Actin-ring segment switching drives nonadhesive gap closure

Qiong Wei, Xuechen Shi, Tiankai Zhao, Pingqiang Cai, Tianwu Chen, Yao Zhang, Changjin Huang, Jian Yang, Xiaodong Chen, Sulin Zhang

Research output: Contribution to journalArticlepeer-review

Abstract

Gap closure to eliminate physical discontinuities and restore tissue integrity is a fundamental process in normal development and repair of damaged tissues and organs. Here, we demonstrate a nonadhesive gap closure model in which collective cell migration, large-scale actin-network fusion, and purse-string contraction orchestrate to restore the gap. Proliferative pressure drives migrating cells to attach onto the gap front at which a pluricellular actin ring is already assembled. An actin-ring segment switching process then occurs by fusion of actin fibers from the newly attached cells into the actin cable and defusion from the previously lined cells, thereby narrowing the gap. Such actin-cable segment switching occurs favorably at high curvature edges of the gap, yielding size-dependent gap closure. Cellular force microscopies evidence that a persistent rise in the radial component of inward traction force signifies successful actin-cable segment switching. A kinetic model that integrates cell proliferation, actin fiber fusion, and purse-string contraction is formulated to quantitatively account for the gap-closure dynamics. Our data reveal a previously unexplored mechanism in which cells exploit multifaceted strategies in a highly cooperative manner to close nonadhesive gaps.

Original languageEnglish (US)
Pages (from-to)33263-33271
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number52
DOIs
StatePublished - Dec 29 2021

All Science Journal Classification (ASJC) codes

  • General

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