Activation of Tumor-Cell STING Primes NK-Cell Therapy
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Abstract
Activation of the stimulator of interferon genes (STING) pathway promotes antitumor immunity but STING agonists have yet to achieve clinical success. Increased understanding of the mechanism of action of STING agonists in human tumors is key to developing therapeutic combinations that activate effective innate antitumor immunity. Here, we report that malignant pleural mesothelioma cells robustly express STING and are responsive to STING agonist treatment ex vivo. Using dynamic single-cell RNA sequencing of explants treated with a STING agonist, we observed CXCR3 chemokine activation primarily in tumor cells and cancer-associated fibroblasts, as well as T-cell cytotoxicity. In contrast, primary natural killer (NK) cells resisted STING agonist–induced cytotoxicity. STING agonists enhanced migration and killing of NK cells and mesothelin-targeted chimeric antigen receptor (CAR)-NK cells, improving therapeutic activity in patient-derived organotypic tumor spheroids. These studies reveal the fundamental importance of using human tumor samples to assess innate and cellular immune therapies. By functionally profiling mesothelioma tumor explants with elevated STING expression in tumor cells, we uncovered distinct consequences of STING agonist treatment in humans that support testing combining STING agonists with NK and CAR-NK cell therapies.
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Treatment of melanoma PDOTS with a STING agonist (ADU-S100) had no impact on PDOTS viability, in contrast to TNFα/IFNγ +/- TBK1i.
“Lastly, treatment of melanoma PDOTS with a STING agonist (ADU-S100 43,44 ) had no impact on PDOTS viability, in contrast to TNF α /IFN γ +/- TBK1i (Extended Data Fig. 9h).”
From Targeting TBK1 to overcome resistance to cancer immunotherapy (2023) · cites this paper as [44]
In post-cryoablated RMS 76-9STINGwt TME compared with RMS 76-9STING-/- TME in wild-type mice, there was a significant increase in total CD4+ T cells expressing IFN-γ and GZMB, NK cells, GZMB expression in CD8+ T cells, and Foxp3+ CD4+ cells.
“we observed a significant increase in the total CD4+ T cells expressing IFN-γ (figure 4H) and granzyme B (GZMB; figure 4J),60–65 NK cells (figure 4N), and the amount of GZMB expression in CD8+ T cells (figure 4L) in the post-cryoablated RMS 76-9STINGwt TME as compared with RMS 76-9STING-/- TME in wild-type mice, as was Foxp3+ CD4+ cells (figure 4M).”
From Functional tumor cell-intrinsic STING, not host STING, drives local and systemic antitumor immunity and therapy efficacy following cryoablation (2023) · cites this paper as [60]
The Results section on dynamic scRNA-seq of MPM explants identifies granzyme-positive T cells and NK cells, but it does not report the claimed increases after cryoablation. Searches for RMS 76-9, cryoablation, and the STING-wild-type versus STING-knockout comparison found no passage addressing that experiment in our copy. (LLM, conf=0.75)
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- Authors
- Knelson, E. H., Ivanova, E. V., Tarannum, M., Campisi, M., Lizotte, P. H., Booker, M. A., Ozgenc, I., Noureddine, M., Meisenheimer, B., Chen, M., Piel, B., Spicer, N., Obua, B., Messier, C. M., Shannon, E., Mahadevan, N. R., Tani, T., Schol, P. J., Lee-Hassett, A. M., Zlota, A., Vo, H. V., Ha, M., Bertram, A. A., Han, S., Thai, T. C., Gustafson, C. E., Venugopal, K., Haggerty, T. J., Albertson, T. P., Hartley, A.-V., Eser, P. O., Li, Z.-H., Cañadas, I., Vivero, M., De Rienzo, A., Richards, W. G., Abu-Yousif, A. O., Appleman, V. A., Gregory, R. C., Parent, A., Lineberry, N., Smith, E. L., Jänne, P. A., Miret, J. J., Tolstorukov, M. Y., Romee, R., Paweletz, C. P., Bueno, R., & Barbie, D. A.
- Affiliations
- Dana-Farber Cancer Institute (US)
- Harvard University (US)
- Boston University (US)
- Brigham and Women's Hospital (US)
- 1Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
- Fox Chase Cancer Center (US)
- 7Deparment of Surgery, Brigham and Women's Hospital, Boston, Massachusetts.
- 9Takeda Development Center Americas, Inc. (TDCA), Lexington, Massachusetts.
- Corresponding author
- Paweletz, Cloud P.
- Bueno, Raphael
- Barbie, David A.
- ORCID
- Knelson, Erik H.
- Ivanova, Elena V.
- Tarannum, Mubin
- Campisi, Marco
- Lizotte, Patrick H.
- Booker, Matthew A.
- Ozgenc, Ismail
- Noureddine, Moataz
- Meisenheimer, Brittany
- Chen, Minyue
- Piel, Brandon
- Spicer, Nathaniel
- Obua, Bonje
- Messier, Cameron M.
- Shannon, Erin
- Mahadevan, Navin R.
- Tani, Tetsuo
- Schol, Pieter J.
- Lee-Hassett, Anna M.
- Zlota, Ari
- Vo, Ha V.
- Ha, Minh
- Bertram, Arrien A.
- Han, Saemi
- Thai, Tran C.
- Gustafson, Corinne E.
- Venugopal, Kartika
- Haggerty, Timothy J.
- Albertson, Thomas P.
- Hartley, Antja-Voy
- Eser, Pinar O.
- Li, Ze-Hua
- Cañadas, Israel
- Vivero, Marina
- De Rienzo, Assunta
- Richards, William G.
- Abu-Yousif, Adnan O.
- Appleman, Vicky A.
- Gregory, Richard C.
- Parent, Alexander
- Lineberry, Neil
- Smith, Eric L.
- Jänne, Pasi A.
- Miret, Juan J.
- Tolstorukov, Michael Y.
- Romee, Rizwan
- Paweletz, Cloud P.
- Bueno, Raphael
- Barbie, David A.
- Venue
- Cancer Immunology Research
- Published
- 2022-06-02
- Volume
- 10
- Issue
- 8
- Pages
- 947-961
- ISSN
- 2326-6066 (ISSN-L)
- 2326-6074
- PMC
- PMC9357206
- OpenAlex
- W4282923345
- Cited by
- 88
- References
- 53
- Citations by year
- 2026: 15 · 2025: 35 · 2024: 16 · 2023: 19 · 2022: 3
- FWCI
- 6.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cancer Immunology Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NCI (P30CA06516)
- NIH NCI (R01 CA190294, U01 CA214381, P01 CA154303)
- Research Agreement (TAK-676)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- STING agonist, natural killer cells, CAR-NK cells, malignant pleural mesothelioma, cancer-associated fibroblasts, mesothelin, innate antitumor immunity, NK cell migration, T cell cytotoxicity, combination immunotherapy
- MeSH terms
- Receptors, Chimeric Antigen, Mesothelioma, Malignant, STING Protein, Humans, Killer Cells, Natural, Membrane Proteins, Immunotherapy, Adoptive, Cell Line, Tumor, Cell- and Tissue-Based Therapy
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