A Cancer Cell Program Promotes T Cell Exclusion and Resistance to Checkpoint Blockade
Open accessAbstract
Immune checkpoint inhibitors (ICIs) produce durable responses in some melanoma patients, but many patients derive no clinical benefit, and the molecular underpinnings of such resistance remain elusive. Here, we leveraged single-cell RNA sequencing (scRNA-seq) from 33 melanoma tumors and computational analyses to interrogate malignant cell states that promote immune evasion. We identified a resistance program expressed by malignant cells that is associated with T cell exclusion and immune evasion. The program is expressed prior to immunotherapy, characterizes cold niches in situ, and predicts clinical responses to anti-PD-1 therapy in an independent cohort of 112 melanoma patients. CDK4/6-inhibition represses this program in individual malignant cells, induces senescence, and reduces melanoma tumor outgrowth in mouse models in vivo when given in combination with immunotherapy. Our study provides a high-resolution landscape of ICI-resistant cell states, identifies clinically predictive signatures, and suggests new therapeutic strategies to overcome immunotherapy resistance.
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Clinically relevant ICR mechanisms include B2M mutations causing MHC Class I loss, antigen presentation downregulation, and IFNγ-JAK/STAT mutations that impair response to T cell anti-tumor activity.
“Clinically relevant mechanisms of include mutations in beta-2-microglobulin (B2M) resulting in loss of MHC Class I presentation, downregulation of the antigen presentation machinery, and mutations in the IFNγ-JAK/STAT pathway that impair response to T cell mediated anti-tumor activity7–9.”
From Multimodal pooled Perturb-CITE-seq screens in patient models define mechanisms of cancer immune evasion (2021) · cites this paper as [9]
Perturbations of B2M, HLA-A, JAK1, JAK2, STAT1, IFNGR1, and IFNGR2 conferred immune evasion, consistent with clinical resistance mechanisms.
“perturbations of B2M, HLA-A, JAK1, JAK2, STAT1, IFNGR1 and IFNGR2 (Fig. 2d,e, Extended Data Fig. 3e,f, Supplementary Table 2) conferred immune evasion, consistent with clinical mechanisms of resistance to immunotherapy7–9.”
From Multimodal pooled Perturb-CITE-seq screens in patient models define mechanisms of cancer immune evasion (2021) · cites this paper as [9]
An ICR signature predictive of intrinsic ICI resistance was previously identified in a subset of malignant cells from metastatic melanoma patients using scRNA-seq.
“We previously identified an ICR signature, which is predictive of intrinsic resistance to ICI, in a subset of malignant cells in patients with metastatic melanoma using scRNA-seq9.”
From Multimodal pooled Perturb-CITE-seq screens in patient models define mechanisms of cancer immune evasion (2021) · cites this paper as [9]
Upregulation of MYC and CDK4/6 and their transcriptional targets was associated with increased resistance to immunotherapy, and CDK4/6 inhibitors reduced resistance in human and pre-clinical melanoma models.
“consistent with our previously reported patient and pre-clinical data, where we demonstrate that upregulation of MYC and CDK4/6 (and their transcriptional targets) was associated with increased resistance to immunotherapy, and CDK4/6 inhibitors reduced resistance in human and pre-clinical melanoma models9.”
From Multimodal pooled Perturb-CITE-seq screens in patient models define mechanisms of cancer immune evasion (2021) · cites this paper as [9]
This cytokine secretion occurs either after endogenous retrovirus derepression and nucleic acid sensing or after permanent cell cycle blockage with a senescence-associated secretory phenotype.
“This occurs either upon the derepression of endogenous retroviruses and consequent nucleic acid sensing (Goel et al., 2017; Vanpouille-Box et al., 2019) or following the establishment of a permanent cell cycle blockage (i.e., cellular senescence) characterized by an abundant secretory component, the so-called senescence-associated secretory phenotype (SASP) (Jerby-Arnon et al., 2018).”
