CFP1 coordinates histone H3 lysine-4 trimethylation and meiotic cell cycle progression in mouse oocytes

Nature Communications
Qian-Qian ShaHeng-Yu Fan

Abstract

Trimethylation of histone H3 on lysine-4 (H3K4me3) is associated with gene-regulatory elements, but its transcription-independent function in cell division is unclear. CxxC-finger protein-1 (CFP1) is a major mediator of H3K4 trimethylation in mouse oocytes. Here we report that oocyte-specific knockout of Cxxc1, inhibition of CFP1 function, or abrogation of H3K4 methylation in oocytes each causes a delay of meiotic resumption as well as metaphase I arrest owing to defective spindle assembly and chromosome misalignment. These phenomena are partially attributed to insufficient phosphorylation of histone H3 at threonine-3. CDK1 triggers cell division-coupled degradation and inhibitory phosphorylation of CFP1. Preventing CFP1 degradation and phosphorylation causes CFP1 accumulation on chromosomes and impairs meiotic maturation and preimplantation embryo development. Therefore, CFP1-mediated H3K4 trimethylation provides 3a permission signal for the G2-M transition. Dual inhibition of CFP1 removes the SETD1-CFP1 complex from chromatin and ensures appropriate chromosome configuration changes during meiosis and mitosis.

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Citations

Oct 20, 2018·Nucleic Acids Research·Xing-Xing DaiHeng-Yu Fan
Jan 11, 2020·Genes & Development·Chunxia ZhangYi Zhang
Sep 10, 2019·Cancer Cell International·Jingyue SunShuang Liu
Sep 8, 2019·Cellular and Molecular Life Sciences : CMLS·Jue ZhangHeng-Yu Fan
Mar 28, 2020·Molecular Reproduction and Development·Qian ZhouQing-Yuan Sun
Sep 12, 2020·Cells·Marion HerbetteFrancesca Palladino
Jan 13, 2021·The Journal of Experimental Medicine·Masahiro KiuchiToshinori Nakayama
Feb 24, 2021·Nucleic Acids Research·Qian-Qian ShaHeng-Yu Fan
Apr 13, 2021·Frontiers in Cell and Developmental Biology·Meina HeChao Wang
May 1, 2021·Biology of Reproduction·Millissia Ben MaamarMichael K Skinner
Jul 29, 2021·FASEB Journal : Official Publication of the Federation of American Societies for Experimental Biology·Yidai YangJean-Francois Couture

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Methods Mentioned

BETA
gene knockout
in vitro transcription
electrophoresis
transfection
immunoprecipitation
co-immunoprecipitation
co-IP
nuclear magnetic resonance
PCR

Software Mentioned

- J
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