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Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch

Author

Listed:
  • Hirotaka Tao

    (The Hospital for Sick Children)

  • Min Zhu

    (The Hospital for Sick Children
    University of Toronto)

  • Kimberly Lau

    (The Hospital for Sick Children)

  • Owen K. W. Whitley

    (The Hospital for Sick Children)

  • Mohammad Samani

    (The Hospital for Sick Children)

  • Xiao Xiao

    (The Hospital for Sick Children)

  • Xiao Xiao Chen

    (The Hospital for Sick Children
    University of Toronto)

  • Noah A. Hahn

    (The Hospital for Sick Children
    University of Toronto)

  • Weifan Liu

    (The Hospital for Sick Children
    University of Toronto)

  • Megan Valencia

    (University of Toronto)

  • Min Wu

    (University of Toronto)

  • Xian Wang

    (University of Toronto)

  • Kelli D. Fenelon

    (The Hospital for Sick Children
    University of Toronto)

  • Clarissa C. Pasiliao

    (The Hospital for Sick Children
    University of Toronto)

  • Di Hu

    (The Hospital for Sick Children)

  • Jinchun Wu

    (The Hospital for Sick Children)

  • Shoshana Spring

    (University of Toronto)

  • James Ferguson

    (Case Western Reserve University)

  • Edith P. Karuna

    (University of California, Davis School of Medicine)

  • R. Mark Henkelman

    (University of Toronto)

  • Alexander Dunn

    (Stanford University)

  • Huaxiong Huang

    (York University)

  • Hsin-Yi Henry Ho

    (University of California, Davis School of Medicine)

  • Radhika Atit

    (Case Western Reserve University)

  • Sidhartha Goyal

    (University of Toronto)

  • Yu Sun

    (University of Toronto)

  • Sevan Hopyan

    (The Hospital for Sick Children
    University of Toronto
    Hospital for Sick Children and University of Toronto)

Abstract

Multiple vertebrate embryonic structures such as organ primordia are composed of confluent cells. Although mechanisms that shape tissue sheets are increasingly understood, those which shape a volume of cells remain obscure. Here we show that 3D mesenchymal cell intercalations are essential to shape the mandibular arch of the mouse embryo. Using a genetically encoded vinculin tension sensor that we knock-in to the mouse genome, we show that cortical force oscillations promote these intercalations. Genetic loss- and gain-of-function approaches show that Wnt5a functions as a spatial cue to coordinate cell polarity and cytoskeletal oscillation. These processes diminish tissue rigidity and help cells to overcome the energy barrier to intercalation. YAP/TAZ and PIEZO1 serve as downstream effectors of Wnt5a-mediated actomyosin polarity and cytosolic calcium transients that orient and drive mesenchymal cell intercalations. These findings advance our understanding of how developmental pathways regulate biophysical properties and forces to shape a solid organ primordium.

Suggested Citation

  • Hirotaka Tao & Min Zhu & Kimberly Lau & Owen K. W. Whitley & Mohammad Samani & Xiao Xiao & Xiao Xiao Chen & Noah A. Hahn & Weifan Liu & Megan Valencia & Min Wu & Xian Wang & Kelli D. Fenelon & Clariss, 2019. "Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch," Nature Communications, Nature, vol. 10(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09540-z
    DOI: 10.1038/s41467-019-09540-z
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    Cited by:

    1. Yusuke Seto & Ryoma Ogihara & Kaori Takizawa & Mototsugu Eiraku, 2024. "In vitro induction of patterned branchial arch-like aggregate from human pluripotent stem cells," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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