Cell response to extracellular matrix viscous energy dissipation outweighs high-rigidity sensing

The mechanics of the extracellular matrix (ECM) determine cell activity and fate through mechanoresponsive proteins including Yes-associated protein 1 (YAP). Rigidity and viscous relaxation have emerged as the main mechanical properties of the ECM steering cell behavior. However, how cells integrate...

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Detalhes bibliográficos
Autores: Huerta Lopez, Carla, Clemente Manteca, Alejandro, Velazquez Carreras, Diana, Espinosa, Francisco M., García Sánchez, Juan, Martinez del Pozo, Álvaro, Garcia Garcia, Maria, Martin Colomo, Sara, Rodríguez Blanco, Andrea, Esteban González, Ricardo, Martín Zamora, Francisco M., Sáez Viñas, Pablo|||0000-0002-9253-0417
Formato: artículo
Fecha de publicación:2024
País:España
Recursos:Universitat Politècnica de Catalunya (UPC)
Repositorio:UPCommons. Portal del coneixement obert de la UPC
Idioma:inglés
OAI Identifier:oai:upcommons.upc.edu:2117/420796
Acesso em linha:https://hdl.handle.net/2117/420796
https://dx.doi.org/10.1126/sciadv.adf9758
Access Level:acceso abierto
Palavra-chave:Numerical analysis--Simulation methods
Biomathematics
Anàlisi numèrica
Biomatemàtica
Classificació AMS::65 Numerical analysis::65C Probabilistic methods, simulation and stochastic differential equations
Classificació AMS::92 Biology and other natural sciences::92B Mathematical biology in general
Àrees temàtiques de la UPC::Matemàtiques i estadística::Anàlisi numèrica
Àrees temàtiques de la UPC::Matemàtiques i estadística::Matemàtica aplicada a les ciències
Descrição
Resumo:The mechanics of the extracellular matrix (ECM) determine cell activity and fate through mechanoresponsive proteins including Yes-associated protein 1 (YAP). Rigidity and viscous relaxation have emerged as the main mechanical properties of the ECM steering cell behavior. However, how cells integrate coexisting ECM rigidity and viscosity cues remains poorly understood, particularly in the high-stiffness regime. Here, we have exploited engineered stiff viscoelastic protein hydrogels to show that, contrary to current models of cell-ECM interaction, substrate viscous energy dissipation attenuates mechanosensing even when cells are exposed to higher effective rigidity. This unexpected behavior is however readily captured by a pull-and-hold model of molecular clutch–based cell mechanosensing, which also recapitulates opposite cellular response at low rigidities. Consistent with predictions of the pull-and-hold model, we find that myosin inhibition can boost mechanosensing on cells cultured on dissipative matrices. Together, our work provides general mechanistic understanding on how cells respond to the viscoelastic properties of the ECM.