Tumor Interferon Signaling Regulates a Multigenic Resistance Program to Immune Checkpoint Blockade
Open accessAbstract
Therapeutic blocking of the PD1 pathway results in significant tumor responses, but resistance is common. We demonstrate that prolonged interferon signaling orchestrates PDL1-dependent and PDL1-independent resistance to immune checkpoint blockade (ICB) and to combinations such as radiation plus anti-CTLA4. Persistent type II interferon signaling allows tumors to acquire STAT1-related epigenomic changes and augments expression of interferon-stimulated genes and ligands for multiple T cell inhibitory receptors. Both type I and II interferons maintain this resistance program. Crippling the program genetically or pharmacologically interferes with multiple inhibitory pathways and expands distinct T cell populations with improved function despite expressing markers of severe exhaustion. Consequently, tumors resistant to multi-agent ICB are rendered responsive to ICB monotherapy. Finally, we observe that biomarkers for interferon-driven resistance associate with clinical progression after anti-PD1 therapy. Thus, the duration of tumor interferon signaling augments adaptive resistance and inhibition of the interferon response bypasses requirements for combinatorial ICB therapies.
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IFNγ and TNFα are key effector cytokines that contribute to anti-tumour immune responses, and genes associated with IFN and TNF signaling pathways contribute to immune evasion.
“IFN γ and TNF α are key effector cytokines that contribute to anti-tumour immune responses 9,11,27-30 , and genes associated with IFN and TNF signaling pathways contribute to immune evasion 4,9,29 .”
From Targeting TBK1 to overcome resistance to cancer immunotherapy (2023) · cites this paper as [28]
The Introduction says IFNγ favors rejection of highly immunogenic tumors, and the Discussion links sustained IFN signaling to adaptive immune resistance. The Results identify IFN-regulated inhibitory ligands and genes, but the cited passages do not establish the corresponding claims about TNFα or TNF signaling. (LLM, conf=0.88)
Experimental — accuracy not yet measuredChronic IFN signaling can promote an immune suppressive environment.
“Chronic IFN signaling can also promote an immune suppressive environment126.”
From The role of retrotransposable elements in ageing and age-associated diseases (2021) · cites this paper as [126]
The expression of PD-L1 and MHC II is regulated by tumor IFN signaling.
“The expression of PD-L1 and MHC II, which may cause exhaustion by binding to T-cell programmed cell death protein 1 (PD-1) and lymphocyte activation gene 3 (LAG-3), respectively, is regulated by tumor interferon (IFN) signaling.”
From Tumor interferon signaling and suppressive myeloid cells are associated with CAR T-cell failure in large B-cell lymphoma (2021) · cites this paper as [24]
In solid tumors, a tumor IFN-stimulated gene signature termed ISG.RS is associated with a multigenic program of T-cell exhaustion and worse outcomes after immune checkpoint blockade.
“In solid tumors, a tumor IFN–stimulated gene signature termed ISG.RS is associated with a multigenic program of T-cell exhaustion and worse outcomes after immune checkpoint blockade.”
From Tumor interferon signaling and suppressive myeloid cells are associated with CAR T-cell failure in large B-cell lymphoma (2021) · cites this paper as [24]
One part of this program is to increase tumor expression of multiple T-cell ligands that lead to exhaustion of T cells infiltrating the TME.
“One part of this program is to increase tumor expression of multiple T-cell ligands that lead to exhaustion of T cells infiltrating the TME.”
From Tumor interferon signaling and suppressive myeloid cells are associated with CAR T-cell failure in large B-cell lymphoma (2021) · cites this paper as [24]
When tumors express a gene signature (ISG.RS) consisting of genes coordinately activated by multiple types of IFN, a multigenic therapy resistance program is activated.
“When tumors express a gene signature (ISG.RS) consisting of genes coordinately activated by multiple types of IFN, a multigenic therapy resistance program is activated.”
From Tumor interferon signaling and suppressive myeloid cells are associated with CAR T-cell failure in large B-cell lymphoma (2021) · cites this paper as [24]
Chronic IFN signaling mediates immunosuppression and resistance to radiation and immune checkpoint inhibitor therapy in solid tumors.
“Recently, the Minn group elucidated how chronic IFN signaling mediates immunosuppression and resistance to radiation and immune checkpoint inhibitor therapy in solid tumors.2,24,54”
From Tumor interferon signaling and suppressive myeloid cells are associated with CAR T-cell failure in large B-cell lymphoma (2021) · cites this paper as [24]
Interferon signaling is of central importance to antitumor immune response.
“interferon signaling is of central importance to antitumor immune response43.”
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Self-citation
- Authors
- Benci, J. L., Xu, B., Qiu, Y., Wu, T. J., Dada, H., Twyman-Saint Victor, C., Cucolo, L., Lee, D. S. M., Pauken, K. E., Huang, A. C., Gangadhar, T. C., Amaravadi, R. K., Schuchter, L. M., Feldman, M. D., Ishwaran, H., Vonderheide, R. H., Maity, A., Wherry, E. J., & Minn, A. J.
- Affiliations
- University of Pennsylvania (US)
- University of Miami (US)
- Parker Institute for Cancer Immunotherapy (US)
- Corresponding author
- Minn, Andy J.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2016-12
- Volume
- 167
- Issue
- 6
- Pages
- 1540-1554.e12
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC5385895
- OpenAlex
- W2558219863
- Cited by
- 1,216
- References
- 42
- Citations by year
- 2026: 150 · 2025: 124 · 2024: 127 · 2023: 135 · 2022: 128 · 2021: 140 · 2020: 140 · 2019: 114 · 2018: 92 · 2017: 64 · 2016: 1 · 2014: 1
- FWCI
- 48.72
- 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, 365 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Apollo
- Funders
- Melanoma Research Alliance
- Parker Institute for Cancer Immunotherapy
- Robertson Foundation
- Cancer Research Institute Irvington Fellowship
- NIH (P50CA174523, R01CA163739, R01CA158186, P30CA016520, U19AI082630, R01AI105343, U01AI095608, P01AI112521)
- Basser Research Center for BRCA
- Abramson Cancer Center Translational Center of Excellence in Pancreatic Cancer
- Department of Defense Era of Hope Scholar (W81XWH-09-1-0339)
- NCI (R01CA172651)
- Merck
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- immune checkpoint inhibitor resistance, type I interferon, interferon-gamma, PD-1 pathway, PD-L1, STAT1, interferon-stimulated genes, T cell inhibitory receptors, T cell exhaustion, radiotherapy, tumor immune microenvironment, resistance biomarkers, anti-PD-1 therapy
- MeSH terms
- Animals, Humans, Interferons, Melanoma, Neoplasm Transplantation, T-Lymphocytes, Radioimmunotherapy, Drug Resistance, Neoplasm, Cell Line, Tumor, STAT1 Transcription Factor, Mice, B7-H1 Antigen, CTLA-4 Antigen, Heterografts
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