Senescent peritoneal mesothelium induces a pro-angiogenic phenotype in ovarian cancer cells in vitro and in a mouse xenograft model in vivo
Open accessAbstract
It is believed that senescent cells contribute to the progression of primary and metastatic tumors, however, the exact mechanisms of this activity remain elusive. In this report we show that senescent human peritoneal mesothelial cells (HPMCs) alter the secretory profile of ovarian cancer cells (A2780, OVCAR-3, SKOV-3) by increasing the release of four angiogenic agents: CXCL1, CXCL8, HGF, and VEGF. Proliferation and migration of endothelial cells subjected to conditioned medium generated by: cancer cells modified by senescent HPMCs; cancer cells co-cultured with senescent HPMCs; and by early-passage HPMCs from aged donors, were markedly intensified. The same was the case for the vascularization, size and number of tumors that developed in the mouse peritoneum upon injection of ovarian cancer cells with senescent HPMCs. When the identified pro-angiogenic proteins were neutralized in conditioned medium from the cancer cells, both aspects of endothelial cell behavior intensified in vitro in response to senescent HPMCs were markedly reduced. The search for mediators of senescent HPMC activity using specific neutralizing antibodies and recombinant exogenous proteins showed that the intensified angiogenic potential of cancer cells was elicited by IL-6 and TGF-β1. At the transcriptional level, increased proliferation and migration of endothelial cells exposed to cancer cells modified by senescent HPMCs was regulated by HIF-1α, NF-κB/p50 and AP-1/c-Jun. Collectively, our findings indicate that senescent HPMCs may promote the progression of ovarian cancer cells by reprogramming their secretory phenotype towards increased production of pro-angiogenic agents and subsequent increase in the angiogenic capabilities of the vascular endothelium.
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Co-injection of senescent fibroblasts or peritoneal mesothelial cells with cancer cells in xenograft models results in significantly greater tumour angiogenesis.
“Similarly, co-injection of senescent fibroblasts or peritoneal mesothelial cells with cancer cells in xenograft models results in significantly greater tumour angiogenesis.62,63”
From Paracrine roles of cellular senescence in promoting tumourigenesis (2018) · cites this paper as [63]
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- Authors
- Mikuła-Pietrasik, J., Sosińska, P., Naumowicz, E., Maksin, K., Piotrowska, H., Woźniak, A., Szpurek, D., & Książek, K.
- Affiliations
- Poznan University of Medical Sciences (PL)
- Corresponding author
- Książek, Krzysztof
- Venue
- Clinical & Experimental Metastasis
- Published
- 2015-10-03
- Volume
- 33
- Issue
- 1
- Pages
- 15-27
- ISSN
- 0262-0898 (ISSN-L)
- 1573-7276
- PMC
- PMC4740564
- OpenAlex
- W2240063018
- Cited by
- 46
- References
- 27
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 8 · 2016: 3
- FWCI
- 3.44
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Clinical & Experimental Metastasis (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Narodowe Centrum Nauki (DEC-2011/03/B/NZ3/01214)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- cellular senescence, peritoneal mesothelial cells, ovarian cancer, tumor angiogenesis, paracrine signaling, CXCL1, interleukin-8, hepatocyte growth factor, vascular endothelial growth factor, endothelial cell proliferation, endothelial cell migration, interleukin-6, TGF-β1, HIF-1α, NF-κB, tumor microenvironment, peritoneal xenograft
- MeSH terms
- Animals, Cell Movement, Epithelium, Female, Humans, Neovascularization, Pathologic, Ovarian Neoplasms, Peritoneum, Phenotype, Mice, SCID, Cellular Senescence, Disease Progression, Cell Proliferation, Mice, Heterografts
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