ATM-ATR–dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype
Open accessAbstract
There is much evidence to support a role for natural killer (NK) cells in controlling the progression of multiple myeloma (MM), a malignancy characterized by an abnormal plasma cell proliferation in the bone marrow (BM). Induction of DNA damage response has been recently shown capable of enhancing NKG2D ligand (NKG2DL) expression, but nothing is known about DNAM-1 ligand (DNAM-1L) regulation. In this study, we show that myeloma cells treated with low doses of therapeutic agents commonly used in the management of patients with MM, such as doxorubicin, melphalan, and bortezomib, up-regulate DNAM-1 and NKG2D ligands. Accordingly, therapeutic drug treatment of MM cells increases NK-cell degranulation, the NKG2D and DNAM-1 receptors being the major triggering molecules. Similar data were also obtained using ex vivo primary plasma cells derived from MM patients. Drug-induced DNAM-1 and NKG2D ligand expression was abolished after treatment with the ATM (ataxia telangiectasia mutated) and ATR (ATM- and RAD3-related) pharmacologic inhibitors caffeine and KU-55933, and was preferentially associated with senescent cells arrested in the G2 phase of the cell cycle. Altogether, our findings have identified a common pathway that can trigger the up-regulation of different NK cell–activating ligands and suggest that NK cells represent an immunosurveillance mechanism toward cells undergoing stress-induced senescent programs.
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Senescent cells are surveilled by several innate and adaptive immune cell types, including NK cells, T cells, and macrophages.
“Senescent cells are indeed subjected to immunosurveillance by multiple components of innate and adaptive immunity, including NK cells, T cells and macrophages145,151,153–156.”
From Cellular senescence in ageing: from mechanisms to therapeutic opportunities (2021) · cites this paper as [154]
The Discussion (page unavailable) proposes NK-cell surveillance of cells undergoing senescence and reports macrophage- and NK-cell-mediated clearance in a murine liver carcinoma study. It does not establish T-cell surveillance of senescent cells, so it supports the innate-cell examples but not the full claim about innate and adaptive immunity. (LLM, conf=0.86)
Experimental — accuracy not yet measuredChemotherapeutic drugs doxorubicin, melphalan and bortezomib upregulate both DNAM-1 ligand PVR and NKG2D ligands MICA and MICB on multiple myeloma cells presenting a senescent phenotype.
“Chemotherapeutic drugs, including doxorubicin, melphalan and bortezomib, upregulate both the DNAX accessory molecule-1 (DNAM-1; CD226) ligand PVR (poliovirus receptor; CD155) and NKG2D ligands (MICA and MICB) on multiple myeloma cells presenting a senescent phenotype.”
From Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases (2020) · cites this paper as [137]
PVR, MICA and MICB ligands enhance NK cell susceptibility.
“These ligands enhance NK cell susceptibility [137].”
From Immune Clearance of Senescent Cells to Combat Ageing and Chronic Diseases (2020) · cites this paper as [137]
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- Authors
- Soriani, A., Zingoni, A., Cerboni, C., Iannitto, M. L., Ricciardi, M. R., Di Gialleonardo, V., Cippitelli, M., Fionda, C., Petrucci, M. T., Guarini, A., Foà, R., & Santoni, A.
- Affiliations
- Istituto Pasteur (IT)
- Sapienza University of Rome (IT)
- Department of Experimental Medicine, Istituto Pasteur-Fondazione Cenci Bolognetti, and
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2009-04-09
- Volume
- 113
- Issue
- 15
- Pages
- 3503-3511
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- OpenAlex
- W2023283620
- Cited by
- 460
- References
- 51
- Citations by year
- 2026: 19 · 2025: 27 · 2024: 28 · 2023: 29 · 2022: 22 · 2021: 28 · 2020: 37 · 2019: 35 · 2018: 35 · 2017: 23 · 2016: 26 · 2015: 30 · 2014: 25 · 2013: 34 · 2012: 23
- FWCI
- 5.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Blood (publishedVersion)
- PubMed (publishedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Funders
- Ministero dell’Istruzione, dell’Università e della Ricerca
- Associazione Italiana per la Ricerca sul Cancro
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Health Sciences › Medicine › Hematology › Multiple Myeloma Research and Treatments
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Keywords
- multiple myeloma, natural killer cells, NKG2D ligands, ATM, ATR, DNA damage response, senescence, NK cell degranulation, doxorubicin, melphalan, bortezomib, caffeine, KU55933, immune surveillance, plasma cells, G2 cell cycle arrest
- MeSH terms
- T Lineage-Specific Activation Antigen 1, Antibiotics, Antineoplastic, Antigens, Differentiation, T-Lymphocyte, Antineoplastic Agents, Caffeine, DNA-Binding Proteins, Doxorubicin, Humans, Killer Cells, Natural, Melphalan, Morpholines, Multiple Myeloma, Phosphodiesterase Inhibitors, Pyrones, Cell Degranulation, Up-Regulation, Cellular Senescence, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Antineoplastic Agents, Alkylating, Tumor Suppressor Proteins, Intercellular Signaling Peptides and Proteins, Cell Line, Tumor, GPI-Linked Proteins, Ataxia Telangiectasia Mutated Proteins
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