From Immunomodulation by targeted anticancer agents (2021) · cites this paper as Jerby-Arnon et al., 2018
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- Authors
- Jerby-Arnon, L., Shah, P., Cuoco, M. S., Rodman, C., Su, M.-J., Melms, J. C., Leeson, R., Kanodia, A., Mei, S., Lin, J.-R., Wang, S., Rabasha, B., Liu, D., Zhang, G., Margolais, C., Ashenberg, O., Ott, P. A., Buchbinder, E. I., Haq, R., Hodi, F. S., Boland, G. M., Sullivan, R. J., Frederick, D. T., Miao, B., Moll, T., Flaherty, K. T., Herlyn, M., Jenkins, R. W., Thummalapalli, R., Kowalczyk, M. S., Cañadas, I., Schilling, B., Cartwright, A. N. R., Luoma, A. M., Malu, S., Hwu, P., Bernatchez, C., Forget, M.-A., Barbie, D. A., Shalek, A. K., Tirosh, I., Sorger, P. K., Wucherpfennig, K., Van Allen, E. M., Schadendorf, D., Johnson, B. E., Rotem, A., Rozenblatt-Rosen, O., Garraway, L. A., Yoon, C. H., Izar, B., & Regev, A.
- Affiliations
- Dana-Farber Cancer Institute (US)
- Broad Institute (US)
- Harvard University (US)
- The Wistar Institute (US)
- Massachusetts General Hospital (US)
- Essen University Hospital (DE)
- The University of Texas MD Anderson Cancer Center (US)
- Brigham and Women's Hospital (US)
- Corresponding author
- Izar, Benjamin
- ORCID
- Shah, Parin
- Cuoco, Michael S.
- Rodman, Christopher
- Melms, Johannes C.
- Kanodia, Abhay
- Mei, Shaolin
- Lin, Jia-Ren
- Wang, Shu
- Liu, David
- Zhang, Gao
- Ashenberg, Orr
- Ott, Patrick A.
- Buchbinder, Elizabeth I.
- Haq, Rizwan
- Hodi, F. Stephen
- Boland, Genevieve M.
- Sullivan, Ryan J.
- Frederick, Dennie T.
- Moll, Tabea
- Flaherty, Keith T.
- Herlyn, Meenhard
- Jenkins, Russell W.
- Thummalapalli, Rohit
- Kowalczyk, Monika S.
- Cañadas, Israel
- Schilling, Bastian
- Cartwright, Adam N.R.
- Luoma, Adrienne M.
- Hwu, Patrick
- Bernatchez, Chantale
- Forget, Marie-Andrée
- Barbie, David A.
- Shalek, Alex K.
- Tirosh, Itay
- Sorger, Peter K.
- Wucherpfennig, Kai
- Schadendorf, Dirk
- Johnson, Bruce E.
- Rotem, Asaf
- Garraway, Levi A.
- Yoon, Charles H.
- Izar, Benjamin
- Regev, Aviv
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-11
- Volume
- 175
- Issue
- 4
- Pages
- 984-997.e24
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6410377
- OpenAlex
- W2898830231
- Cited by
- 1,429
- References
- 47
- Citations by year
- 2026: 166 · 2025: 187 · 2024: 195 · 2023: 207 · 2022: 203 · 2021: 202 · 2020: 161 · 2019: 102 · 2018: 3 · 2012: 1
- FWCI
- 44.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- CRI
- NCI (K08-CA222663, 1U24CA180922, R33-CA202820)
- DFCI
- SITC
- Klarman Cell Observatory
- STARR Cancer Consortium
- Koch Institute (P30-CA14051)
- Harvard
- MIT
- AMRF
- Broad Institute
- 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
- melanoma, immune checkpoint inhibitors, immunotherapy resistance, T-cell exclusion, immune evasion, cold tumors, anti-PD-1 therapy, CDK4/6 inhibition, cellular senescence, cancer cell states, predictive biomarkers, combination therapy
- MeSH terms
- Aged, Aged, 80 and over, Animals, Antineoplastic Agents, Female, Humans, Immunotherapy, Male, Melanoma, Mice, Inbred C57BL, Middle Aged, T-Lymphocytes, Tumor Escape, Cell Line, Tumor, Protein Kinase Inhibitors, Cyclin-Dependent Kinase 4, Cyclin-Dependent Kinase 6, Mice, 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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