Loss of IFN-γ pathway genes in tumor cells as a mechanism of resistance to anti-CTLA-4 therapy
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Antibody blockade of the inhibitory CTLA-4 pathway has led to clinical benefit in a subset of patients with metastatic melanoma. Anti-CTLA-4 enhances T cell responses, including production of IFN-γ, which is a critical cytokine for host immune responses. However, the role of IFN-γ signaling in tumor cells in the setting of anti-CTLA-4 therapy remains unknown. Here, we demonstrate that patients identified as non-responders to anti-CTLA-4 (ipilimumab) have tumors with genomic defects in IFN-γ pathway genes. Furthermore, mice bearing melanoma tumors with knockdown of IFN-γ receptor 1 (IFNGR1) have impaired tumor rejection upon anti-CTLA-4 therapy. These data highlight that loss of the IFN-γ signaling pathway is associated with primary resistance to anti-CTLA-4 therapy. Our findings demonstrate the importance of tumor genomic data, especially IFN-γ related genes, as prognostic information for patients selected to receive treatment with immune checkpoint therapy.
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Mutations in IFNGR1 and JAK, part of IFNγ signaling, have been found in patients who developed resistance to checkpoint inhibitors.
“Mutations in IFNGR1 and JAK, a component of the IFNγ signaling pathway, have been found in patients presenting resistance to checkpoint inhibitors (Gao et al., 2016; Zaretsky et al., 2016).”
From Protein Barcodes Enable High-Dimensional Single-Cell CRISPR Screens (2018) · cites this paper as Gao et al., 2016
These findings are consistent with clinical data correlating resistance to checkpoint inhibitors with mutations in B2m and IFNγ pathways and with recent genome-wide CRISPR screening data.
“These findings are consistent with emerging clinical data correlating resistance to checkpoint inhibitors with mutations in the B2m and IFNγ pathways (Gao et al., 2016; Zaretsky et al., 2016), and with recent genome-wide CRISPR screening data (Patel et al., 2017).”
From Protein Barcodes Enable High-Dimensional Single-Cell CRISPR Screens (2018) · cites this paper as Gao et al., 2016
P. distasonis enhances immune checkpoint inhibitor-mediated anticancer immunity by inducing production of IFNγ+CD8+ T cells.
“P. distasonis has been shown to enhance immune checkpoint inhibitor-mediated anticancer immunity by inducing the production of IFNγ+CD8+ T cells.53 54”
Knockdown of IFN-gamma receptor 1 impaired antitumor responses to anti-CTLA4 in a murine melanoma model.
“In addition, knockdown of IFNγ-receptor 1 led to impaired antitumor responses with anti-CTLA4 in a murine model of melanoma (159).”
From The Next Decade of Immune Checkpoint Therapy (2021) · cites this paper as [159]
IFN signaling through JAK/STAT plays a prominent role in tumor immunity.
“Interferon (IFN) signaling through the Janus kinase (JAK)/signal transducer and activator of transcription (STAT) pathway plays a prominent role in tumor immunity.”
From Hallmarks of response, resistance, and toxicity to immune checkpoint blockade (2021) · cites this paper as Gao et al., 2016
Defects in the IFN/JAK/STAT pathway and downstream effectors show both negative and positive correlations with ICB response, suggesting a dual role.
“Defects associated with this pathway and its downstream effectors have shown both negative and positive correlations with response to ICB, suggesting a dual role for this pathway in tumor immunity (Ayers et al., 2017; Gao et al., 2016).”
From Hallmarks of response, resistance, and toxicity to immune checkpoint blockade (2021) · cites this paper as Gao et al., 2016
Loss of IFN-gamma signaling could induce resistance to anti-CTLA-4 treatment.
“Loss of IFN-ɤ signaling could induce resistance to anti-CTLA-4 treatment (95).”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [95]
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“Copy-number alterations (CNAs) of IFNGR1/IFGR2, IRF1, and interferon-receptor-associated Janus kinase 2(JAK2), as well as amplification of SOCS1 and PIAS4, have been identified in nonresponders with metastatic melanoma patients through wholeexome sequencing (WES).(127,128) Mutations of JAK1/2 and beta-2microglobulin (…”
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“Accordingly, loss-of-function mutations and genomic alterations in the IFN signaling pathway have been associated with clinical ICB resistance and/or relapse (Gao et al., 2016; Shin et al., 2017; Zaretsky et al., 2016), and unbiased genetic screens have identified this same pathway as being important for immunotherapy…”
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“Melanoma CTLA‐4 Loss of IFN‐γ axes in tumor cells is contributed to the cell resistance to anti‐ CTLA‐4 therapy [262]”
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“Genomic defects in IFNg pathway genes occurred at higher frequencies in melanoma tumors from anti–CTLA-4 nonresponders relative to responders (33).”
BackgroundLessons learned from the blockade of immune checkpoints in cancer immunotherapy
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“However, shortage or excess of IFN-γ signaling may also lead to immune resistance [81, 150].”
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“Moreover, deficiency of IFN- signaling may cause tumor cells to resist other immune checkpoints [53].”
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- Authors
- Gao, J., Shi, L. Z., Zhao, H., Chen, J., Xiong, L., He, Q., Chen, T., Roszik, J., Bernatchez, C., Woodman, S. E., Chen, P.-L., Hwu, P., Allison, J. P., Futreal, A., Wargo, J. A., & Sharma, P.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- Corresponding author
- Sharma, Padmanee
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 167
- Issue
- 2
- Pages
- 397-404.e9
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC5088716
- OpenAlex
- W2522313999
- Cited by
- 1,300
- References
- 41
- Citations by year
- 2026: 83 · 2025: 107 · 2024: 128 · 2023: 158 · 2022: 137 · 2021: 174 · 2020: 162 · 2019: 128 · 2018: 121 · 2017: 89 · 2016: 8 · 2015: 2
- FWCI
- 62.21
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (L30 CA117817, R01CA163793, K08CA160692, P30CA016672, K12CA088084)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- interferon-gamma signaling, IFNGR1, CTLA-4 blockade, ipilimumab, metastatic melanoma, immune checkpoint therapy, tumor rejection, prognostic factors, T cell response
- MeSH terms
- Ipilimumab, Interferon gamma Receptor, Animals, Antibodies, Monoclonal, Humans, Interferon-gamma, Melanoma, Melanoma, Experimental, Mice, Inbred C57BL, Skin Neoplasms, T-Lymphocytes, Cytokines, Receptors, Interferon, Drug Resistance, Neoplasm, Cell Line, Tumor, Mice, Gene Knockdown Techniques, CTLA-4 Antigen
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