Neighbor cells restrain furrowing during Xenopus epithelial cytokinesis

• Published in: Developmental cell Vol. 60; no. 16; pp. 2139 - 2148.e6
• Main Authors: Landino, Jennifer, Misterovich, Eileen, van den Goor, Lotte, Adhikary, Babli, Chumki, Shahana, Davidson, Lance A., Miller, Ann L.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 18.08.2025
• Subjects: actin; Animals; computational modeling; cytokinesis; Cytokinesis - physiology; Epithelial Cells - cytology; Epithelial Cells - metabolism; epithelium; Epithelium - metabolism; Mechanotransduction, Cellular - physiology; myosin II; optogenetics; Rho GTPase; vinculin; Xenopus; Xenopus laevis; Xenopus Proteins - metabolism; ɑ-actinin; Xenopus; actin; vinculin; cytokinesis; myosin II; optogenetics; epithelium; ɑ-actinin; computational modeling; Rho GTPase
• ISSN: 1534-5807; 1878-1551; 1878-1551
• DOI: 10.1016/j.devcel.2025.03.010

Cytokinesis challenges epithelial tissue homeostasis by generating forces that pull on neighboring cells. Junction reinforcement at the furrow in Xenopus epithelia regulates the speed of furrowing, suggesting that cytokinesis is subject to resistive forces from epithelial neighbors. We show that contractility factors accumulate near the furrow in neighboring cells, and increasing neighbor cell stiffness slows furrowing. Optogenetically increasing contractility in one or both neighbor cells slows furrowing or induces cytokinetic failure. Uncoupling mechanotransduction between dividing cells and their neighbors increases the furrow ingression rate, alters topological cell packing following cytokinesis, and impairs barrier function at the furrow. Computational modeling validates our findings and provides additional insights about epithelial mechanics during cytokinesis. We conclude that forces from the cytokinetic array must be carefully balanced with restraining forces generated by neighbor cells to regulate the speed and success of cytokinesis and maintain epithelial homeostasis. [Display omitted] •Neighboring cells assemble actomyosin arrays adjacent to the cytokinetic furrow•Overexpression of an F-actin cross-linker in neighbor cells slows furrowing•Optogenetic activation of contractility in neighbors slows or disrupts cytokinesis•Junction reinforcement at the furrow supports epithelial organization and integrity Xenopus epithelial cells mechanosensitively reinforce connections to neighbor cells during cytokinesis. Here, Landino et al. show that actomyosin arrays assembled in neighbor cells restrain cytokinetic furrow closure, and modulation of neighbor cell contractility or mechanical coupling to neighbor cells leads to failed cytokinesis, altered cell packing, and impaired barrier function.