Quantitative atlas of collagen hydrogels reveals mesenchymal cancer cell traction adaptation to the matrix nanoarchitecture.

Autor: Blázquez-Carmona P; Escuela Técnica Superior de Ingeniería, Universidad de Sevilla. Avenida Camino de los Descubrimientos s/n, 41092 Sevilla, Spain; Instituto de Biomedicina de Sevilla (IBIS). C. Antonio Maura Montaner, 41013 Sevilla, Spain., Ruiz-Mateos R; Escuela Técnica Superior de Ingeniería, Universidad de Sevilla. Avenida Camino de los Descubrimientos s/n, 41092 Sevilla, Spain; Instituto de Biomedicina de Sevilla (IBIS). C. Antonio Maura Montaner, 41013 Sevilla, Spain., Barrasa-Fano J; Department of Mechanical Engineering, Biomechanics Section, KU Leuven, Celestijnenlaan 300. B-3001 Heverlee, Belgium., Shapeti A; Department of Mechanical Engineering, Biomechanics Section, KU Leuven, Celestijnenlaan 300. B-3001 Heverlee, Belgium., Martín-Alfonso JE; Escuela Técnica Superior de Ingeniería, Universidad de Huelva. Avda. de las Fuerzas Armadas s/n, 21007 Huelva, Spain., Domínguez J; Escuela Técnica Superior de Ingeniería, Universidad de Sevilla. Avenida Camino de los Descubrimientos s/n, 41092 Sevilla, Spain; Instituto de Biomedicina de Sevilla (IBIS). C. Antonio Maura Montaner, 41013 Sevilla, Spain., Van Oosterwyck H; Department of Mechanical Engineering, Biomechanics Section, KU Leuven, Celestijnenlaan 300. B-3001 Heverlee, Belgium., Reina-Romo E; Escuela Técnica Superior de Ingeniería, Universidad de Sevilla. Avenida Camino de los Descubrimientos s/n, 41092 Sevilla, Spain; Instituto de Biomedicina de Sevilla (IBIS). C. Antonio Maura Montaner, 41013 Sevilla, Spain., Sanz-Herrera JA; Escuela Técnica Superior de Ingeniería, Universidad de Sevilla. Avenida Camino de los Descubrimientos s/n, 41092 Sevilla, Spain; Instituto de Biomedicina de Sevilla (IBIS). C. Antonio Maura Montaner, 41013 Sevilla, Spain. Electronic address: jsanz@us.es.
Jazyk: angličtina
Zdroj: Acta biomaterialia [Acta Biomater] 2024 Sep 01; Vol. 185, pp. 281-295. Date of Electronic Publication: 2024 Jul 09.
DOI: 10.1016/j.actbio.2024.07.002
Abstrakt: Collagen-based hydrogels are commonly used in mechanobiology to mimic the extracellular matrix. A quantitative analysis of the influence of collagen concentration and properties on the structure and mechanics of the hydrogels is essential for tailored design adjustments for specific in vitro conditions. We combined focused ion beam scanning electron microscopy and rheology to provide a detailed quantitative atlas of the mechanical and nanoscale three-dimensional structural alterations that occur when manipulating different hydrogel's physicochemistry. Moreover, we study the effects of such alterations on the phenotype of breast cancer cells and their mechanical interactions with the extracellular matrix. Regardless of the microenvironment's pore size, porosity or mechanical properties, cancer cells are able to reach a stable mesenchymal-like morphology. Additionally, employing 3D traction force microscopy, a positive correlation between cellular tractions and ECM mechanics is observed up to a critical threshold, beyond which tractions plateau. This suggests that cancer cells in a stable mesenchymal state calibrate their mechanical interactions with the ECM to keep their migration and invasiveness capacities unaltered. STATEMENT OF SIGNIFICANCE: The paper presents a thorough study on the mechanical microenvironment in breast cancer cells during their interaction with collagen based hydrogels of different compositions. The hydrogels' microstructure were obtained using state-of-the-art 3D microscopy, namely focused ion beam-scanning electron microscope (FIB-SEM). FIB-SEM was originally applied in this work to reconstruct complex fibered collagen microstructures within the nanometer range, to obtain key microarchitectural parameters. The mechanical microenvironment of cells was recovered using Traction Force Microscopy (TFM). The obtained results suggest that cells calibrate tractions such that they depend on mechanical, microstructural and physicochemical characteristics of the hydrogels, hence revealing a steric hindrance. We hypothesize that cancer cells studied in this paper tune their mechanical state to keep their migration and invasiveness capacities unaltered.
Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
(Copyright © 2024 The Author(s). Published by Elsevier Ltd.. All rights reserved.)
Databáze: MEDLINE
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