The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanics

The progression of tumors is heavily influenced by mechanical properties of their microenvironment. In this work, we applied micropatterned models with varying distances and shapes to investigate the differences between metastatic MDA-MB-231 and non-metastatic MCF-7 breast cancer cells in reconfigur...

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Main Authors: Mingxing Ouyang, Weihui Chen, Ting Zhou, Hongjie Liu, Lei Liu, Bing Bu, Linhong Deng
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Mechanobiology in Medicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2949907025000014
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author Mingxing Ouyang
Weihui Chen
Ting Zhou
Hongjie Liu
Lei Liu
Bing Bu
Linhong Deng
author_facet Mingxing Ouyang
Weihui Chen
Ting Zhou
Hongjie Liu
Lei Liu
Bing Bu
Linhong Deng
author_sort Mingxing Ouyang
collection DOAJ
description The progression of tumors is heavily influenced by mechanical properties of their microenvironment. In this work, we applied micropatterned models with varying distances and shapes to investigate the differences between metastatic MDA-MB-231 and non-metastatic MCF-7 breast cancer cells in reconfiguring extracellular matrix to promote cell migration induced by cell mechanics. Both cancer cells were able to rearrange type I collagen (COL) to form fibre threads, in which MDA-MB-231 consistently migrated more rapidly than MCF-7, ranging from geometrical square arrays with different spacings to complex polygonal models. MDA-MB-231 displayed higher capability of reorganizing fibre bundles at longer distance (800 ​μm). Further looking for differences in cell molecular mechanisms, siRNA knockdown inhibiting either integrin β1 or Piezo1 decreased fibre assembly and reduced the difference in COL remodeling and migration between two cancer cells. MDA-MB-231 showed inhibited migration with integrin knockdown, whereas scattering migration with Piezo1 knockdown, indicating cells losing directional mechanosensation. After inhibiting junctional E-cadherin with siRNA, MCF-7 cells migrated faster, resulting in reduced difference in comparison to MDA-MB-231 that didn't express E-cadherin. In summary, this work has explored the biomechanical differences between metastatic and non-metastatic breast cancer cells regarding COL fibre matrix remodeling and cell movements. The significant differences in E-cadherin expression in the two breast cancer cells had an effect on cell migrations. The results of this study provide research approaches for evaluating therapeutic effort on breast cancer.
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spelling doaj-art-c4925b10326f41d5ab182de5a2e8152c2025-08-20T03:30:39ZengElsevierMechanobiology in Medicine2949-90702025-06-013210011310.1016/j.mbm.2025.100113The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanicsMingxing Ouyang0Weihui Chen1Ting Zhou2Hongjie Liu3Lei Liu4Bing Bu5Linhong Deng6Institute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University, Changzhou, 213164 China; Corresponding author. Institute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University 1 Gehu Rd, Wujin District, Changzhou, 213164 China.Institute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University, Changzhou, 213164 China; School of Pharmacy, Changzhou University, Changzhou, 213164 ChinaInstitute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University, Changzhou, 213164 ChinaInstitute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University, Changzhou, 213164 China; School of Pharmacy, Changzhou University, Changzhou, 213164 ChinaInstitute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University, Changzhou, 213164 ChinaInstitute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University, Changzhou, 213164 ChinaInstitute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University, Changzhou, 213164 China; Corresponding author. Founding Director Institute of Biomedical Engineering and Health Sciences, School of Medical and Health Engineering, Changzhou University 1 Gehu Rd, Wujin District, Changzhou, Jiangsu Province 213164 China.The progression of tumors is heavily influenced by mechanical properties of their microenvironment. In this work, we applied micropatterned models with varying distances and shapes to investigate the differences between metastatic MDA-MB-231 and non-metastatic MCF-7 breast cancer cells in reconfiguring extracellular matrix to promote cell migration induced by cell mechanics. Both cancer cells were able to rearrange type I collagen (COL) to form fibre threads, in which MDA-MB-231 consistently migrated more rapidly than MCF-7, ranging from geometrical square arrays with different spacings to complex polygonal models. MDA-MB-231 displayed higher capability of reorganizing fibre bundles at longer distance (800 ​μm). Further looking for differences in cell molecular mechanisms, siRNA knockdown inhibiting either integrin β1 or Piezo1 decreased fibre assembly and reduced the difference in COL remodeling and migration between two cancer cells. MDA-MB-231 showed inhibited migration with integrin knockdown, whereas scattering migration with Piezo1 knockdown, indicating cells losing directional mechanosensation. After inhibiting junctional E-cadherin with siRNA, MCF-7 cells migrated faster, resulting in reduced difference in comparison to MDA-MB-231 that didn't express E-cadherin. In summary, this work has explored the biomechanical differences between metastatic and non-metastatic breast cancer cells regarding COL fibre matrix remodeling and cell movements. The significant differences in E-cadherin expression in the two breast cancer cells had an effect on cell migrations. The results of this study provide research approaches for evaluating therapeutic effort on breast cancer.http://www.sciencedirect.com/science/article/pii/S2949907025000014Cancer metastasisMatrix remodelingMechanical communicationIntegrinPiezoE-Cadherin
spellingShingle Mingxing Ouyang
Weihui Chen
Ting Zhou
Hongjie Liu
Lei Liu
Bing Bu
Linhong Deng
The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanics
Mechanobiology in Medicine
Cancer metastasis
Matrix remodeling
Mechanical communication
Integrin
Piezo
E-Cadherin
title The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanics
title_full The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanics
title_fullStr The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanics
title_full_unstemmed The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanics
title_short The underlying difference of metastatic and non-metastatic breast cancer cells in configuring type I collagen fibres to promote migration by cell mechanics
title_sort underlying difference of metastatic and non metastatic breast cancer cells in configuring type i collagen fibres to promote migration by cell mechanics
topic Cancer metastasis
Matrix remodeling
Mechanical communication
Integrin
Piezo
E-Cadherin
url http://www.sciencedirect.com/science/article/pii/S2949907025000014
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