Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion

Chao Jiang, Hong-Yu Luo, Xinpeng Xu, Shuo-Xing Dou, Wei Li, Dongshi Guan, Fangfu Ye, Xiaosong Chen, Ming Guo, Peng-Ye Wang () and Hui Li ()
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Chao Jiang: Chinese Academy of Sciences
Hong-Yu Luo: Chinese Academy of Sciences
Xinpeng Xu: Guangdong Technion—Israel Institute of Technology
Shuo-Xing Dou: Chinese Academy of Sciences
Wei Li: Chinese Academy of Sciences
Dongshi Guan: University of Chinese Academy of Sciences
Fangfu Ye: Chinese Academy of Sciences
Xiaosong Chen: Beijing Normal University
Ming Guo: 77 Massachusetts Ave
Peng-Ye Wang: Chinese Academy of Sciences
Hui Li: Beijing Normal University

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract Cell migration plays important roles in many biological processes, but how migrating cells orchestrate intracellular molecules and subcellular structures to regulate their speed and direction is still not clear. Here, by characterizing the intracellular diffusion and the three-dimensional lamellipodium structures of fish keratocyte cells, we observe a strong positive correlation between the intracellular diffusion and cell migration speed and, more importantly, discover a switching of cell migration modes with reversible intracellular diffusion variation and lamellipodium structure deformation. Distinct from the normal fast mode, cells migrating in the newly-found slow mode have a deformed lamellipodium with swollen-up front and thinned-down rear, reduced intracellular diffusion and compartmentalized macromolecule distribution in the lamellipodium. Furthermore, in turning cells, both lamellipodium structure and intracellular diffusion dynamics are also changed, with left-right symmetry breaking. We propose a mechanism involving the front-localized actin polymerization and increased molecular crowding in the lamellipodium to explain how cells spatiotemporally coordinate the intracellular diffusion dynamics and the lamellipodium structure in regulating their migrations.

Date: 2023
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DOI: 10.1038/s41467-023-40858-x

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