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Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition

Author

Listed:
  • Miler T. Lee

    (Yale University School of Medicine)

  • Ashley R. Bonneau

    (Yale University School of Medicine)

  • Carter M. Takacs

    (Yale University School of Medicine)

  • Ariel A. Bazzini

    (Yale University School of Medicine)

  • Kate R. DiVito

    (Yale University School of Medicine)

  • Elizabeth S. Fleming

    (Yale University School of Medicine)

  • Antonio J. Giraldez

    (Yale University School of Medicine
    Yale Stem Cell Center, Yale University School of Medicine)

Abstract

After fertilization, maternal factors direct development and trigger zygotic genome activation (ZGA) at the maternal-to-zygotic transition (MZT). In zebrafish, ZGA is required for gastrulation and clearance of maternal messenger RNAs, which is in part regulated by the conserved microRNA miR-430. However, the factors that activate the zygotic program in vertebrates are unknown. Here we show that Nanog, Pou5f1 (also called Oct4) and SoxB1 regulate zygotic gene activation in zebrafish. We identified several hundred genes directly activated by maternal factors, constituting the first wave of zygotic transcription. Ribosome profiling revealed that nanog, sox19b and pou5f1 are the most highly translated transcription factors pre-MZT. Combined loss of these factors resulted in developmental arrest before gastrulation and a failure to activate >75% of zygotic genes, including miR-430. Our results demonstrate that maternal Nanog, Pou5f1 and SoxB1 are required to initiate the zygotic developmental program and induce clearance of the maternal program by activating miR-430 expression.

Suggested Citation

  • Miler T. Lee & Ashley R. Bonneau & Carter M. Takacs & Ariel A. Bazzini & Kate R. DiVito & Elizabeth S. Fleming & Antonio J. Giraldez, 2013. "Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition," Nature, Nature, vol. 503(7476), pages 360-364, November.
    • Handle: RePEc:nat:nature:v:503:y:2013:i:7476:d:10.1038_nature12632
    DOI: 10.1038/nature12632
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    Citations

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    Cited by:

    1. Xiaoqing Nie & Qianhua Xu & Chengpeng Xu & Fengling Chen & Qizhi Wang & Dandan Qin & Rui Wang & Zheng Gao & Xukun Lu & Xinai Yang & Yu Wu & Chen Gu & Wei Xie & Lei Li, 2023. "Maternal TDP-43 interacts with RNA Pol II and regulates zygotic genome activation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Aileen Julia Riesle & Meijiang Gao & Marcus Rosenblatt & Jacques Hermes & Helge Hass & Anna Gebhard & Marina Veil & Björn Grüning & Jens Timmer & Daria Onichtchouk, 2023. "Activator-blocker model of transcriptional regulation by pioneer-like factors," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Meijiang Gao & Marina Veil & Marcus Rosenblatt & Aileen Julia Riesle & Anna Gebhard & Helge Hass & Lenka Buryanova & Lev Y. Yampolsky & Björn Grüning & Sergey V. Ulianov & Jens Timmer & Daria Onichtch, 2022. "Pluripotency factors determine gene expression repertoire at zygotic genome activation," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. Xinru Zhang & Bohao Fang & Yi-Fei Huang, 2023. "Transcription factor binding sites are frequently under accelerated evolution in primates," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Lior Fishman & Avani Modak & Gal Nechooshtan & Talya Razin & Florian Erhard & Aviv Regev & Jeffrey A. Farrell & Michal Rabani, 2024. "Cell-type-specific mRNA transcription and degradation kinetics in zebrafish embryogenesis from metabolically labeled single-cell RNA-seq," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. Ya Gao & Daisylyn Senna Tan & Mathias Girbig & Haoqing Hu & Xiaomin Zhou & Qianwen Xie & Shi Wing Yeung & Kin Shing Lee & Sik Yin Ho & Vlad Cojocaru & Jian Yan & Georg K. A. Hochberg & Alex Mendoza & , 2024. "The emergence of Sox and POU transcription factors predates the origins of animal stem cells," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Saurabh J. Pradhan & Puli Chandramouli Reddy & Michael Smutny & Ankita Sharma & Keisuke Sako & Meghana S. Oak & Rini Shah & Mrinmoy Pal & Ojas Deshpande & Greg Dsilva & Yin Tang & Rakesh Mishra & Giri, 2021. "Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis," Nature Communications, Nature, vol. 12(1), pages 1-19, December.

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