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CPEB1-dependent disruption of the mRNA translation program in oocytes during maternal aging

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  • Nozomi Takahashi

    (University of California
    University of California
    University of California)

  • Federica Franciosi

    (University of California
    University of California
    University of California
    Università degli Studi di Milano)

  • Enrico Maria Daldello

    (University of California
    University of California
    University of California
    Laboratoire de Biologie du Développement—Institut de Biologie Paris Seine, LBD-IBPS)

  • Xuan G. Luong

    (University of California
    University of California
    University of California)

  • Peter Althoff

    (University of California
    University of California
    University of California)

  • Xiaotian Wang

    (University of California
    University of California
    University of California)

  • Marco Conti

    (University of California
    University of California
    University of California)

Abstract

The molecular causes of deteriorating oocyte quality during aging are poorly defined. Since oocyte developmental competence relies on post-transcriptional regulations, we tested whether defective mRNA translation contributes to this decline in quality. Disruption in ribosome loading on maternal transcripts is present in old oocytes. Using a candidate approach, we detect altered translation of 3’-UTR-reporters and altered poly(A) length of the endogenous mRNAs. mRNA polyadenylation depends on the cytoplasmic polyadenylation binding protein 1 (CPEB1). Cpeb1 mRNA translation and protein levels are decreased in old oocytes. This decrease causes de-repression of Ccnb1 translation in quiescent oocytes, premature CDK1 activation, and accelerated reentry into meiosis. De-repression of Ccnb1 is corrected by Cpeb1 mRNA injection in old oocytes. Oocyte-specific Cpeb1 haploinsufficiency in young oocytes recapitulates all the translation phenotypes of old oocytes. These findings demonstrate that a dysfunction in the oocyte translation program is associated with the decline in oocyte quality during aging.

Suggested Citation

  • Nozomi Takahashi & Federica Franciosi & Enrico Maria Daldello & Xuan G. Luong & Peter Althoff & Xiaotian Wang & Marco Conti, 2023. "CPEB1-dependent disruption of the mRNA translation program in oocytes during maternal aging," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35994-3
    DOI: 10.1038/s41467-023-35994-3
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    1. Wenqi Hu & Haitao Zeng & Yanan Shi & Chuanchuan Zhou & Jiana Huang & Lei Jia & Siqi Xu & Xiaoyu Feng & Yanyan Zeng & Tuanlin Xiong & Wenze Huang & Peng Sun & Yajie Chang & Tingting Li & Cong Fang & Ke, 2022. "Single-cell transcriptome and translatome dual-omics reveals potential mechanisms of human oocyte maturation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Aldema Sas-Chen & Justin M. Thomas & Donna Matzov & Masato Taoka & Kellie D. Nance & Ronit Nir & Keri M. Bryson & Ran Shachar & Geraldy L. S. Liman & Brett W. Burkhart & Supuni Thalalla Gamage & Yuko , 2020. "Dynamic RNA acetylation revealed by quantitative cross-evolutionary mapping," Nature, Nature, vol. 583(7817), pages 638-643, July.
    3. Qian-Qian Sha & Wei Zheng & Yun-Wen Wu & Sen Li & Lei Guo & Shuoping Zhang & Ge Lin & Xiang-Hong Ou & Heng-Yu Fan, 2020. "Dynamics and clinical relevance of maternal mRNA clearance during the oocyte-to-embryo transition in humans," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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