Collective cell migration has distinct directionality and speed dynamics

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

Research output: Contribution to journalArticle

Abstract

When a constraint is removed, confluent cells migrate directionally into the available space. How the migration directionality and speed increase are initiated at the leading edge and propagate into neighboring cells are not well understood. Using a quantitative visualization technique—Particle Image Velocimetry (PIV)—we revealed that migration directionality and speed had strikingly different dynamics. Migration directionality increases as a wave propagating from the leading edge into the cell sheet, while the increase in cell migration speed is maintained only at the leading edge. The overall directionality steadily increases with time as cells migrate into the cell-free space, but migration speed remains largely the same. A particle-based compass (PBC) model suggests cellular interplay (which depends on cell–cell distance) and migration speed are sufficient to capture the dynamics of migration directionality revealed experimentally. Extracellular Ca2+ regulated both migration speed and directionality, but in a significantly different way, suggested by the correlation between directionality and speed only in some dynamic ranges. Our experimental and modeling results reveal distinct directionality and speed dynamics in collective migration, and these factors can be regulated by extracellular Ca2+ through cellular interplay. Quantitative visualization using PIV and our PBC model thus provide a powerful approach to dissect the mechanisms of collective cell migration.

Original languageEnglish (US)
Pages (from-to)1-10
Number of pages10
JournalCellular and Molecular Life Sciences
DOIs
StateAccepted/In press - Jun 13 2017

Fingerprint

Cell Movement
Rheology

Keywords

  • Blebbistatin
  • Cell communication
  • Cell contractility
  • Corneal epithelial cell
  • PDMS
  • Wound healing

ASJC Scopus subject areas

  • Molecular Medicine
  • Molecular Biology
  • Pharmacology
  • Cellular and Molecular Neuroscience
  • Cell Biology

Cite this

Zhang, Y., Xu, G., Lee, R. M., Zhu, Z., Wu, J., Liao, S., ... Zhao, M. (Accepted/In press). Collective cell migration has distinct directionality and speed dynamics. Cellular and Molecular Life Sciences, 1-10. https://doi.org/10.1007/s00018-017-2553-6

Collective cell migration has distinct directionality and speed dynamics. / Zhang, Yan; Xu, Guoqing; Lee, Rachel M.; Zhu, Zijie; Wu, Jiandong; Liao, Simon; Zhang, Gong; Sun, Yaohui; Mogilner, Alexander; Losert, Wolfgang; Pan, Tingrui; Lin, Francis; Xu, Zhengping; Zhao, Min.

In: Cellular and Molecular Life Sciences, 13.06.2017, p. 1-10.

Research output: Contribution to journalArticle

Zhang, Y, Xu, G, Lee, RM, Zhu, Z, Wu, J, Liao, S, Zhang, G, Sun, Y, Mogilner, A, Losert, W, Pan, T, Lin, F, Xu, Z & Zhao, M 2017, 'Collective cell migration has distinct directionality and speed dynamics', Cellular and Molecular Life Sciences, pp. 1-10. https://doi.org/10.1007/s00018-017-2553-6
Zhang, Yan ; Xu, Guoqing ; Lee, Rachel M. ; Zhu, Zijie ; Wu, Jiandong ; Liao, Simon ; Zhang, Gong ; Sun, Yaohui ; Mogilner, Alexander ; Losert, Wolfgang ; Pan, Tingrui ; Lin, Francis ; Xu, Zhengping ; Zhao, Min. / Collective cell migration has distinct directionality and speed dynamics. In: Cellular and Molecular Life Sciences. 2017 ; pp. 1-10.
@article{4a017d2c09bb44efb83ef2f3ba70e8a0,
title = "Collective cell migration has distinct directionality and speed dynamics",
abstract = "When a constraint is removed, confluent cells migrate directionally into the available space. How the migration directionality and speed increase are initiated at the leading edge and propagate into neighboring cells are not well understood. Using a quantitative visualization technique—Particle Image Velocimetry (PIV)—we revealed that migration directionality and speed had strikingly different dynamics. Migration directionality increases as a wave propagating from the leading edge into the cell sheet, while the increase in cell migration speed is maintained only at the leading edge. The overall directionality steadily increases with time as cells migrate into the cell-free space, but migration speed remains largely the same. A particle-based compass (PBC) model suggests cellular interplay (which depends on cell–cell distance) and migration speed are sufficient to capture the dynamics of migration directionality revealed experimentally. Extracellular Ca2+ regulated both migration speed and directionality, but in a significantly different way, suggested by the correlation between directionality and speed only in some dynamic ranges. Our experimental and modeling results reveal distinct directionality and speed dynamics in collective migration, and these factors can be regulated by extracellular Ca2+ through cellular interplay. Quantitative visualization using PIV and our PBC model thus provide a powerful approach to dissect the mechanisms of collective cell migration.",
keywords = "Blebbistatin, Cell communication, Cell contractility, Corneal epithelial cell, PDMS, Wound healing",
author = "Yan Zhang and Guoqing Xu and Lee, {Rachel M.} and Zijie Zhu and Jiandong Wu and Simon Liao and Gong Zhang and Yaohui Sun and Alexander Mogilner and Wolfgang Losert and Tingrui Pan and Francis Lin and Zhengping Xu and Min Zhao",
year = "2017",
month = "6",
day = "13",
doi = "10.1007/s00018-017-2553-6",
language = "English (US)",
pages = "1--10",
journal = "Cellular and Molecular Life Sciences",
issn = "1420-682X",
publisher = "Birkhauser Verlag Basel",

