Basal actomyosin pulses expand epithelium coordinating cell flattening and tissue elongation

Shun Li, Zong-Yuan Liu, Hao Li, Sijia Zhou, Jiaying Liu, Ningwei Sun, Kai-Fu Yang, Vanessa Dougados, Thomas Mangeat, Karine Belguise, Xi-Qiao Feng (), Yiyao Liu () and Xiaobo Wang ()
Additional contact information
Shun Li: University of Electronic Science and Technology of China
Zong-Yuan Liu: Tsinghua University
Hao Li: UPS
Sijia Zhou: UPS
Jiaying Liu: UPS
Ningwei Sun: UPS
Kai-Fu Yang: University of Electronic Science and Technology of China
Vanessa Dougados: UPS
Thomas Mangeat: UPS
Karine Belguise: UPS
Xi-Qiao Feng: Tsinghua University
Yiyao Liu: University of Electronic Science and Technology of China
Xiaobo Wang: UPS

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: Abstract Actomyosin networks constrict cell area and junctions to alter cell and tissue shape. However, during cell expansion under mechanical stress, actomyosin networks are strengthened and polarized to relax stress. Thus, cells face a conflicting situation between the enhanced actomyosin contractile properties and the expansion behaviour of the cell or tissue. To address this paradoxical situation, we study late Drosophila oogenesis and reveal an unusual epithelial expansion wave behaviour. Mechanistically, Rac1 and Rho1 integrate basal pulsatile actomyosin networks with ruffles and focal adhesions to increase and then stabilize basal area of epithelial cells allowing their flattening and elongation. This epithelial expansion behaviour bridges cell changes to oocyte growth and extension, while oocyte growth in turn deforms the epithelium to drive cell spreading. Basal pulsatile actomyosin networks exhibit non-contractile mechanics, non-linear structures and F-actin/Myosin-II spatiotemporal signal separation, implicating unreported expanding properties. Biophysical modelling incorporating these expanding properties well simulates epithelial cell expansion waves. Our work thus highlights actomyosin expanding properties as a key mechanism driving tissue morphogenesis.

Date: 2024
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DOI: 10.1038/s41467-024-47236-1

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