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 & 7 others Alexander Dunn, Huaxiong Huang, Hsin-Yi Henry Ho, Radhika Atit, Sidhartha Goyal, Yu Sun, Sevan Hopyan

Research output: Contribution to journalArticle

1 Citation (Scopus)

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

Fingerprint

arches
Cell Shape
Arches
Intercalation
intercalation
cells
Tissue
Vinculin
organs
Actomyosin
Embryonic Structures
mice
Energy barriers
Rigidity
effectors
vertebrates
oscillations
Cell Size
genome
Genes

ASJC Scopus subject areas

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

Cite this

Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch. / Tao, Hirotaka; Zhu, Min; Lau, Kimberly; Whitley, Owen K.W.; Samani, Mohammad; Xiao, Xiao; Chen, Xiao Xiao; Hahn, Noah A.; Liu, Weifan; Valencia, Megan; Wu, Min; Wang, Xian; Fenelon, Kelli D.; Pasiliao, Clarissa C.; Hu, Di; Wu, Jinchun; Spring, Shoshana; Ferguson, James; Karuna, Edith P.; Henkelman, R. Mark; Dunn, Alexander; Huang, Huaxiong; Ho, Hsin-Yi Henry; Atit, Radhika; Goyal, Sidhartha; Sun, Yu; Hopyan, Sevan.

In: Nature communications, Vol. 10, No. 1, 1703, 01.12.2019.

Research output: Contribution to journalArticle

Tao, H, Zhu, M, Lau, K, Whitley, OKW, Samani, M, Xiao, X, Chen, XX, Hahn, NA, Liu, W, Valencia, M, Wu, M, Wang, X, Fenelon, KD, Pasiliao, CC, Hu, D, Wu, J, Spring, S, Ferguson, J, Karuna, EP, Henkelman, RM, Dunn, A, Huang, H, Ho, H-YH, Atit, R, Goyal, S, Sun, Y & Hopyan, S 2019, 'Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch', Nature communications, vol. 10, no. 1, 1703. https://doi.org/10.1038/s41467-019-09540-z
Tao, Hirotaka ; Zhu, Min ; Lau, Kimberly ; Whitley, Owen K.W. ; Samani, Mohammad ; Xiao, Xiao ; Chen, Xiao Xiao ; Hahn, Noah A. ; Liu, Weifan ; Valencia, Megan ; Wu, Min ; Wang, Xian ; Fenelon, Kelli D. ; Pasiliao, Clarissa C. ; Hu, Di ; Wu, Jinchun ; Spring, Shoshana ; Ferguson, James ; Karuna, Edith P. ; Henkelman, R. Mark ; Dunn, Alexander ; Huang, Huaxiong ; Ho, Hsin-Yi Henry ; Atit, Radhika ; Goyal, Sidhartha ; Sun, Yu ; Hopyan, Sevan. / Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch. In: Nature communications. 2019 ; Vol. 10, No. 1.
@article{9984c625af2241e0abea3343dc8a39c4,
title = "Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch",
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.",
author = "Hirotaka Tao and Min Zhu and Kimberly Lau and Whitley, {Owen K.W.} and Mohammad Samani and Xiao Xiao and Chen, {Xiao Xiao} and Hahn, {Noah A.} and Weifan Liu and Megan Valencia and Min Wu and Xian Wang and Fenelon, {Kelli D.} and Pasiliao, {Clarissa C.} and Di Hu and Jinchun Wu and Shoshana Spring and James Ferguson and Karuna, {Edith P.} and Henkelman, {R. Mark} and Alexander Dunn and Huaxiong Huang and Ho, {Hsin-Yi Henry} and Radhika Atit and Sidhartha Goyal and Yu Sun and Sevan Hopyan",
year = "2019",
month = "12",
day = "1",
doi = "10.1038/s41467-019-09540-z",
language = "English (US)",
volume = "10",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",
number = "1",

}

TY - JOUR

T1 - Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch

AU - Tao, Hirotaka

AU - Zhu, Min

AU - Lau, Kimberly

AU - Whitley, Owen K.W.

AU - Samani, Mohammad

AU - Xiao, Xiao

AU - Chen, Xiao Xiao

AU - Hahn, Noah A.

AU - Liu, Weifan

AU - Valencia, Megan

AU - Wu, Min

AU - Wang, Xian

AU - Fenelon, Kelli D.

AU - Pasiliao, Clarissa C.

AU - Hu, Di

AU - Wu, Jinchun

AU - Spring, Shoshana

AU - Ferguson, James

AU - Karuna, Edith P.

AU - Henkelman, R. Mark

AU - Dunn, Alexander

AU - Huang, Huaxiong

AU - Ho, Hsin-Yi Henry

AU - Atit, Radhika

AU - Goyal, Sidhartha

AU - Sun, Yu

AU - Hopyan, Sevan

PY - 2019/12/1

Y1 - 2019/12/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85064339438&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85064339438&partnerID=8YFLogxK

U2 - 10.1038/s41467-019-09540-z

DO - 10.1038/s41467-019-09540-z

M3 - Article

VL - 10

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 1703

ER -