Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition

John Arne Dahl; Inkyung Jung; Håvard Aanes; Gareth D Greggains; Adeel Manaf; Mads Lerdrup; Guoqiang Li; Samantha Kuan; Bin Li; Ah Young Lee; Sebastian Preissl; Ingunn Jermstad; Mads Haugland Haugen; Rajikala Suganthan; Magnar Bjørås; Klaus Hansen; Knut Tomas Dalen; Peter Fedorcsak; Bing Ren; Arne Klungland

doi:10.1038/nature19360

Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition

John Arne Dahl, Inkyung Jung, Håvard Aanes, Gareth D Greggains, Adeel Manaf, Mads Lerdrup, Guoqiang Li, Samantha Kuan, Bin Li, Ah Young Lee, Sebastian Preissl, Ingunn Jermstad, Mads Haugland Haugen, Rajikala Suganthan, Magnar Bjørås, Klaus Hansen, Knut Tomas Dalen, Peter Fedorcsak, Bing Ren, Arne Klungland

231 Citationer (Scopus)

Abstract

Maternal-to-zygotic transition (MZT) is essential for the formation of a new individual, but is still poorly understood despite recent progress in analysis of gene expression and DNA methylation in early embryogenesis. Dynamic histone modifications may have important roles in MZT, but direct measurements of chromatin states have been hindered by technical difficulties in profiling histone modifications from small quantities of cells. Recent improvements allow for 500 cell-equivalents of chromatin per reaction, but require 10,000 cells for initial steps or require a highly specialized microfluidics device that is not readily available. We developed a micro-scale chromatin immunoprecipitation and sequencing (μChIP-seq) method, which we used to profile genome-wide histone H3 lysine methylation (H3K4me3) and acetylation (H3K27ac) in mouse immature and metaphase II oocytes and in 2-cell and 8-cell embryos. Notably, we show that ~22% of the oocyte genome is associated with broad H3K4me3 domains that are anti-correlated with DNA methylation. The H3K4me3 signal becomes confined to transcriptional-start-site regions in 2-cell embryos, concomitant with the onset of major zygotic genome activation. Active removal of broad H3K4me3 domains by the lysine demethylases KDM5A and KDM5B is required for normal zygotic genome activation and is essential for early embryo development. Our results provide insight into the onset of the developmental program in mouse embryos and demonstrate a role for broad H3K4me3 domains in MZT.

Originalsprog	Engelsk
Tidsskrift	Nature
Vol/bind	537
Sider (fra-til)	548–552
ISSN	0028-0836
DOI	https://doi.org/10.1038/nature19360
Status	Udgivet - 14 sep. 2016

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10.1038/nature19360

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Dahl, J. A., Jung, I., Aanes, H., Greggains, G. D., Manaf, A., Lerdrup, M., Li, G., Kuan, S., Li, B., Lee, A. Y., Preissl, S., Jermstad, I., Haugen, M. H., Suganthan, R., Bjørås, M., Hansen, K., Dalen, K. T., Fedorcsak, P., Ren, B., & Klungland, A. (2016). Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature, 537, 548–552. https://doi.org/10.1038/nature19360

Dahl, JA, Jung, I, Aanes, H, Greggains, GD, Manaf, A, Lerdrup, M, Li, G, Kuan, S, Li, B, Lee, AY, Preissl, S, Jermstad, I, Haugen, MH, Suganthan, R, Bjørås, M, Hansen, K, Dalen, KT, Fedorcsak, P, Ren, B & Klungland, A 2016, 'Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition', Nature, bind 537, s. 548–552. https://doi.org/10.1038/nature19360

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title = "Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition",

abstract = "Maternal-to-zygotic transition (MZT) is essential for the formation of a new individual, but is still poorly understood despite recent progress in analysis of gene expression and DNA methylation in early embryogenesis. Dynamic histone modifications may have important roles in MZT, but direct measurements of chromatin states have been hindered by technical difficulties in profiling histone modifications from small quantities of cells. Recent improvements allow for 500 cell-equivalents of chromatin per reaction, but require 10,000 cells for initial steps or require a highly specialized microfluidics device that is not readily available. We developed a micro-scale chromatin immunoprecipitation and sequencing (μChIP-seq) method, which we used to profile genome-wide histone H3 lysine methylation (H3K4me3) and acetylation (H3K27ac) in mouse immature and metaphase II oocytes and in 2-cell and 8-cell embryos. Notably, we show that ~22% of the oocyte genome is associated with broad H3K4me3 domains that are anti-correlated with DNA methylation. The H3K4me3 signal becomes confined to transcriptional-start-site regions in 2-cell embryos, concomitant with the onset of major zygotic genome activation. Active removal of broad H3K4me3 domains by the lysine demethylases KDM5A and KDM5B is required for normal zygotic genome activation and is essential for early embryo development. Our results provide insight into the onset of the developmental program in mouse embryos and demonstrate a role for broad H3K4me3 domains in MZT.",

