Propagation dynamics of electrotactic motility in large epithelial cell sheets

Yan Zhang; Guoqing Xu; Jiandong Wu; Rachel M Lee; Zijie Zhu; Yaohui Sun; Kan Zhu; Wolfgang Losert; Simon Liao; Gong Zhang; Tingrui Pan; Zhengping Xu; Francis Lin; Min Zhao

doi:10.1016/j.isci.2022.105136

Propagation dynamics of electrotactic motility in large epithelial cell sheets

iScience. 2022 Sep 13;25(10):105136. doi: 10.1016/j.isci.2022.105136. eCollection 2022 Oct 21.

Authors

Yan Zhang^{1

2

3

4}, Guoqing Xu^{5

6}, Jiandong Wu^{5

7}, Rachel M Lee⁸, Zijie Zhu⁴, Yaohui Sun¹, Kan Zhu¹, Wolfgang Losert^{8

9}, Simon Liao⁶, Gong Zhang^{6

10}, Tingrui Pan^{4

7

11

12

13}, Zhengping Xu³, Francis Lin^{1

5}, Min Zhao^{1

14}

Affiliations

¹ Department of Ophthalmology and Vision Science, University of California, Davis, Davis, CA 95616, USA.
² School of Public Health, Hangzhou Normal University, Hangzhou 310018, China.
³ Institute of Environmental Medicine, Zhejiang University School of Medicine, Hangzhou 310058, China.
⁴ Micro-Nano Innovations (MiNI) Laboratory, Department of Biomedical Engineering, University of California, Davis, Davis, CA 95616, USA.
⁵ Department of Physics and Astronomy, University of Manitoba, Winnipeg, MB, R3T 2N2, Canada.
⁶ Department of Applied Computer Science, University of Winnipeg, Winnipeg, MB, R3B 2E9, Canada.
⁷ Institute of Biomedical and Health Engineering, Shenzhen Institute of Advanced Technology, Shenzhen 518055, China.
⁸ Institute for Physical Science and Technology, University of Maryland, College Park, MD 20742, USA.
⁹ Department of Physics, University of Maryland, College Park, MD 20742, USA.
¹⁰ Brain Engineering Center, Anhui University, Hefei 230601, China.
¹¹ Shenzhen Engineering Laboratory of Single-molecule Detection and Instrument Development, Shenzhen, Guangdong 518055, China.
¹² Suzhou Institute for Advanced Research, University of Science and Technology of China, Suzhou 215123, China.
¹³ Department of Precision Machinery and Precision Instrumentation, University of Science and Technology of China, Hefei 230026, China.
¹⁴ Department of Dermatology, University of California, Davis, Davis, CA 95616, USA.

Abstract

Directional migration initiated at the wound edge leads epithelia to migrate in wound healing. How such coherent migration is achieved is not well understood. Here, we used electric fields to induce robust migration of sheets of human keratinocytes and developed an in silico model to characterize initiation and propagation of epithelial collective migration. Electric fields initiate an increase in migration directionality and speed at the leading edge. The increases propagate across the epithelial sheets, resulting in directional migration of cell sheets as coherent units. Both the experimental and in silico models demonstrated vector-like integration of the electric and default directional cues at free edge in space and time. The resultant collective migration is consistent in experiments and modeling, both qualitatively and quantitatively. The keratinocyte model thus faithfully reflects key features of epithelial migration as a coherent tissue in vivo, e.g. that leading cells lead, and that epithelium maintains cell-cell junction.

Keywords: Biological sciences; Cell biology; Functional aspects of cell biology; Systems biology.