CDK inhibitors (p16/p19/p21) induce senescence and autophagy in cancer-associated fibroblasts, “fueling” tumor growth via paracrine interactions, without an increase in neo-angiogenesis
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Here, we investigated the compartment-specific role of cell cycle arrest and senescence in breast cancer tumor growth. For this purpose, we generated a number of hTERT-immortalized senescent fibroblast cell lines overexpressing CDK inhibitors, such as p16(INK4A), p19(ARF) or p21(WAF1/CIP1). Interestingly, all these senescent fibroblast cell lines showed evidence of increased susceptibility toward the induction of autophagy (either at baseline or after starvation), as well as significant mitochondrial dysfunction. Most importantly, these senescent fibroblasts also dramatically promoted tumor growth (up to ~2-fold), without any comparable increases in tumor angiogenesis. Conversely, we generated human breast cancer cells (MDA-MB-231 cells) overexpressing CDK inhibitors, namely p16(INK4A) or p21(WAF1/CIP1). Senescent MDA-MB-231 cells also showed increased expression of markers of cell cycle arrest and autophagy, including β-galactosidase, as predicted. Senescent MDA-MB-231 cells had retarded tumor growth, with up to a near 2-fold reduction in tumor volume. Thus, the effects of CDK inhibitors are compartment-specific and are related to their metabolic effects, which results in the induction of autophagy and mitochondrial dysfunction. Finally, induction of cell cycle arrest with specific inhibitors (PD0332991) or cellular stressors [hydrogen peroxide (H(2)O(2)) or starvation] indicated that the onset of autophagy and senescence are inextricably linked biological processes. The compartment-specific induction of senescence (and hence autophagy) may be a new therapeutic target that could be exploited for the successful treatment of human breast cancer patients.
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BNIP3 encodes BCL2 interacting protein 3, which is increased in hypoxic-ischemic-encephalopathy and physiological ageing, and increases in association with cellular senescence especially in cells over-expressing p21 and p16.
“BNIP3 (FC = 1.17, p = 0.04) encodes BCL2 interacting protein 3, which is increased in hypoxic-ischemic-encephalopathy [18] and physiological ageing [31], and has been shown to increase in association with cellular senescence especially in cells over-expressing p21 and p16 [16].”
From Early onset senescence and cognitive impairment in a murine model of repeated mTBI (2021) · cites this paper as [16]
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- Authors
- Capparelli, C., Chiavarina, B., Whitaker-Menezes, D., Pestell, T. G., Pestell, R. G., Hulit, J., Andò, S., Howell, A., Martinez-Outschoorn, U. E., Sotgia, F., & Lisanti, M. P.
- Affiliations
- Thomas Jefferson University (US)
- The Jefferson Stem Cell Biology and Regenerative Medicine Center; Kimmel Cancer Center; Thomas Jefferson University; Philadelphia, PA USA
- Manchester Academic Health Science Centre (GB)
- University of Calabria (IT)
- Corresponding author
- Sotgia, Federica
- Lisanti, Michael P.
- ORCID
- Venue
- Cell Cycle
- Publisher
- Informa UK Limited
- Published
- 2012-08-30
- Volume
- 11
- Issue
- 19
- Pages
- 3599-3610
- ISSN
- 1538-4101 (ISSN-L)
- 1551-4005
- PMC
- PMC3478311
- OpenAlex
- W2012173754
- Cited by
- 221
- References
- 70
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 16 · 2023: 11 · 2022: 17 · 2021: 19 · 2020: 25 · 2019: 16 · 2018: 21 · 2017: 20 · 2016: 10 · 2015: 18 · 2014: 11 · 2013: 16 · 2012: 4
- FWCI
- 10.51
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Cell Cycle (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- The Medicine Forum (submittedVersion)
- Archive of Doctoral Theses and Digital Collections (University of Calabria) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- National Cancer Institute (R01CA107382, R01 CA75503, R01-CA-86072, R01CA120876, R01 CA70896, R01CA086072, R01CA080250, R01CA075503, R01CA098779, R01CA070896, P30CA056036, P30 CA 56036)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR055660)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- cyclin-dependent kinase inhibitors, cellular senescence, autophagy, cancer-associated fibroblasts, breast cancer, tumor growth, paracrine signaling, angiogenesis, mitochondrial dysfunction, p16INK4a, p19ARF, p21, cell cycle arrest, palbociclib, hydrogen peroxide, starvation, tumor microenvironment
- MeSH terms
- Animals, Autophagy, Breast Neoplasms, Cell Cycle, Female, Fibroblasts, Humans, Hydrogen Peroxide, Models, Biological, Neovascularization, Pathologic, Piperazines, Pyridines, Cellular Senescence, Lactic Acid, Paracrine Communication, Cyclin-Dependent Kinase Inhibitor p16, Cell Proliferation, Cyclin-Dependent Kinase Inhibitor Proteins, Cyclin-Dependent Kinase Inhibitor p21, Cyclin-Dependent Kinase Inhibitor p19, Mice
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