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MARTRE family proteins negatively regulate CCR4-NOT activity to protect poly(A) tail length and promote translation of maternal mRNA

Author

Listed:
  • Jing Yang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Jiachen Bu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Bowen Liu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Yusheng Liu

    (Chinese Academy of Sciences
    Northeast Forestry University)

  • Zhuqiang Zhang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Ziyi Li

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Falong Lu

    (University of Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Bing Zhu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Yingfeng Li

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

Abstract

The mammalian early embryo development requires translation of maternal mRNA inherited from the oocyte. While poly(A) tail length influences mRNA translation efficiency during the oocyte-to-embryo transition (OET), molecular mechanisms regulating maternal RNA poly(A) tail length are not fully understood. In this study, we identified MARTRE, a previously uncharacterized protein family (MARTRE1-MARTRE6), as regulators expressed during mouse OET that modulate poly(A) tail length. MARTRE inhibits deadenylation through the direct interaction with the deadenylase CCR4-NOT, and ectopic expression of Martre stabilized mRNA by attenuating poly(A) tail shortening. Deletion of the Martre gene locus results in shortened poly(A) tails and decreased translation efficiency of actively translated mRNAs in mouse zygotes, but does not affect maternal mRNA decay. MARTRE proteins thus fine-tune maternal mRNA translation by negatively regulating the deadenylating activity of CCR4-NOT. Moreover, Martre knockout embryos show delayed 2-cell stage progression and compromised preimplantation development. Together, our findings highlight protection of long poly(A) tails from active deadenylation as an important mechanism to coordinate translation of maternal mRNA.

Suggested Citation

  • Jing Yang & Jiachen Bu & Bowen Liu & Yusheng Liu & Zhuqiang Zhang & Ziyi Li & Falong Lu & Bing Zhu & Yingfeng Li, 2025. "MARTRE family proteins negatively regulate CCR4-NOT activity to protect poly(A) tail length and promote translation of maternal mRNA," Nature Communications, Nature, vol. 16(1), pages 1-23, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-024-55610-2
    DOI: 10.1038/s41467-024-55610-2
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    2. Yusheng Liu & Hu Nie & Hongxiang Liu & Falong Lu, 2019. "Poly(A) inclusive RNA isoform sequencing (PAIso−seq) reveals wide-spread non-adenosine residues within RNA poly(A) tails," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Jingyi Wu & Bo Huang & He Chen & Qiangzong Yin & Yang Liu & Yunlong Xiang & Bingjie Zhang & Bofeng Liu & Qiujun Wang & Weikun Xia & Wenzhi Li & Yuanyuan Li & Jing Ma & Xu Peng & Hui Zheng & Jia Ming &, 2016. "The landscape of accessible chromatin in mammalian preimplantation embryos," Nature, Nature, vol. 534(7609), pages 652-657, June.
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