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The developing mouse coronal suture at single-cell resolution

Author

Listed:
  • D’Juan T. Farmer

    (University of Southern California)

  • Hana Mlcochova

    (University of Oxford)

  • Yan Zhou

    (University of Oxford)

  • Nils Koelling

    (University of Oxford)

  • Guanlin Wang

    (University of Oxford
    University of Oxford)

  • Neil Ashley

    (University of Oxford)

  • Helena Bugacov

    (University of Southern California)

  • Hung-Jhen Chen

    (University of Southern California)

  • Riana Parvez

    (University of Southern California)

  • Kuo-Chang Tseng

    (University of Southern California)

  • Amy E. Merrill

    (University of Southern California)

  • Robert E. Maxson

    (University of Southern California)

  • Andrew O. M. Wilkie

    (University of Oxford)

  • J. Gage Crump

    (University of Southern California)

  • Stephen R. F. Twigg

    (University of Oxford)

Abstract

Sutures separate the flat bones of the skull and enable coordinated growth of the brain and overlying cranium. The coronal suture is most commonly fused in monogenic craniosynostosis, yet the unique aspects of its development remain incompletely understood. To uncover the cellular diversity within the murine embryonic coronal suture, we generated single-cell transcriptomes and performed extensive expression validation. We find distinct pre-osteoblast signatures between the bone fronts and periosteum, a ligament-like population above the suture that persists into adulthood, and a chondrogenic-like population in the dura mater underlying the suture. Lineage tracing reveals an embryonic Six2+ osteoprogenitor population that contributes to the postnatal suture mesenchyme, with these progenitors being preferentially affected in a Twist1+/−; Tcf12+/− mouse model of Saethre-Chotzen Syndrome. This single-cell atlas provides a resource for understanding the development of the coronal suture and the mechanisms for its loss in craniosynostosis.

Suggested Citation

  • D’Juan T. Farmer & Hana Mlcochova & Yan Zhou & Nils Koelling & Guanlin Wang & Neil Ashley & Helena Bugacov & Hung-Jhen Chen & Riana Parvez & Kuo-Chang Tseng & Amy E. Merrill & Robert E. Maxson & Andre, 2021. "The developing mouse coronal suture at single-cell resolution," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-24917-9
    DOI: 10.1038/s41467-021-24917-9
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    Cited by:

    1. D’Juan T. Farmer & Jennifer E. Dukov & Hung-Jhen Chen & Claire Arata & Jose Hernandez-Trejo & Pengfei Xu & Camilla S. Teng & Robert E. Maxson & J. Gage Crump, 2024. "Cellular transitions during cranial suture establishment in zebrafish," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Junjun Jing & Jifan Feng & Yuan Yuan & Tingwei Guo & Jie Lei & Fei Pei & Thach-Vu Ho & Yang Chai, 2022. "Spatiotemporal single-cell regulatory atlas reveals neural crest lineage diversification and cellular function during tooth morphogenesis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Sudha Sunil Rajderkar & Kitt Paraiso & Maria Luisa Amaral & Michael Kosicki & Laura E. Cook & Fabrice Darbellay & Cailyn H. Spurrell & Marco Osterwalder & Yiwen Zhu & Han Wu & Sarah Yasmeen Afzal & Ma, 2024. "Dynamic enhancer landscapes in human craniofacial development," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Ariel C. Vonk & Xiaofan Zhao & Zheyu Pan & Megan L. Hudnall & Conrad G. Oakes & Gabriela A. Lopez & Sarah C. Hasel-Kolossa & Alexander W. C. Kuncz & Sasha B. Sengelmann & Darian J. Gamble & Thomas P. , 2023. "Single-cell analysis of lizard blastema fibroblasts reveals phagocyte-dependent activation of Hedgehog-responsive chondrogenesis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Seppe Goovaerts & Hanne Hoskens & Ryan J. Eller & Noah Herrick & Anthony M. Musolf & Cristina M. Justice & Meng Yuan & Sahin Naqvi & Myoung Keun Lee & Dirk Vandermeulen & Heather L. Szabo-Rogers & Pau, 2023. "Joint multi-ancestry and admixed GWAS reveals the complex genetics behind human cranial vault shape," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    6. Greg Holmes & Ana S. Gonzalez-Reiche & Madrikha Saturne & Susan M. Motch Perrine & Xianxiao Zhou & Ana C. Borges & Bhavana Shewale & Joan T. Richtsmeier & Bin Zhang & Harm Bakel & Ethylin Wang Jabs, 2021. "Single-cell analysis identifies a key role for Hhip in murine coronal suture development," Nature Communications, Nature, vol. 12(1), pages 1-16, December.

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