Electric field-guided collective motility initiation of large epidermal cell groups

• Type of Material: Article
• Authors: Yaohui Sun, University of California, Davis, Sacramento; Brian Reid, University of California, Davis, Sacramento; Yan Zhang, University of California, Davis, Sacramento; Kan Zhu, University of California, Davis, Sacramento; Fernando Ferreira, University of California, Davis, Sacramento; Alejandro Estrada, University of California, Davis, Sacramento; Yuxin Sun, University of California, Davis, Sacramento; Bruce W Draper, University of California Davis; Haicen Yue, Emory University; Calina Copos, Northeastern University; Francis Lin, University of Manitoba; Yelena Y Bernadskaya, New York University; Min Zhao, University of California, Davis, Sacramento; Alex Mogilner, New York University
• Language: English
• Date: 2023-05-01
• Publisher: AMER SOC CELL BIOLOGY
• Publication Version: Final Published Version
• Copyright Statement: © 2023 Sun et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
• License: Creative Commons Attribution-ShareAlike 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1091/mbc.E22-09-0391
• Title of Journal or Parent Work: MOLECULAR BIOLOGY OF THE CELL
• Volume: 34
• Issue: 5
• Start Page: ar48
• End Page: ar48
• Keywords: Cell Biology; Science & Technology; Life Sciences & Biomedicine
• Research Categories: Health Sciences, Opthamology; Health Sciences, Radiology

Abstract

Recent research has elucidated mechanochemical pathways of single cell polarization, but much less is known about collective motility initiation in adhesive cell groups. We used galvanotactic assays of zebrafish keratocyte cell groups, pharmacological perturbations, electric field switches, particle imaging velocimetry, and cell tracking to show that large cell groups initiate motility in minutes toward the cathode. Interestingly, while PI3K-inhibited single cells are biased toward the anode, inhibiting PI3K does not affect the cathode-directed cell group migration. We observed that control groups had the fastest cathode-migrating cell at the front, while the front cells in PI3K-inhibited groups were the slowest. Both control and PI3K-inhibited groups rapidly repolarized when the electric field direction was reversed, and the group migration continued after the electric field was switched off. Inhibiting myosin disrupted the cohesiveness of keratocyte groups and abolished the collective directionality and ability to switch direction when the electric field is reversed. Our data are consistent with a model according to which cells in the group sense the electric field individually and mechanical integration of the cells results in coherent group motility.