Co-evolution of Matrisome and Adaptive Adhesion Dynamics Drives Ovarian Cancer Chemoresistance
Open accessAbstract
Due to its dynamic nature, the evolution of cancer cell-extracellular matrix (ECM) crosstalk, critically affecting metastasis and treatment resistance, remains elusive. Our results show that platinum-chemotherapy itself enhances resistance by progressively changing the cancer cell-intrinsic adhesion signaling and cell-surrounding ECM. Examining ovarian high-grade serous carcinoma (HGSC) transcriptome and histology, we describe the fibrotic ECM heterogeneity at primary tumors and distinct metastatic sites, prior and after chemotherapy. Using cell models from systematic ECM screen to collagen-based 2D and 3D cultures, we demonstrate that both specific ECM substrates and stiffness increase resistance to platinum-mediated, apoptosis-inducing DNA damage via FAK and β1 integrin-pMLC-YAP signaling. Among such substrates around metastatic HGSCs, COL6 was upregulated by chemotherapy and enhanced the resistance of relapse, but not treatment-naïve, HGSC organoids. These results identify matrix adhesion as an adaptive response, driving HGSC aggressiveness via co-evolving ECM composition and sensing, suggesting stromal and tumor strategies for ECM pathway targeting.
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Microfibrillar collagen-VI, in addition to collagen-I, has also been reported to promote platinum resistance, cancer cell survival and HGSOC relapse both in vivo and ex vivo in collagen hydrogels.
“Microfibrillar collagen-VI, in addition to collagen-I, has also been reported to promote platinum resistance, cancer cell survival and HGSOC relapse both in vivo and ex vivo in collagen hydrogels (Pietilä et al., 2021).”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as Pietilä et al., 2021
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- Authors
- Pietilä, E. A., Gonzalez-Molina, J., Moyano-Galceran, L., Jamalzadeh, S., Zhang, K., Lehtinen, L., Turunen, S. P., Martins, T. A., Gultekin, O., Lamminen, T., Kaipio, K., Joneborg, U., Hynninen, J., Hietanen, S., Grénman, S., Lehtonen, R., Hautaniemi, S., Carpén, O., Carlson, J. W., & Lehti, K.
- Affiliations
- University of Helsinki (FI)
- University of Turku (FI)
- Karolinska Institutet (SE)
- Karolinska University Hospital (SE)
- Corresponding author
- Lehti, Kaisa
- ORCID
- Venue
- Nature Communications
- Published
- 2021-06-23
- Volume
- 12
- Issue
- 1
- Pages
- 3904-3904
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC8222388
- OpenAlex
- W3177441967
- Cited by
- 175
- References
- 74
- Citations by year
- 2026: 27 · 2025: 32 · 2024: 43 · 2023: 45 · 2022: 27 · 2021: 1
- FWCI
- 15.14
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Työväentutkimus Vuosikirja (submittedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, cc-by)
- Funders
- K. Albin Johanssons Stiftelse
- Emil Aaltosen Säätiö
- Orionin Tutkimussäätiö
- Finnish Cancer Foundation
- Sigrid Juséliuksen Säätiö
- Cancerfonden
- Vetenskapsrådet (2019-01541)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- high-grade serous ovarian cancer, extracellular matrix, matrisome, cell adhesion signaling, extracellular matrix stiffness, focal adhesion kinase, beta1 integrin, YAP signaling, tumor fibrosis, metastasis, tumor stroma, ECM-targeted therapy
- MeSH terms
- Antineoplastic Agents, Cell Adhesion, Cisplatin, Collagen, Extracellular Matrix, Female, Humans, Neoplasm Recurrence, Local, Ovarian Neoplasms, Signal Transduction, Gene Expression Regulation, Neoplastic, Apoptosis, Cystadenocarcinoma, Serous, Drug Resistance, Neoplasm, Evolution, Molecular, Gene Expression Profiling, Cell Line, Tumor, Kaplan-Meier Estimate, Tumor Microenvironment
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