Cited by 141Cancer Immunotherapy and BiomarkersT-cell and B-cell ImmunologyImmunotherapy and Immune Responses

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Clonal Deletion of Tumor-Specific T Cells by Interferon-γ Confers Therapeutic Resistance to Combination Immune Checkpoint Blockade

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Pai, Chien-Chun Steven, Huang, John T., Lu, Xiaoqing, Simons, Donald M., Park, Chanhyuk, Chang, Anthony, Tamaki, Whitney, Liu, Eric, Roybal, Kole T., Seagal, Jane, Chen, Mingyi, Hagihara, Katsunobu, Wei, Xiao X., DuPage, Michel, Kwek, Serena S., Oh, David Y., Daud, Adil, Tsai, Katy K., Wu, Clint, Zhang, Li, Fasso, Marcella, Sachidanandam, Ravi, Jayaprakash, Anitha, Lin, Ingrid, Casbon, Amy-Jo, Kinsbury, Gillian A., Fong, Lawrence·2019·Immunity

DOI 10.1016/j.immuni.2019.01.006PMC PMC6886475

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Abstract

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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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: Lu, Xiaoqing
Simons, Donald M.
Chang, Anthony
Tamaki, Whitney
Liu, Eric
Roybal, Kole T.
Seagal, Jane
Chen, Mingyi
Hagihara, Katsunobu
Wei, Xiao X.
DuPage, Michel
Kwek, Serena S.
Oh, David Y.
Daud, Adil
Tsai, Katy K.
Zhang, Li
Sachidanandam, Ravi
Jayaprakash, Anitha
Fong, Lawrence
Venue: Immunity
Publisher: Elsevier BV
Published: 2019-02
Volume: 50
Issue: 2
Pages: 477-492.e8
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2019.01.006
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 383 d)
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

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Clonal Deletion of Tumor-Specific T Cells by Interferon-γ Confers Therapeutic Resistance to Combination Immune Checkpoint Blockade

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