Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix

© The Author(s) 2024

Detalhes bibliográficos
Autores: Apolinar Fernández, Alejandro, Barrasa Fano, Jorge, Van Oosterwyck, Hans, Sanz Herrera, José Antonio
Tipo de documento: artigo
Estado:Versão publicada
Data de publicação:2024
País:España
Recursos:Universidad de Sevilla (US)
Repositório:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/164504
Acesso em linha:https://hdl.handle.net/11441/164504
https://doi.org/10.1007/s00366-024-02017-8
Access Level:Acceso aberto
Palavra-chave:Computational mechanics
Finite element method
Mechanobiology
Metalloproteinase-induced ECM degradation
Nonlinear mechanics
Traction force microscopy
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spelling Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrixApolinar Fernández, AlejandroBarrasa Fano, JorgeVan Oosterwyck, HansSanz Herrera, José AntonioComputational mechanicsFinite element methodMechanobiologyMetalloproteinase-induced ECM degradationNonlinear mechanicsTraction force microscopy© The Author(s) 20243D Traction Force Microscopy (3DTFM) constitutes a powerful methodology that enables the computation of realistic forces exerted by cells on the surrounding extracellular matrix (ECM). The ECM is characterized by its highly dynamic structure, which is constantly remodeled in order to regulate most basic cellular functions and processes. Certain pathological processes, such as cancer and metastasis, alter the way the ECM is remodeled. In particular, cancer cells are able to invade its surrounding tissue by the secretion of metalloproteinases that degrade the extracellular matrix to move and migrate towards different tissues, inducing ECM heterogeneity. Typically, 3DTFM studies neglect such heterogeneity and assume homogeneous ECM properties, which can lead to inaccuracies in traction reconstruction. Some studies have implemented ECM degradation models into 3DTFM, but the associated degradation maps are defined in an ad hoc manner. In this paper, we present a novel multiphysics approach to 3DTFM with evolving mechanical properties of the ECM. Our modeling considers a system of partial differential equations based on the mechanisms of activation of diffusive metalloproteinase MMP2 by membrane-bound metalloproteinase MT1-MMP. The obtained ECM density maps in an ECM-mimicking hydrogel are then used to compute the heterogeneous mechanical properties of the hydrogel through a multiscale approach. We perform forward and inverse TFM simulations both accounting for and omitting degradation, and results are compared to ground truth reference solutions in which degradation is considered. The main conclusions resulting from the study are: (i) the inverse methodology yields results that are significantly more accurate than those provided by the forward methodology; (ii) ignoring ECM degradation results in a considerable overestimation of tractions and non negligible errors in all analyzed casesSpringerMecánica de Medios Continuos y Teoría de EstructurasMinisterio de Ciencia e Innovación (MICIN). EspañaJunta de Andalucía2024info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/11441/164504https://doi.org/10.1007/s00366-024-02017-8reponame:idUS. Depósito de Investigación de la Universidad de Sevillainstname:Universidad de Sevilla (US)InglésEngineering with Computers.PID2021-126051OB-C42https://link.springer.com/article/10.1007/s00366-024-02017-8info:eu-repo/semantics/openAccessoai:idus.us.es:11441/1645042026-06-17T12:51:07Z
dc.title.none.fl_str_mv Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
title Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
spellingShingle Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
Apolinar Fernández, Alejandro
Computational mechanics
Finite element method
Mechanobiology
Metalloproteinase-induced ECM degradation
Nonlinear mechanics
Traction force microscopy
title_short Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
title_full Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
title_fullStr Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
title_full_unstemmed Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
title_sort Multiphysics modeling of 3D traction force microscopy with application to cancer cell-induced degradation of the extracellular matrix
dc.creator.none.fl_str_mv Apolinar Fernández, Alejandro
Barrasa Fano, Jorge
Van Oosterwyck, Hans
Sanz Herrera, José Antonio
author Apolinar Fernández, Alejandro
author_facet Apolinar Fernández, Alejandro
Barrasa Fano, Jorge
Van Oosterwyck, Hans
Sanz Herrera, José Antonio
author_role author
author2 Barrasa Fano, Jorge
Van Oosterwyck, Hans
Sanz Herrera, José Antonio
author2_role author
author
author
dc.contributor.none.fl_str_mv Mecánica de Medios Continuos y Teoría de Estructuras
Ministerio de Ciencia e Innovación (MICIN). España
Junta de Andalucía
dc.subject.none.fl_str_mv Computational mechanics
Finite element method
Mechanobiology
Metalloproteinase-induced ECM degradation
Nonlinear mechanics
Traction force microscopy
topic Computational mechanics
Finite element method
Mechanobiology
Metalloproteinase-induced ECM degradation
Nonlinear mechanics
Traction force microscopy
description © The Author(s) 2024
publishDate 2024
dc.date.none.fl_str_mv 2024
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/11441/164504
https://doi.org/10.1007/s00366-024-02017-8
url https://hdl.handle.net/11441/164504
https://doi.org/10.1007/s00366-024-02017-8
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Engineering with Computers.
PID2021-126051OB-C42
https://link.springer.com/article/10.1007/s00366-024-02017-8
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
dc.source.none.fl_str_mv reponame:idUS. Depósito de Investigación de la Universidad de Sevilla
instname:Universidad de Sevilla (US)
instname_str Universidad de Sevilla (US)
reponame_str idUS. Depósito de Investigación de la Universidad de Sevilla
collection idUS. Depósito de Investigación de la Universidad de Sevilla
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,811543

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