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Activator-blocker model of transcriptional regulation by pioneer-like factors

Author

Listed:
  • Aileen Julia Riesle

    (Albert-Ludwigs-University of Freiburg
    EMBL Rome, Adriano Buzzati-Traverso Campus)

  • Meijiang Gao

    (Albert-Ludwigs-University of Freiburg
    Signalling Research centers BIOSS and CIBSS)

  • Marcus Rosenblatt

    (Albert-Ludwigs-University of Freiburg
    Freiburg Center for Data Analysis and Modelling (FDM))

  • Jacques Hermes

    (Albert-Ludwigs-University of Freiburg
    Freiburg Center for Data Analysis and Modelling (FDM))

  • Helge Hass

    (Albert-Ludwigs-University of Freiburg
    Freiburg Center for Data Analysis and Modelling (FDM))

  • Anna Gebhard

    (Albert-Ludwigs-University of Freiburg)

  • Marina Veil

    (Albert-Ludwigs-University of Freiburg)

  • Björn Grüning

    (University of Freiburg
    University of Freiburg)

  • Jens Timmer

    (Signalling Research centers BIOSS and CIBSS
    Albert-Ludwigs-University of Freiburg
    Freiburg Center for Data Analysis and Modelling (FDM))

  • Daria Onichtchouk

    (Albert-Ludwigs-University of Freiburg
    Signalling Research centers BIOSS and CIBSS
    Institute of Developmental Biology RAS)

Abstract

Zygotic genome activation (ZGA) in the development of flies, fish, frogs and mammals depends on pioneer-like transcription factors (TFs). Those TFs create open chromatin regions, promote histone acetylation on enhancers, and activate transcription. Here, we use the panel of single, double and triple mutants for zebrafish genome activators Pou5f3, Sox19b and Nanog, multi-omics and mathematical modeling to investigate the combinatorial mechanisms of genome activation. We show that Pou5f3 and Nanog act differently on synergistic and antagonistic enhancer types. Pou5f3 and Nanog both bind as pioneer-like TFs on synergistic enhancers, promote histone acetylation and activate transcription. Antagonistic enhancers are activated by binding of one of these factors. The other TF binds as non-pioneer-like TF, competes with the activator and blocks all its effects, partially or completely. This activator-blocker mechanism mutually restricts widespread transcriptional activation by Pou5f3 and Nanog and prevents premature expression of late developmental regulators in the early embryo.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41507-z
    DOI: 10.1038/s41467-023-41507-z
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    References listed on IDEAS

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    1. Noam Kaplan & Irene K. Moore & Yvonne Fondufe-Mittendorf & Andrea J. Gossett & Desiree Tillo & Yair Field & Emily M. LeProust & Timothy R. Hughes & Jason D. Lieb & Jonathan Widom & Eran Segal, 2009. "The DNA-encoded nucleosome organization of a eukaryotic genome," Nature, Nature, vol. 458(7236), pages 362-366, March.
    2. 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.
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