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Reconstitution of the oocyte transcriptional network with transcription factors

Author

Listed:
  • Nobuhiko Hamazaki

    (Kyushu University)

  • Hirohisa Kyogoku

    (RIKEN Center for Biosystems Dynamics Research)

  • Hiromitsu Araki

    (Kyushu University)

  • Fumihito Miura

    (Kyushu University)

  • Chisako Horikawa

    (Kyushu University)

  • Norio Hamada

    (Kyushu University
    Kyushu University)

  • So Shimamoto

    (Kyushu University)

  • Orie Hikabe

    (Kyushu University)

  • Kinichi Nakashima

    (Kyushu University)

  • Tomoya S. Kitajima

    (RIKEN Center for Biosystems Dynamics Research)

  • Takashi Ito

    (Kyushu University)

  • Harry G. Leitch

    (MRC London Institute of Medical Sciences (LMS)
    Institute of Clinical Sciences (ICS), Faculty of Medicine, Imperial College London)

  • Katsuhiko Hayashi

    (Kyushu University)

Abstract

During female germline development, oocytes become a highly specialized cell type and form a maternal cytoplasmic store of crucial factors. Oocyte growth is triggered at the transition from primordial to primary follicle and is accompanied by dynamic changes in gene expression1, but the gene regulatory network that controls oocyte growth remains unknown. Here we identify a set of transcription factors that are sufficient to trigger oocyte growth. By investigation of the changes in gene expression and functional screening using an in vitro mouse oocyte development system, we identified eight transcription factors, each of which was essential for the transition from primordial to primary follicle. Notably, enforced expression of these transcription factors swiftly converted pluripotent stem cells into oocyte-like cells that were competent for fertilization and subsequent cleavage. These transcription-factor-induced oocyte-like cells were formed without specification of primordial germ cells, epigenetic reprogramming or meiosis, and demonstrate that oocyte growth and lineage-specific de novo DNA methylation are separable from the preceding epigenetic reprogramming in primordial germ cells. This study identifies a core set of transcription factors for orchestrating oocyte growth, and provides an alternative source of ooplasm, which is a unique material for reproductive biology and medicine.

Suggested Citation

  • Nobuhiko Hamazaki & Hirohisa Kyogoku & Hiromitsu Araki & Fumihito Miura & Chisako Horikawa & Norio Hamada & So Shimamoto & Orie Hikabe & Kinichi Nakashima & Tomoya S. Kitajima & Takashi Ito & Harry G., 2021. "Reconstitution of the oocyte transcriptional network with transcription factors," Nature, Nature, vol. 589(7841), pages 264-269, January.
  • Handle: RePEc:nat:nature:v:589:y:2021:i:7841:d:10.1038_s41586-020-3027-9
    DOI: 10.1038/s41586-020-3027-9
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    Citations

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    Cited by:

    1. Ryuki Shimada & Yuzuru Kato & Naoki Takeda & Sayoko Fujimura & Kei-ichiro Yasunaga & Shingo Usuki & Hitoshi Niwa & Kimi Araki & Kei-ichiro Ishiguro, 2023. "STRA8–RB interaction is required for timely entry of meiosis in mouse female germ cells," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Mengwen Hu & Yu-Han Yeh & Yasuhisa Munakata & Hironori Abe & Akihiko Sakashita & So Maezawa & Miguel Vidal & Haruhiko Koseki & Neil Hunter & Richard M. Schultz & Satoshi H. Namekawa, 2022. "PRC1-mediated epigenetic programming is required to generate the ovarian reserve," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Ilmatar Rooda & Jasmin Hassan & Jie Hao & Magdalena Wagner & Elisabeth Moussaud-Lamodière & Kersti Jääger & Marjut Otala & Katri Knuus & Cecilia Lindskog & Kiriaki Papaikonomou & Sebastian Gidlöf & Ce, 2024. "In-depth analysis of transcriptomes in ovarian cortical follicles from children and adults reveals interfollicular heterogeneity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Yusheng Liu & Wenrong Tao & Shuang Wu & Yiwei Zhang & Hu Nie & Zhenzhen Hou & Jingye Zhang & Zhen Yang & Zi-Jiang Chen & Jiaqiang Wang & Falong Lu & Keliang Wu, 2024. "Maternal mRNA deadenylation is defective in in vitro matured mouse and human oocytes," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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