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 HenkelmanAlexander Dunn, Huaxiong Huang, Hsin-Yi Henry Ho, Radhika Atit, Sidhartha Goyal, Yu Sun, Sevan Hopyan

Research output: Contribution to journalArticle

6 Scopus citations

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.

Original languageEnglish (US)
Article number1703
JournalNature communications
Volume10
Issue number1
DOIs
StatePublished - Dec 1 2019

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

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    Tao, H., Zhu, M., Lau, K., Whitley, O. K. W., Samani, M., Xiao, X., Chen, X. X., Hahn, N. A., Liu, W., Valencia, M., Wu, M., Wang, X., Fenelon, K. D., Pasiliao, C. C., Hu, D., Wu, J., Spring, S., Ferguson, J., Karuna, E. P., ... Hopyan, S. (2019). Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch. Nature communications, 10(1), [1703]. https://doi.org/10.1038/s41467-019-09540-z