Functional genomic landscape of cancer-intrinsic evasion of killing by T cells
Open accessAbstract
The genetic circuits that allow cancer cells to evade destruction by the host immune system remain poorly understood 1-3. Here, to identify a phenotypically robust core set of genes and pathways that enable cancer cells to evade killing mediated by cytotoxic T lymphocytes (CTLs), we performed genome-wide CRISPR screens across a panel of genetically diverse mouse cancer cell lines that were cultured in the presence of CTLs. We identify a core set of 182 genes across these mouse cancer models, the individual perturbation of which increases either the sensitivity or the resistance of cancer cells to CTL-mediated toxicity. Systematic exploration of our dataset using genetic co-similarity reveals the hierarchical and coordinated manner in which genes and pathways act in cancer cells to orchestrate their evasion of CTLs, and shows that discrete functional modules that control the interferon response and tumour necrosis factor (TNF)-induced cytotoxicity are dominant sub-phenotypes. Our data establish a central role for genes that were previously identified as negative regulators of the type-II interferon response (for example, Ptpn2, Socs1 and Adar1) in mediating CTL evasion, and show that the lipid-droplet-related gene Fitm2 is required for maintaining cell fitness after exposure to interferon-γ (IFNγ). In addition, we identify the autophagy pathway as a conserved mediator of the evasion of CTLs by cancer cells, and show that this pathway is required to resist cytotoxicity induced by the cytokines IFNγ and TNF. Through the mapping of cytokine- and CTL-based genetic interactions, together with in vivo CRISPR screens, we show how the pleiotropic effects of autophagy control cancer-cell-intrinsic evasion of killing by CTLs and we highlight the importance of these effects within the tumour microenvironment. Collectively, these data expand our knowledge of the genetic circuits that are involved in the evasion of the immune system by cancer cells, and highlight genetic interactions that contribute to phenotypes associated with escape from killing by CTLs.
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Pooled in vivo and in vitro CRISPR-Cas9 based screening have nominated several tumour intrinsic drivers of resistance to immunotherapy, but therapeutic applications of these findings remain limited.
“Pooled in vivo and in vitro CRISPR-Cas9 based screening have nominated several tumour intrinsic drivers of resistance to immunotherapy 4,8-11 , but therapeutic applications of these findings remain limited.”
From Targeting TBK1 to overcome resistance to cancer immunotherapy (2023) · cites this paper as [9]
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 [9]
TBK1 has been nominated as a candidate immune evasion gene.
“thus it is surprising that TBK1 has been nominated as a candidate immune evasion gene 4,9-11”
From Targeting TBK1 to overcome resistance to cancer immunotherapy (2023) · cites this paper as [9]
A CRISPR-Cas9 screen performed across multiple cell lines indicates that autophagy proficiency entails the inherent ability to evade immune detection.
“This result has been further reinforced in a CRISPR‐Cas9 screen performed across multiple cell lines, indicating that autophagy proficiency entails the inherent ability to evade immune detection (Lawson et al, 2020).”
From Autophagy in major human diseases (2021) · cites this paper as Lawson et al, 2020
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- Authors
- Lawson, K. A., Sousa, C. M., Zhang, X., Kim, E., Akthar, R., Caumanns, J. J., Yao, Y., Mikolajewicz, N., Ross, C., Brown, K. R., Zid, A. A., Fan, Z. P., Hui, S., Krall, J. A., Simons, D. M., Slater, C. J., De Jesus, V., Tang, L., Singh, R., Goldford, J. E., Martin, S., Huang, Q., Francis, E. A., Habsid, A., Climie, R., Tieu, D., Wei, J., Li, R., Tong, A. H. Y., Aregger, M., Chan, K. S., Han, H., Wang, X., Mero, P., Brumell, J. H., Finelli, A., Ailles, L., Bader, G., Smolen, G. A., Kingsbury, G. A., Hart, T., Kung, C., & Moffat, J.
- Affiliations
- University Health Network (CA)
- Agios Pharmaceuticals (United States) (US)
- University of Toronto (CA)
- The University of Texas MD Anderson Cancer Center (US)
- Hospital for Sick Children (CA)
- Ontario Institute for Cancer Research (CA)
- Corresponding author
- Moffat, Jason
- ORCID
- Lawson, Keith A.
- Sousa, Cristovão M.
- Zhang, Xiaoyu
- Kim, Eiru
- Mikolajewicz, Nicholas
- