsky Ignasi Forné Tobias Straub Axel Imhof Ralph A W Rupp
author_sort	Daniil Pokrovsky
title	A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.
title_short	A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.
title_full	A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.
title_fullStr	A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.
title_full_unstemmed	A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.
title_sort	systemic cell cycle block impacts stage-specific histone modification profiles during xenopus embryogenesis.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/fb46f09e89a54444ba25fcaa7b86a912
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A systemic cell cycle block impacts stage-specific histone modification profiles during Xenopus embryogenesis.

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