Polar pattern formation induced by contact following locomotion in a multicellular system

Biophysical mechanisms underlying collective cell migration of eukaryotic cells have been studied extensively in recent years. One mechanism that induces cells to correlate their motions is contact inhibition of locomotion, by which cells migrating away from the contact site. Here, we report that ta...

Full description

Bibliographic Details
Main Authors: Masayuki Hayakawa, Tetsuya Hiraiwa, Yuko Wada, Hidekazu Kuwayama, Tatsuo Shibata
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/53609
_version_ 1811201277279862784
author Masayuki Hayakawa
Tetsuya Hiraiwa
Yuko Wada
Hidekazu Kuwayama
Tatsuo Shibata
author_facet Masayuki Hayakawa
Tetsuya Hiraiwa
Yuko Wada
Hidekazu Kuwayama
Tatsuo Shibata
author_sort Masayuki Hayakawa
collection DOAJ
description Biophysical mechanisms underlying collective cell migration of eukaryotic cells have been studied extensively in recent years. One mechanism that induces cells to correlate their motions is contact inhibition of locomotion, by which cells migrating away from the contact site. Here, we report that tail-following behavior at the contact site, termed contact following locomotion (CFL), can induce a non-trivial collective behavior in migrating cells. We show the emergence of a traveling band showing polar order in a mutant Dictyostelium cell that lacks chemotactic activity. We find that CFL is the cell–cell interaction underlying this phenomenon, enabling a theoretical description of how this traveling band forms. We further show that the polar order phase consists of subpopulations that exhibit characteristic transversal motions with respect to the direction of band propagation. These findings describe a novel mechanism of collective cell migration involving cell–cell interactions capable of inducing traveling band with polar order.
first_indexed 2024-04-12T02:19:24Z
format Article
id doaj.art-ca1642cacbc745ec8ff1e566a92cb3d9
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T02:19:24Z
publishDate 2020-04-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-ca1642cacbc745ec8ff1e566a92cb3d92022-12-22T03:52:11ZengeLife Sciences Publications LtdeLife2050-084X2020-04-01910.7554/eLife.53609Polar pattern formation induced by contact following locomotion in a multicellular systemMasayuki Hayakawa0https://orcid.org/0000-0002-9245-9593Tetsuya Hiraiwa1https://orcid.org/0000-0003-3221-345XYuko Wada2Hidekazu Kuwayama3https://orcid.org/0000-0002-4362-0790Tatsuo Shibata4https://orcid.org/0000-0002-9294-9998Laboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanMechanobiology Institute, National University of Singapore, Singapore, Singapore; Universal Biology Institute, University of Tokyo, Tokyo, JapanLaboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanFaculty of Life and Environmental Sciences, University of Tsukuba, Tennodai, Ibaraki, JapanLaboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanBiophysical mechanisms underlying collective cell migration of eukaryotic cells have been studied extensively in recent years. One mechanism that induces cells to correlate their motions is contact inhibition of locomotion, by which cells migrating away from the contact site. Here, we report that tail-following behavior at the contact site, termed contact following locomotion (CFL), can induce a non-trivial collective behavior in migrating cells. We show the emergence of a traveling band showing polar order in a mutant Dictyostelium cell that lacks chemotactic activity. We find that CFL is the cell–cell interaction underlying this phenomenon, enabling a theoretical description of how this traveling band forms. We further show that the polar order phase consists of subpopulations that exhibit characteristic transversal motions with respect to the direction of band propagation. These findings describe a novel mechanism of collective cell migration involving cell–cell interactions capable of inducing traveling band with polar order.https://elifesciences.org/articles/53609collective cell migrationself-propelled particlescell-cell contactcell migration
spellingShingle Masayuki Hayakawa
Tetsuya Hiraiwa
Yuko Wada
Hidekazu Kuwayama
Tatsuo Shibata
Polar pattern formation induced by contact following locomotion in a multicellular system
eLife
collective cell migration
self-propelled particles
cell-cell contact
cell migration
title Polar pattern formation induced by contact following locomotion in a multicellular system
title_full Polar pattern formation induced by contact following locomotion in a multicellular system
title_fullStr Polar pattern formation induced by contact following locomotion in a multicellular system
title_full_unstemmed Polar pattern formation induced by contact following locomotion in a multicellular system
title_short Polar pattern formation induced by contact following locomotion in a multicellular system
title_sort polar pattern formation induced by contact following locomotion in a multicellular system
topic collective cell migration
self-propelled particles
cell-cell contact
cell migration
url https://elifesciences.org/articles/53609
work_keys_str_mv AT masayukihayakawa polarpatternformationinducedbycontactfollowinglocomotioninamulticellularsystem
AT tetsuyahiraiwa polarpatternformationinducedbycontactfollowinglocomotioninamulticellularsystem
AT yukowada polarpatternformationinducedbycontactfollowinglocomotioninamulticellularsystem
AT hidekazukuwayama polarpatternformationinducedbycontactfollowinglocomotioninamulticellularsystem
AT tatsuoshibata polarpatternformationinducedbycontactfollowinglocomotioninamulticellularsystem