author = "Dahl, {John Arne} and Inkyung Jung and H{\aa}vard Aanes and Greggains, {Gareth D} and Adeel Manaf and Mads Lerdrup and Guoqiang Li and Samantha Kuan and Bin Li and Lee, {Ah Young} and Sebastian Preissl and Ingunn Jermstad and Haugen, {Mads Haugland} and Rajikala Suganthan and Magnar Bj{\o}r{\aa}s and Klaus Hansen and Dalen, {Knut Tomas} and Peter Fedorcsak and Bing Ren and Arne Klungland",

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doi = "10.1038/nature19360",

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T1 - Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition

AU - Dahl, John Arne

AU - Jung, Inkyung

AU - Aanes, Håvard

AU - Greggains, Gareth D

AU - Manaf, Adeel

AU - Lerdrup, Mads

AU - Li, Guoqiang

AU - Kuan, Samantha

AU - Li, Bin

AU - Lee, Ah Young

AU - Preissl, Sebastian

AU - Jermstad, Ingunn

AU - Haugen, Mads Haugland

AU - Suganthan, Rajikala

AU - Bjørås, Magnar

AU - Hansen, Klaus

AU - Dalen, Knut Tomas

AU - Fedorcsak, Peter

AU - Ren, Bing

AU - Klungland, Arne

PY - 2016/9/14

Y1 - 2016/9/14

N2 - Maternal-to-zygotic transition (MZT) is essential for the formation of a new individual, but is still poorly understood despite recent progress in analysis of gene expression and DNA methylation in early embryogenesis. Dynamic histone modifications may have important roles in MZT, but direct measurements of chromatin states have been hindered by technical difficulties in profiling histone modifications from small quantities of cells. Recent improvements allow for 500 cell-equivalents of chromatin per reaction, but require 10,000 cells for initial steps or require a highly specialized microfluidics device that is not readily available. We developed a micro-scale chromatin immunoprecipitation and sequencing (μChIP-seq) method, which we used to profile genome-wide histone H3 lysine methylation (H3K4me3) and acetylation (H3K27ac) in mouse immature and metaphase II oocytes and in 2-cell and 8-cell embryos. Notably, we show that ~22% of the oocyte genome is associated with broad H3K4me3 domains that are anti-correlated with DNA methylation. The H3K4me3 signal becomes confined to transcriptional-start-site regions in 2-cell embryos, concomitant with the onset of major zygotic genome activation. Active removal of broad H3K4me3 domains by the lysine demethylases KDM5A and KDM5B is required for normal zygotic genome activation and is essential for early embryo development. Our results provide insight into the onset of the developmental program in mouse embryos and demonstrate a role for broad H3K4me3 domains in MZT.

AB - Maternal-to-zygotic transition (MZT) is essential for the formation of a new individual, but is still poorly understood despite recent progress in analysis of gene expression and DNA methylation in early embryogenesis. Dynamic histone modifications may have important roles in MZT, but direct measurements of chromatin states have been hindered by technical difficulties in profiling histone modifications from small quantities of cells. Recent improvements allow for 500 cell-equivalents of chromatin per reaction, but require 10,000 cells for initial steps or require a highly specialized microfluidics device that is not readily available. We developed a micro-scale chromatin immunoprecipitation and sequencing (μChIP-seq) method, which we used to profile genome-wide histone H3 lysine methylation (H3K4me3) and acetylation (H3K27ac) in mouse immature and metaphase II oocytes and in 2-cell and 8-cell embryos. Notably, we show that ~22% of the oocyte genome is associated with broad H3K4me3 domains that are anti-correlated with DNA methylation. The H3K4me3 signal becomes confined to transcriptional-start-site regions in 2-cell embryos, concomitant with the onset of major zygotic genome activation. Active removal of broad H3K4me3 domains by the lysine demethylases KDM5A and KDM5B is required for normal zygotic genome activation and is essential for early embryo development. Our results provide insight into the onset of the developmental program in mouse embryos and demonstrate a role for broad H3K4me3 domains in MZT.

U2 - 10.1038/nature19360

DO - 10.1038/nature19360

M3 - Letter

C2 - 27626377

SN - 0028-0836

VL - 537

SP - 548

EP - 552

JO - Nature

JF - Nature

ER -

Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition

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