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ZIC2 and ZIC3 promote SWI/SNF recruitment to safeguard progression towards human primed pluripotency

Author

Listed:
  • Ishtiaque Hossain

    (McGill University)

  • Pierre Priam

    (University of Montreal
    University of Montreal)

  • Sofia C. Reynoso

    (McGill University)

  • Sahil Sahni

    (McGill University)

  • Xiao X. Zhang

    (McGill University)

  • Laurence Côté

    (University of Montreal
    University of Montreal)

  • Joelle Doumat

    (McGill University)

  • Candus Chik

    (McGill University)

  • Tianxin Fu

    (McGill University)

  • Julie A. Lessard

    (University of Montreal
    University of Montreal)

  • William A. Pastor

    (McGill University
    McGill University)

Abstract

The primed epiblast acts as a transitional stage between the relatively homogeneous naïve epiblast and the gastrulating embryo. Its formation entails coordinated changes in regulatory circuits driven by transcription factors and epigenetic modifications. Using a multi-omic approach in human embryonic stem cell models across the spectrum of peri-implantation development, we demonstrate that the transcription factors ZIC2 and ZIC3 have overlapping but essential roles in opening primed-specific enhancers. Together, they are essential to facilitate progression to and maintain primed pluripotency. ZIC2/3 accomplish this by recruiting SWI/SNF to chromatin and loss of ZIC2/3 or degradation of SWI/SNF both prevent enhancer activation. Loss of ZIC2/3 also results in transcriptome changes consistent with perturbed Polycomb activity and a shift towards the expression of genes linked to differentiation towards the mesendoderm. Additionally, we find an intriguing dependency on the transcriptional machinery for sustained recruitment of ZIC2/3 over a subset of primed-hESC specific enhancers. Taken together, ZIC2 and ZIC3 regulate highly dynamic lineage-specific enhancers and collectively act as key regulators of human primed pluripotency.

Suggested Citation

  • Ishtiaque Hossain & Pierre Priam & Sofia C. Reynoso & Sahil Sahni & Xiao X. Zhang & Laurence Côté & Joelle Doumat & Candus Chik & Tianxin Fu & Julie A. Lessard & William A. Pastor, 2024. "ZIC2 and ZIC3 promote SWI/SNF recruitment to safeguard progression towards human primed pluripotency," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52431-1
    DOI: 10.1038/s41467-024-52431-1
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    References listed on IDEAS

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    1. Alexander M. Tsankov & Hongcang Gu & Veronika Akopian & Michael J. Ziller & Julie Donaghey & Ido Amit & Andreas Gnirke & Alexander Meissner, 2015. "Transcription factor binding dynamics during human ES cell differentiation," Nature, Nature, vol. 518(7539), pages 344-349, February.
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