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

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, Clarissa C. Pasiliao, Di Hu, Jinchun Wu, Shoshana Spring, James Ferguson, Edith P. Karuna, R. Mark Henkelman, Alexander Dunn, Huaxiong Huang, Hsin-Yi Henry Ho, Radhika Atit, Sidhartha Goyal, Yu Sun () and Sevan Hopyan ()
Additional contact information
Hirotaka Tao: The Hospital for Sick Children
Min Zhu: The Hospital for Sick Children
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
Noah A. Hahn: The Hospital for Sick Children
Weifan Liu: The Hospital for Sick Children
Megan Valencia: University of Toronto
Min Wu: University of Toronto
Xian Wang: University of Toronto
Kelli D. Fenelon: The Hospital for Sick Children
Clarissa C. Pasiliao: The Hospital for Sick Children
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

Nature Communications, 2019, vol. 10, issue 1, 1-18

Abstract: 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.

Date: 2019
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DOI: 10.1038/s41467-019-09540-z

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