}

TY - JOUR

T1 - Collective cell migration has distinct directionality and speed dynamics

AU - Zhang, Yan

AU - Xu, Guoqing

AU - Lee, Rachel M.

AU - Zhu, Zijie

AU - Wu, Jiandong

AU - Liao, Simon

AU - Zhang, Gong

AU - Sun, Yaohui

AU - Mogilner, Alexander

AU - Losert, Wolfgang

AU - Pan, Tingrui

AU - Lin, Francis

AU - Xu, Zhengping

AU - Zhao, Min

PY - 2017/6/13

Y1 - 2017/6/13

N2 - When a constraint is removed, confluent cells migrate directionally into the available space. How the migration directionality and speed increase are initiated at the leading edge and propagate into neighboring cells are not well understood. Using a quantitative visualization technique—Particle Image Velocimetry (PIV)—we revealed that migration directionality and speed had strikingly different dynamics. Migration directionality increases as a wave propagating from the leading edge into the cell sheet, while the increase in cell migration speed is maintained only at the leading edge. The overall directionality steadily increases with time as cells migrate into the cell-free space, but migration speed remains largely the same. A particle-based compass (PBC) model suggests cellular interplay (which depends on cell–cell distance) and migration speed are sufficient to capture the dynamics of migration directionality revealed experimentally. Extracellular Ca2+ regulated both migration speed and directionality, but in a significantly different way, suggested by the correlation between directionality and speed only in some dynamic ranges. Our experimental and modeling results reveal distinct directionality and speed dynamics in collective migration, and these factors can be regulated by extracellular Ca2+ through cellular interplay. Quantitative visualization using PIV and our PBC model thus provide a powerful approach to dissect the mechanisms of collective cell migration.

AB - When a constraint is removed, confluent cells migrate directionally into the available space. How the migration directionality and speed increase are initiated at the leading edge and propagate into neighboring cells are not well understood. Using a quantitative visualization technique—Particle Image Velocimetry (PIV)—we revealed that migration directionality and speed had strikingly different dynamics. Migration directionality increases as a wave propagating from the leading edge into the cell sheet, while the increase in cell migration speed is maintained only at the leading edge. The overall directionality steadily increases with time as cells migrate into the cell-free space, but migration speed remains largely the same. A particle-based compass (PBC) model suggests cellular interplay (which depends on cell–cell distance) and migration speed are sufficient to capture the dynamics of migration directionality revealed experimentally. Extracellular Ca2+ regulated both migration speed and directionality, but in a significantly different way, suggested by the correlation between directionality and speed only in some dynamic ranges. Our experimental and modeling results reveal distinct directionality and speed dynamics in collective migration, and these factors can be regulated by extracellular Ca2+ through cellular interplay. Quantitative visualization using PIV and our PBC model thus provide a powerful approach to dissect the mechanisms of collective cell migration.

KW - Blebbistatin

KW - Cell communication

KW - Cell contractility

KW - Corneal epithelial cell

KW - PDMS

KW - Wound healing

UR - http://www.scopus.com/inward/record.url?scp=85020722165&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85020722165&partnerID=8YFLogxK

U2 - 10.1007/s00018-017-2553-6

DO - 10.1007/s00018-017-2553-6

M3 - Article

SP - 1

EP - 10

JO - Cellular and Molecular Life Sciences

JF - Cellular and Molecular Life Sciences

SN - 1420-682X

ER -