Clonal Deletion of Tumor-Specific T Cells by Interferon-γ Confers Therapeutic Resistance to Combination Immune Checkpoint Blockade
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Resistance to checkpoint-blockade treatments is a challenge in the clinic. We found that although treatment with combined anti-CTLA-4 and anti-PD-1 improved control of established tumors, this combination compromised anti-tumor immunity in the low tumor burden (LTB) state in pre-clinical models as well as in melanoma patients. Activated tumor-specific T cells expressed higher amounts of interferon-γ (IFN-γ) receptor and were more susceptible to apoptosis than naive T cells. Combination treatment induced deletion of tumor-specific T cells and altered the T cell repertoire landscape, skewing the distribution of T cells toward lower-frequency clonotypes. Additionally, combination therapy induced higher IFN-γ production in the LTB state than in the high tumor burden (HTB) state on a per-cell basis, reflecting a less exhausted immune status in the LTB state. Thus, elevated IFN-γ secretion in the LTB state contributes to the development of an immune-intrinsic mechanism of resistance to combination checkpoint blockade, highlighting the importance of achieving the optimal magnitude of immune stimulation for successful combination immunotherapy strategies.
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In mouse models of colon and prostate cancer, combined anti-CTLA4 and anti-PD-1 antibodies in the low tumour burden state after primary tumour resection improved control of established tumours but compromised antitumour immunity.
“in mouse models of colon and prostate cancer, combined administration of anti-CTLA4 and anti-PD-1 antibodies in the low tumour burden state (following resection of the primary tumour) provided improved control of established tumours but compromised antitumour immunity109.”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [109]
The Results section on low tumour burden reports that adding anti-PD-1 to anti-CTLA-4 compromised tumour control, and the section on memory responses reports weaker protection on tumour re-challenge. The cited experiments treated mice after tumour implantation, not after primary-tumour resection. Improved control with the combination is therefore not supported in the low-burden setting described by the claim. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe impaired response was attributed to IFNγ-mediated depletion of tumour-reactive T cells through activation-induced cell death.
“This impaired response was attributed to IFNγ-mediated depletion of tumour-reactive T cells owing to activation-induced cell death.”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [109]
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- Authors
- Pai, C.-C. S., Huang, J. T., Lu, X., Simons, D. M., Park, C., Chang, A., Tamaki, W., Liu, E., Roybal, K. T., Seagal, J., Chen, M., Hagihara, K., Wei, X. X., DuPage, M., Kwek, S. S., Oh, D. Y., Daud, A., Tsai, K. K., Wu, C., Zhang, L., Fasso, M., Sachidanandam, R., Jayaprakash, A., Lin, I., Casbon, A.-J., Kinsbury, G. A., & Fong, L.
- Affiliations
- University of California, San Francisco (US)
- AbbVie (United States) (US)
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Fong, Lawrence
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2019-02
- Volume
- 50
- Issue
- 2
- Pages
- 477-492.e8
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC6886475
- OpenAlex
- W2913142277
- Cited by
- 141
- References
- 60
- Citations by year
- 2026: 10 · 2025: 20 · 2024: 18 · 2023: 18 · 2022: 18 · 2021: 26 · 2020: 17 · 2019: 14
- FWCI
- 7.84
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Bristol-Myers Squibb
- AbbVie
- National Cancer Institute (R01CA163012, R01CA194511, U01CA233100)
- Prostate Cancer Foundation
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- interferon-gamma, immune checkpoint blockade, anti-CTLA-4, anti-PD-1, combination immunotherapy, tumor-specific T cells, clonal deletion, T cell apoptosis, IFN-gamma receptor, T cell exhaustion, T cell receptor repertoire, low tumor burden, melanoma, immunotherapy resistance, T cell clonotypes
- MeSH terms
- Animals, Antibodies, Monoclonal, Humans, Interferon-gamma, Male, Mice, Inbred C57BL, Neoplasms, Experimental, T-Lymphocytes, Clonal Deletion, Mice, Knockout, Drug Resistance, Neoplasm, Cell Line, Tumor, Tumor Burden, CTLA-4 Antigen, Programmed Cell Death 1 Receptor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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