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Targetable mechanisms driving immunoevasion of persistent senescent cells link chemotherapy-resistant cancer to aging
Open accessAbstract
Cellular senescence is a tumor-suppressive mechanism that can paradoxically contribute to aging pathologies. Despite evidence of immune clearance in mouse models, it is not known how senescent cells (SnCs) persist and accumulate with age or in tumors in individuals. Here, we identify cooperative mechanisms that orchestrate the immunoevasion and persistence of normal and cancer human SnCs through extracellular targeting of natural killer receptor signaling. Damaged SnCs avoided immune recognition through MMP-dependent shedding of NKG2D ligands reinforced via paracrine suppression of NKG2D receptor–mediated immunosurveillance. These coordinated immunoediting processes were evident in residual, drug-resistant tumors from cohorts of more than 700 prostate and breast cancer patients treated with senescence-inducing genotoxic chemotherapies. Unlike in mice, these reversible senescence subversion mechanisms were independent of p53/p16 and exacerbated in oncogenic RAS-induced senescence. Critically, the p16 INK4A tumor suppressor could disengage the senescence growth arrest from the damage-associated immune senescence program, which was manifest in benign nevus lesions, where indolent SnCs accumulated over time and preserved a non-proinflammatory tissue microenvironment maintaining NKG2D-mediated immunosurveillance. Our study shows how subpopulations of SnCs elude immunosurveillance and reveals potential secretome-targeted therapeutic strategies to selectively eliminate — and restore the clearance of — the detrimental SnCs that actively persist after chemotherapy and accumulate at sites of aging pathologies.
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“Senescence is also an important mechanism of efficacy in the treatment of breast cancer with PARP inhibitors [59] and many typical chemotherapy agents used to treat breast cancer, such as epirubicin and cyclophosphamide [60].”
From Senescence and Cancer: A Review of Clinical Implications of Senescence and Senotherapies (2020) · cites this paper as [60]
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“At younger ages, senescent cells are cleared by the host immune system [63–66]”
From Reducing Senescent Cell Burden in Aging and Disease (2020) · cites this paper as [63]
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Metadata
- Authors
- Muñoz, D. P., Yannone, S. M., Daemen, A., Sun, Y., Vakar-Lopez, F., Kawahara, M., Freund, A. M., Rodier, F., Wu, J. D., Desprez, P.-Y., Raulet, D. H., Nelson, P. S., van ’t Veer, L. J., Campisi, J., & Coppé, J.-P.
- Affiliations
- University of California, San Francisco (US)
- Lawrence Berkeley National Laboratory (US)
- Fred Hutch Cancer Center (US)
- Department of Pathology, University of Washington, Seattle, Washington, USA.
- Buck Institute for Research on Aging (US)
- Lawrence Berkeley National Laboratory, Life Sciences Division, Berkeley, California, USA.
- University of Washington (US)
- University of California, Berkeley (US)
- Helen Diller Family Comprehensive Cancer Center, Department of Laboratory Medicine, UCSF, San Francisco, California, USA.
- Corresponding author
- Coppé, Jean-Philippe
- ORCID
- Venue
- JCI Insight
- Published
- 2019-07-25
- Volume
- 4
- Issue
- 14
- ISSN
- 2379-3708 (ISSN-L)
- PMC
- PMC6675550
- OpenAlex
- W2952749575
- Cited by
- 162
- References
- 92
- Citations by year
- 2026: 18 · 2025: 18 · 2024: 25 · 2023: 21 · 2022: 30 · 2021: 26 · 2020: 23 · 2019: 1
- FWCI
- 13.72
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- JCI Insight (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute on Aging (R56AG009909, R37AG009909, P01AG017242)
- National Cancer Institute (R01CA093678, R01CA204021, R01CA165573, P50CA097186)
- National Institute of Allergy and Infectious Diseases (R01AI113041)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- cellular senescence, senescent cells, immune evasion, NKG2D, natural killer cells, matrix metalloproteinases, immune surveillance, immunoediting, chemoresistance, aging, prostate cancer, breast cancer, Ras-induced senescence, p16INK4a, benign nevi, tumor microenvironment
- MeSH terms
- Aging, Animals, Antineoplastic Agents, Biopsy, Breast, Breast Neoplasms, DNA Damage, Female, Humans, Immunologic Surveillance, Male, Metalloendopeptidases, Prostate, Prostatic Neoplasms, Gene Expression Regulation, Neoplastic, Cellular Senescence, Drug Resistance, Neoplasm, Tumor Escape, Cyclin-Dependent Kinase Inhibitor p16, Gene Expression Profiling, Cell Line, Tumor, Tissue Array Analysis, Mice, NK Cell Lectin-Like Receptor Subfamily K, Tumor Microenvironment, Datasets as Topic
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