Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues

Cell neighbor exchanges are integral to tissue rearrangements in biology, including development and repair. Often, these processes occur via topological T1 transitions analogous to those observed in foams, grains, and colloids. However, in contrast to those in nonliving materials, the T1 transitions...

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Autores principales: Amit Das, Srikanth Sastry, Dapeng Bi
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Publicado: American Physical Society 2021
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spelling oai:doaj.org-article:8741d34c8e97483abc1228dafbf4c1042021-11-22T17:24:07ZControlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues10.1103/PhysRevX.11.0410372160-3308https://doaj.org/article/8741d34c8e97483abc1228dafbf4c1042021-11-01T00:00:00Zhttp://doi.org/10.1103/PhysRevX.11.041037http://doi.org/10.1103/PhysRevX.11.041037https://doaj.org/toc/2160-3308Cell neighbor exchanges are integral to tissue rearrangements in biology, including development and repair. Often, these processes occur via topological T1 transitions analogous to those observed in foams, grains, and colloids. However, in contrast to those in nonliving materials, the T1 transitions in biological tissues are rate limited and cannot occur instantaneously due to the finite time required to remodel complex structures at cell-cell junctions. Here, we study how this rate-limiting process affects the mechanics and collective behavior of cells in a tissue by introducing this important biological constraint in a theoretical vertex-based model as an intrinsic single-cell property. We report that, in the absence of this time constraint, the tissue undergoes a glass transition with lowering of cell motility characterized by a sharp increase in the intermittency of cell-cell rearrangements. Remarkably, this glass transition disappears, as T1 transitions are temporally limited. As a unique consequence of limited rearrangements, we also find that the tissue develops spatially correlated populations of fast and slow cells, in which the fast cells organize into streamlike patterns and maintain optimally stable cell-cell contacts. The predictions of this work are compared with existing in vivo experiments in Drosophila pupal development.Amit DasSrikanth SastryDapeng BiAmerican Physical SocietyarticlePhysicsQC1-999ENPhysical Review X, Vol 11, Iss 4, p 041037 (2021)
institution DOAJ
collection DOAJ
language EN
topic Physics
QC1-999
spellingShingle Physics
QC1-999
Amit Das
Srikanth Sastry
Dapeng Bi
Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues
description Cell neighbor exchanges are integral to tissue rearrangements in biology, including development and repair. Often, these processes occur via topological T1 transitions analogous to those observed in foams, grains, and colloids. However, in contrast to those in nonliving materials, the T1 transitions in biological tissues are rate limited and cannot occur instantaneously due to the finite time required to remodel complex structures at cell-cell junctions. Here, we study how this rate-limiting process affects the mechanics and collective behavior of cells in a tissue by introducing this important biological constraint in a theoretical vertex-based model as an intrinsic single-cell property. We report that, in the absence of this time constraint, the tissue undergoes a glass transition with lowering of cell motility characterized by a sharp increase in the intermittency of cell-cell rearrangements. Remarkably, this glass transition disappears, as T1 transitions are temporally limited. As a unique consequence of limited rearrangements, we also find that the tissue develops spatially correlated populations of fast and slow cells, in which the fast cells organize into streamlike patterns and maintain optimally stable cell-cell contacts. The predictions of this work are compared with existing in vivo experiments in Drosophila pupal development.
format article
author Amit Das
Srikanth Sastry
Dapeng Bi
author_facet Amit Das
Srikanth Sastry
Dapeng Bi
author_sort Amit Das
title Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues
title_short Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues
title_full Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues
title_fullStr Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues
title_full_unstemmed Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues
title_sort controlled neighbor exchanges drive glassy behavior, intermittency, and cell streaming in epithelial tissues
publisher American Physical Society
publishDate 2021
url https://doaj.org/article/8741d34c8e97483abc1228dafbf4c104
work_keys_str_mv AT amitdas controlledneighborexchangesdriveglassybehaviorintermittencyandcellstreaminginepithelialtissues
AT srikanthsastry controlledneighborexchangesdriveglassybehaviorintermittencyandcellstreaminginepithelialtissues
AT dapengbi controlledneighborexchangesdriveglassybehaviorintermittencyandcellstreaminginepithelialtissues
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