Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices

The mechanical properties of the extracellular matrix (ECM)–a complex, 3D, fibrillar scaffold of cells in physiological environments–modulate cell behavior and can drive tissue morphogenesis, regeneration, and disease progression. For simplicity, it is often convenient to assume these properties to...

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Detalles Bibliográficos
Autores: Malandrino, Andrea, Trepat Guixer, Xavier, Kamm, Roger D., Mak, Michael
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Universidad de Barcelona
Repositorio:Dipòsit Digital de la UB
OAI Identifier:oai:diposit.ub.edu:2445/138987
Acceso en línea:https://hdl.handle.net/2445/138987
Access Level:acceso abierto
Palabra clave:Col·lagen
Citologia
Matriu extracel·lular
Collagen
Cytology
Extracellular matrix
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spelling Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matricesMalandrino, AndreaTrepat Guixer, XavierKamm, Roger D.Mak, MichaelCol·lagenCitologiaMatriu extracel·lularCollagenCytologyExtracellular matrixThe mechanical properties of the extracellular matrix (ECM)–a complex, 3D, fibrillar scaffold of cells in physiological environments–modulate cell behavior and can drive tissue morphogenesis, regeneration, and disease progression. For simplicity, it is often convenient to assume these properties to be time-invariant. In living systems, however, cells dynamically remodel the ECM and create time-dependent local microenvironments. Here, we show how cell-generated contractile forces produce substantial irreversible changes to the density and architecture of physiologically relevant ECMs–collagen I and fibrin–in a matter of minutes. We measure the 3D deformation profiles of the ECM surrounding cancer and endothelial cells during stages when force generation is active or inactive. We further correlate these ECM measurements to both discrete fiber simulations that incorporate fiber crosslink unbinding kinetics and continuum-scale simulations that account for viscoplastic and damage features. Our findings further confirm that plasticity, as a mechanical law to capture remodeling in these networks, is fundamentally tied to material damage via force-driven unbinding of fiber crosslinks. These results characterize in a multiscale manner the dynamic nature of the mechanical environment of physiologically mimicking cell-in-gel systems.Public Library of Science (PLoS)2019info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2445/138987Articles publicats en revistes (Biomedicina)reponame:Dipòsit Digital de la UBinstname:Universidad de BarcelonaInglésReproducció del document publicat a: https://doi.org/10.1371/journal.pcbi.1006684PLOS Computational Biology, 2019, vol. 15, num. 4, p. e1006684https://doi.org/10.1371/journal.pcbi.1006684info:eu-repo/grantAgreement/EC/FP7/616480cc by (c) Malandrino et al., 2019http://creativecommons.org/licenses/by/3.0/es/info:eu-repo/semantics/openAccessoai:diposit.ub.edu:2445/1389872026-05-27T06:46:51Z
dc.title.none.fl_str_mv Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
title Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
spellingShingle Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
Malandrino, Andrea
Col·lagen
Citologia
Matriu extracel·lular
Collagen
Cytology
Extracellular matrix
title_short Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
title_full Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
title_fullStr Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
title_full_unstemmed Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
title_sort Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices
dc.creator.none.fl_str_mv Malandrino, Andrea
Trepat Guixer, Xavier
Kamm, Roger D.
Mak, Michael
author Malandrino, Andrea
author_facet Malandrino, Andrea
Trepat Guixer, Xavier
Kamm, Roger D.
Mak, Michael
author_role author
author2 Trepat Guixer, Xavier
Kamm, Roger D.
Mak, Michael
author2_role author
author
author
dc.subject.none.fl_str_mv Col·lagen
Citologia
Matriu extracel·lular
Collagen
Cytology
Extracellular matrix
topic Col·lagen
Citologia
Matriu extracel·lular
Collagen
Cytology
Extracellular matrix
description The mechanical properties of the extracellular matrix (ECM)–a complex, 3D, fibrillar scaffold of cells in physiological environments–modulate cell behavior and can drive tissue morphogenesis, regeneration, and disease progression. For simplicity, it is often convenient to assume these properties to be time-invariant. In living systems, however, cells dynamically remodel the ECM and create time-dependent local microenvironments. Here, we show how cell-generated contractile forces produce substantial irreversible changes to the density and architecture of physiologically relevant ECMs–collagen I and fibrin–in a matter of minutes. We measure the 3D deformation profiles of the ECM surrounding cancer and endothelial cells during stages when force generation is active or inactive. We further correlate these ECM measurements to both discrete fiber simulations that incorporate fiber crosslink unbinding kinetics and continuum-scale simulations that account for viscoplastic and damage features. Our findings further confirm that plasticity, as a mechanical law to capture remodeling in these networks, is fundamentally tied to material damage via force-driven unbinding of fiber crosslinks. These results characterize in a multiscale manner the dynamic nature of the mechanical environment of physiologically mimicking cell-in-gel systems.
publishDate 2019
dc.date.none.fl_str_mv 2019
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/138987
url https://hdl.handle.net/2445/138987
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/10.1371/journal.pcbi.1006684
PLOS Computational Biology, 2019, vol. 15, num. 4, p. e1006684
https://doi.org/10.1371/journal.pcbi.1006684
info:eu-repo/grantAgreement/EC/FP7/616480
dc.rights.none.fl_str_mv cc by (c) Malandrino et al., 2019
http://creativecommons.org/licenses/by/3.0/es/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc by (c) Malandrino et al., 2019
http://creativecommons.org/licenses/by/3.0/es/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Public Library of Science (PLoS)
publisher.none.fl_str_mv Public Library of Science (PLoS)
dc.source.none.fl_str_mv Articles publicats en revistes (Biomedicina)
reponame:Dipòsit Digital de la UB
instname:Universidad de Barcelona
instname_str Universidad de Barcelona
reponame_str Dipòsit Digital de la UB
collection Dipòsit Digital de la UB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,300719

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