Collective Cell Migration on Collagen-I Networks: The Impact of Matrix Viscoelasticity

Collective cell migration on extracellular matrix (ECM) networks is a key biological process involved in development, tissue homeostasis and diseases such as metastatic cancer. During invasion of epithelial cancers, cell clusters migrate through the surrounding stroma, which is comprised primarily o...

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Main Authors: Ivana Pajic-Lijakovic, Milan Milivojevic, Andrew G. Clark
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2022.901026/full
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author Ivana Pajic-Lijakovic
Milan Milivojevic
Andrew G. Clark
Andrew G. Clark
Andrew G. Clark
author_facet Ivana Pajic-Lijakovic
Milan Milivojevic
Andrew G. Clark
Andrew G. Clark
Andrew G. Clark
author_sort Ivana Pajic-Lijakovic
collection DOAJ
description Collective cell migration on extracellular matrix (ECM) networks is a key biological process involved in development, tissue homeostasis and diseases such as metastatic cancer. During invasion of epithelial cancers, cell clusters migrate through the surrounding stroma, which is comprised primarily of networks of collagen-I fibers. There is growing evidence that the rheological and topological properties of collagen networks can impact cell behavior and cell migration dynamics. During migration, cells exert mechanical forces on their substrate, resulting in an active remodeling of ECM networks that depends not only on the forces produced, but also on the molecular mechanisms that dictate network rheology. One aspect of collagen network rheology whose role is emerging as a crucial parameter in dictating cell behavior is network viscoelasticity. Dynamic reorganization of ECM networks can induce local changes in network organization and mechanics, which can further feed back on cell migration dynamics and cell-cell rearrangement. A number of studies, including many recent publications, have investigated the mechanisms underlying structural changes to collagen networks in response to mechanical force as well as the role of collagen rheology and topology in regulating cell behavior. In this mini-review, we explore the cause-consequence relationship between collagen network viscoelasticity and cell rearrangements at various spatiotemporal scales. We focus on structural alterations of collagen-I networks during collective cell migration and discuss the main rheological parameters, and in particular the role of viscoelasticity, which can contribute to local matrix stiffening during cell movement and can elicit changes in cell dynamics.
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spelling doaj.art-800414b9e27941a38046f1ec8f2d95b42022-12-22T02:43:50ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-07-011010.3389/fcell.2022.901026901026Collective Cell Migration on Collagen-I Networks: The Impact of Matrix ViscoelasticityIvana Pajic-Lijakovic0Milan Milivojevic1Andrew G. Clark2Andrew G. Clark3Andrew G. Clark4University of Belgrade, Faculty of Technology and Metallurgy, Belgrade, SerbiaUniversity of Belgrade, Faculty of Technology and Metallurgy, Belgrade, SerbiaUniversity of Stuttgart, Institute of Cell Biology and Immunology, Stuttgart, GermanyUniversity of Stuttgart, Stuttgart Research Center Systems Biology, Stuttgart, GermanyUniversity of Tübingen, Center for Personalized Medicine, Tübingen, GermanyCollective cell migration on extracellular matrix (ECM) networks is a key biological process involved in development, tissue homeostasis and diseases such as metastatic cancer. During invasion of epithelial cancers, cell clusters migrate through the surrounding stroma, which is comprised primarily of networks of collagen-I fibers. There is growing evidence that the rheological and topological properties of collagen networks can impact cell behavior and cell migration dynamics. During migration, cells exert mechanical forces on their substrate, resulting in an active remodeling of ECM networks that depends not only on the forces produced, but also on the molecular mechanisms that dictate network rheology. One aspect of collagen network rheology whose role is emerging as a crucial parameter in dictating cell behavior is network viscoelasticity. Dynamic reorganization of ECM networks can induce local changes in network organization and mechanics, which can further feed back on cell migration dynamics and cell-cell rearrangement. A number of studies, including many recent publications, have investigated the mechanisms underlying structural changes to collagen networks in response to mechanical force as well as the role of collagen rheology and topology in regulating cell behavior. In this mini-review, we explore the cause-consequence relationship between collagen network viscoelasticity and cell rearrangements at various spatiotemporal scales. We focus on structural alterations of collagen-I networks during collective cell migration and discuss the main rheological parameters, and in particular the role of viscoelasticity, which can contribute to local matrix stiffening during cell movement and can elicit changes in cell dynamics.https://www.frontiersin.org/articles/10.3389/fcell.2022.901026/fullextracellular matrixviscoelasticitycell rearrangementmatrix remodelingresidual stress accumulationcollective cell migration
spellingShingle Ivana Pajic-Lijakovic
Milan Milivojevic
Andrew G. Clark
Andrew G. Clark
Andrew G. Clark
Collective Cell Migration on Collagen-I Networks: The Impact of Matrix Viscoelasticity
Frontiers in Cell and Developmental Biology
extracellular matrix
viscoelasticity
cell rearrangement
matrix remodeling
residual stress accumulation
collective cell migration
title Collective Cell Migration on Collagen-I Networks: The Impact of Matrix Viscoelasticity
title_full Collective Cell Migration on Collagen-I Networks: The Impact of Matrix Viscoelasticity
title_fullStr Collective Cell Migration on Collagen-I Networks: The Impact of Matrix Viscoelasticity
title_full_unstemmed Collective Cell Migration on Collagen-I Networks: The Impact of Matrix Viscoelasticity
title_short Collective Cell Migration on Collagen-I Networks: The Impact of Matrix Viscoelasticity
title_sort collective cell migration on collagen i networks the impact of matrix viscoelasticity
topic extracellular matrix
viscoelasticity
cell rearrangement
matrix remodeling
residual stress accumulation
collective cell migration
url https://www.frontiersin.org/articles/10.3389/fcell.2022.901026/full
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AT andrewgclark collectivecellmigrationoncollageninetworkstheimpactofmatrixviscoelasticity
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