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The chromatin, topological and regulatory properties of pluripotency-associated poised enhancers are conserved in vivo

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  • Giuliano Crispatzu

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne
    University Hospital Cologne
    University of Cologne)

  • Rizwan Rehimi

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne)

  • Tomas Pachano

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne)

  • Tore Bleckwehl

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne)

  • Sara Cruz-Molina

    (Max Planck Institute for Molecular Biomedicine)

  • Cally Xiao

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne
    University of Cologne
    University Hospital Cologne
    Keck School of Medicine of University of Southern California)

  • Esther Mahabir

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne)

  • Hisham Bazzi

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne
    University of Cologne
    University Hospital Cologne)

  • Alvaro Rada-Iglesias

    (Center for Molecular Medicine Cologne (CMMC), University of Cologne
    University of Cologne
    CSIC-Universidad de Cantabria-SODERCAN)

Abstract

Poised enhancers (PEs) represent a genetically distinct set of distal regulatory elements that control the expression of major developmental genes. Before becoming activated in differentiating cells, PEs are already bookmarked in pluripotent cells with unique chromatin and topological features that could contribute to their privileged regulatory properties. However, since PEs were originally characterized in embryonic stem cells (ESC), it is currently unknown whether PEs are functionally conserved in vivo. Here, we show that the chromatin and 3D structural features of PEs are conserved among mouse pluripotent cells both in vitro and in vivo. We also uncovered that the interactions between PEs and their target genes are globally controlled by the combined action of Polycomb, Trithorax and architectural proteins. Moreover, distal regulatory sequences located close to developmental genes and displaying the typical genetic (i.e. CpG islands) and chromatin (i.e. high accessibility and H3K27me3 levels) features of PEs are commonly found across vertebrates. These putative PEs show high sequence conservation within specific vertebrate clades, with only a few being evolutionary conserved across all vertebrates. Lastly, by genetically disrupting PEs in mouse and chicken embryos, we demonstrate that these regulatory elements play essential roles during the induction of major developmental genes in vivo.

Suggested Citation

  • Giuliano Crispatzu & Rizwan Rehimi & Tomas Pachano & Tore Bleckwehl & Sara Cruz-Molina & Cally Xiao & Esther Mahabir & Hisham Bazzi & Alvaro Rada-Iglesias, 2021. "The chromatin, topological and regulatory properties of pluripotency-associated poised enhancers are conserved in vivo," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-24641-4
    DOI: 10.1038/s41467-021-24641-4
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    Cited by:

    1. Aileen Szczepanski & Natsumi Tsuboyama & Huijue Lyu & Ping Wang & Oguzhan Beytullahoglu & Te Zhang & Benjamin David Singer & Feng Yue & Zibo Zhao & Lu Wang, 2024. "A SWI/SNF-dependent transcriptional regulation mediated by POU2AF2/C11orf53 at enhancer," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Umut Berkay Altıntaş & Ji-Heui Seo & Claudia Giambartolomei & Dogancan Ozturan & Brad J. Fortunato & Geoffrey M. Nelson & Seth R. Goldman & Karen Adelman & Faraz Hach & Matthew L. Freedman & Nathan A., 2024. "Decoding the epigenetics and chromatin loop dynamics of androgen receptor-mediated transcription," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Chaitali Chakraborty & Itzel Nissen & Craig A. Vincent & Anna-Carin Hägglund & Andreas Hörnblad & Silvia Remeseiro, 2023. "Rewiring of the promoter-enhancer interactome and regulatory landscape in glioblastoma orchestrates gene expression underlying neurogliomal synaptic communication," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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