Biomechanical Remodeling of the Microenvironment by Stromal Caveolin-1 Favors Tumor Invasion and Metastasis
Open accessAbstract
Mechanotransduction is a key determinant of tissue homeostasis and tumor progression. It is driven by intercellular adhesions, cell contractility, and forces generated within the microenvironment and is dependent on extracellular matrix composition, organization, and compliance. We show that caveolin-1 (Cav1) favors cell elongation in three-dimensional cultures and promotes Rho- and force-dependent contraction, matrix alignment, and microenvironment stiffening through regulation of p190RhoGAP. In turn, microenvironment remodeling by Cav1 fibroblasts forces cell elongation. Cav1-deficient mice have disorganized stromal tissue architecture. Stroma associated with human carcinomas and melanoma metastases is enriched in Cav1-expressing carcinoma-associated fibroblasts (CAFs). Cav1 expression in breast CAFs correlates with low survival, and Cav1 depletion in CAFs decreases CAF contractility. Consistently, fibroblast expression of Cav1, through p190RhoGAP regulation, favors directional migration and invasiveness of carcinoma cells in vitro. In vivo, stromal Cav1 remodels peri- and intratumoral microenvironments to facilitate tumor invasion, correlating with increased metastatic potency. Thus, Cav1 modulates tissue responses through force-dependent architectural regulation of the microenvironment.
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CAF ECM deposition and remodelling depends on RHO and RAB GTPase-mediated control of integrin-mediated adhesions and the actomyosin cytoskeleton and is linked to downregulation of CD36.
“This depends on RHO and RAB GTPase-mediated control of integrin-mediated adhesions and the actomyosin cytoskeleton81–83 and is linked to downregulation of the transmembrane receptor CD36 (also known as platelet glycoprotein 4)84.”
From A framework for advancing our understanding of cancer-associated fibroblasts (2020) · cites this paper as [82]
The Results section on Cav1-promoted remodeling reports Rho-GTPase-dependent fibronectin remodeling and cell contractility; another Results section describes integrin-dependent matrix adhesions. Our copy does not establish Rab-GTPase-mediated control of those processes. The CD36 clause has a separate citation (84) in the printed sentence, so it is not attributed to this source. (LLM, conf=0.87)
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- Authors
- Goetz, J. G., Minguet, S., Navarro-Lérida, I., Lazcano, J. J., Samaniego, R., Calvo, E., Tello, M., Osteso-Ibáñez, T., Pellinen, T., Echarri, A., Cerezo, A., Klein-Szanto, A. J. P., Garcia, R., Keely, P. J., Sánchez-Mateos, P., Cukierman, E., & Del Pozo, M. A.
- Affiliations
- Spanish National Centre for Cardiovascular Research (ES)
- Hospital General Universitario Gregorio Marañón (ES)
- Consejo Superior de Investigaciones Científicas (ES)
- University of Wisconsin–Madison (US)
- Corresponding author
- Goetz, Jacky G.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2011-07
- Volume
- 146
- Issue
- 1
- Pages
- 148-163
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3244213
- OpenAlex
- W2044339772
- Cited by
- 720
- References
- 3
- Citations by year
- 2026: 16 · 2025: 26 · 2024: 42 · 2023: 46 · 2022: 49 · 2021: 47 · 2020: 70 · 2019: 50 · 2018: 52 · 2017: 52 · 2016: 55 · 2015: 64 · 2014: 47 · 2013: 43 · 2012: 42
- FWCI
- 22.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 747 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- Ministerio de Ciencia e Innovación (MAT2009-08650, CSD2009, CSD2010-00024, CSD2009–00016)
- Centro Nacional de Investigaciones Cardiovasculares
- National Institutes of Health (RD06/0020)
- National Cancer Institute (CA113451, RD06/0020, R01CA142833, R01CA114462, R01CA113451)
- European Social Fund
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- caveolin-1, mechanotransduction, tumor microenvironment remodeling, cancer-associated fibroblasts, p190RhoGAP, RhoA signaling, fibroblast contractility, extracellular matrix stiffness, cell elongation, tumor invasion, metastasis, breast cancer, melanoma, directional cell migration, stromal microenvironment
- MeSH terms
- Animals, Cell Movement, Fibroblasts, Humans, Melanoma, Neoplasm Metastasis, Neoplasms, Mice, Knockout, Caveolin 1, Mice
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