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A multiple super-enhancer region establishes inter-TAD interactions and controls Hoxa function in cranial neural crest

Author

Listed:
  • Sandra Kessler

    (Friedrich Miescher Institute for Biomedical Research
    University of Basel)

  • Maryline Minoux

    (Friedrich Miescher Institute for Biomedical Research
    Université de Strasbourg, Faculté de Chirurgie Dentaire)

  • Onkar Joshi

    (Friedrich Miescher Institute for Biomedical Research)

  • Yousra Zouari

    (Friedrich Miescher Institute for Biomedical Research)

  • Sebastien Ducret

    (Friedrich Miescher Institute for Biomedical Research)

  • Fiona Ross

    (Friedrich Miescher Institute for Biomedical Research
    University of Basel)

  • Nathalie Vilain

    (Friedrich Miescher Institute for Biomedical Research)

  • Adwait Salvi

    (Friedrich Miescher Institute for Biomedical Research
    University of Basel)

  • Joachim Wolff

    (Friedrich Miescher Institute for Biomedical Research)

  • Hubertus Kohler

    (Friedrich Miescher Institute for Biomedical Research)

  • Michael B. Stadler

    (Friedrich Miescher Institute for Biomedical Research)

  • Filippo M. Rijli

    (Friedrich Miescher Institute for Biomedical Research
    University of Basel)

Abstract

Enhancer-promoter interactions preferentially occur within boundary-insulated topologically associating domains (TADs), limiting inter-TAD interactions. Enhancer clusters in linear proximity, termed super-enhancers (SEs), ensure high target gene expression levels. Little is known about SE topological regulatory impact during craniofacial development. Here, we identify 2232 genome-wide putative SEs in mouse cranial neural crest cells (CNCCs), 147 of which target genes establishing CNCC positional identity during face formation. In second pharyngeal arch (PA2) CNCCs, a multiple SE-containing region, partitioned into Hoxa Inter-TAD Regulatory Element 1 and 2 (HIRE1 and HIRE2), establishes long-range inter-TAD interactions selectively with Hoxa2, that is required for external and middle ear structures. HIRE2 deletion in a Hoxa2 haploinsufficient background results in microtia. HIRE1 deletion phenocopies the full homeotic Hoxa2 knockout phenotype and induces PA3 and PA4 CNCC abnormalities correlating with Hoxa2 and Hoxa3 transcriptional downregulation. Thus, SEs can overcome TAD insulation and regulate anterior Hoxa gene collinear expression in a CNCC subpopulation-specific manner during craniofacial development.

Suggested Citation

  • Sandra Kessler & Maryline Minoux & Onkar Joshi & Yousra Zouari & Sebastien Ducret & Fiona Ross & Nathalie Vilain & Adwait Salvi & Joachim Wolff & Hubertus Kohler & Michael B. Stadler & Filippo M. Rijl, 2023. "A multiple super-enhancer region establishes inter-TAD interactions and controls Hoxa function in cranial neural crest," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38953-0
    DOI: 10.1038/s41467-023-38953-0
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    Cited by:

    1. Samuel Abassah-Oppong & Matteo Zoia & Brandon J. Mannion & Raquel Rouco & Virginie Tissières & Cailyn H. Spurrell & Virginia Roland & Fabrice Darbellay & Anja Itum & Julie Gamart & Tabitha A. Festa-Da, 2024. "A gene desert required for regulatory control of pleiotropic Shox2 expression and embryonic survival," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    2. Andrea Wilderman & Eva D’haene & Machteld Baetens & Tara N. Yankee & Emma Wentworth Winchester & Nicole Glidden & Ellen Roets & Jo Dorpe & Sandra Janssens & Danny E. Miller & Miranda Galey & Kari M. B, 2024. "A distant global control region is essential for normal expression of anterior HOXA genes during mouse and human craniofacial development," Nature Communications, Nature, vol. 15(1), pages 1-23, December.

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