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Single-cell transcriptome and translatome dual-omics reveals potential mechanisms of human oocyte maturation

Author

Listed:
  • Wenqi Hu

    (Tsinghua University)

  • Haitao Zeng

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Yanan Shi

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Chuanchuan Zhou

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Jiana Huang

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Lei Jia

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Siqi Xu

    (Tsinghua University)

  • Xiaoyu Feng

    (Tsinghua University)

  • Yanyan Zeng

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Tuanlin Xiong

    (Tsinghua University)

  • Wenze Huang

    (Tsinghua University)

  • Peng Sun

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Yajie Chang

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Tingting Li

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Cong Fang

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Keliang Wu

    (Shandong University)

  • Lingbo Cai

    (Nanjing Medical University)

  • Wuhua Ni

    (The First Affiliated Hospital of Wenzhou Medical University)

  • Yan Li

    (The First Affiliated Hospital of Wenzhou Medical University)

  • Zhiyong Yang

    (Shanghai Tenth People’s Hospital of Tongji University)

  • Qiangfeng Cliff Zhang

    (Tsinghua University)

  • RiCheng Chian

    (Shanghai Tenth People’s Hospital of Tongji University)

  • Zijiang Chen

    (Shandong University)

  • Xiaoyan Liang

    (The Sixth Affiliated Hospital of Sun Yat-sen University)

  • Kehkooi Kee

    (Tsinghua University)

Abstract

The combined use of transcriptome and translatome as indicators of gene expression profiles is usually more accurate than the use of transcriptomes alone, especially in cell types governed by translational regulation, such as mammalian oocytes. Here, we developed a dual-omics methodology that includes both transcriptome and translatome sequencing (T&T-seq) of single-cell oocyte samples, and we used it to characterize the transcriptomes and translatomes during mouse and human oocyte maturation. T&T-seq analysis revealed distinct translational expression patterns between mouse and human oocytes and delineated a sequential gene expression regulation from the cytoplasm to the nucleus during human oocyte maturation. By these means, we also identified a functional role of OOSP2 inducing factor in human oocyte maturation, as human recombinant OOSP2 induced in vitro maturation of human oocytes, which was blocked by anti-OOSP2. Single-oocyte T&T-seq analyses further elucidated that OOSP2 induces specific signaling pathways, including small GTPases, through translational regulation.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32791-2
    DOI: 10.1038/s41467-022-32791-2
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    References listed on IDEAS

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    1. Dajung Jung & Jie Xiong & Min Ye & Xunsi Qin & Lin Li & Shunfeng Cheng & Mengyuan Luo & Jia Peng & Ji Dong & Fuchou Tang & Wei Shen & Martin M. Matzuk & Kehkooi Kee, 2017. "In vitro differentiation of human embryonic stem cells into ovarian follicle-like cells," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    2. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    3. Cai-Rong Yang & Gabriel Rajkovic & Enrico Maria Daldello & Xuan G. Luong & Jing Chen & Marco Conti, 2020. "The RNA-binding protein DAZL functions as repressor and activator of mRNA translation during oocyte maturation," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    4. Yingyao Zhou & Bin Zhou & Lars Pache & Max Chang & Alireza Hadj Khodabakhshi & Olga Tanaseichuk & Christopher Benner & Sumit K. Chanda, 2019. "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    5. Michael VanInsberghe & Jeroen Berg & Amanda Andersson-Rolf & Hans Clevers & Alexander Oudenaarden, 2021. "Single-cell Ribo-seq reveals cell cycle-dependent translational pausing," Nature, Nature, vol. 597(7877), pages 561-565, September.
    6. Zhong-Yi Wang & Evgeny Leushkin & Angélica Liechti & Svetlana Ovchinnikova & Katharina Mößinger & Thoomke Brüning & Coralie Rummel & Frank Grützner & Margarida Cardoso-Moreira & Peggy Janich & David G, 2020. "Transcriptome and translatome co-evolution in mammals," Nature, Nature, vol. 588(7839), pages 642-647, December.
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    Cited by:

    1. 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.

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