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

Author

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  • Qian-Qian Sha

    (Zhejiang University)

  • Xing-Xing Dai

    (Zhejiang University)

  • Jun-Chao Jiang

    (Zhejiang University)

  • Chao Yu

    (Zhejiang University)

  • Yu Jiang

    (Zhejiang University)

  • Junping Liu

    (Hangzhou Normal University)

  • Xiang-Hong Ou

    (Guangdong Second Provincial General Hospital)

  • Song-Ying Zhang

    (Zhejiang University, Key Laboratory of Reproductive Dysfunction Management of Zhejiang Province)

  • Heng-Yu Fan

    (Zhejiang University
    Zhejiang University, Key Laboratory of Reproductive Dysfunction Management of Zhejiang Province)

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.

Suggested Citation

  • Qian-Qian Sha & Xing-Xing Dai & Jun-Chao Jiang & Chao Yu & Yu Jiang & Junping Liu & Xiang-Hong Ou & Song-Ying Zhang & Heng-Yu Fan, 2018. "CFP1 coordinates histone H3 lysine-4 trimethylation and meiotic cell cycle progression in mouse oocytes," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-05930-x
    DOI: 10.1038/s41467-018-05930-x
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    Cited by:

    1. Seung Chel Yang & Mira Park & Kwon-Ho Hong & Hyeonwoo La & Chanhyeok Park & Peike Wang & Gaizhen Li & Qionghua Chen & Youngsok Choi & Francesco J. DeMayo & John P. Lydon & David G. Skalnik & Hyunjung , 2023. "CFP1 governs uterine epigenetic landscapes to intervene in progesterone responses for uterine physiology and suppression of endometriosis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Yun-Wen Wu & Sen Li & Wei Zheng & Yan-Chu Li & Lu Chen & Yong Zhou & Zuo-Qi Deng & Ge Lin & Heng-Yu Fan & Qian-Qian Sha, 2022. "Dynamic mRNA degradome analyses indicate a role of histone H3K4 trimethylation in association with meiosis-coupled mRNA decay in oocyte aging," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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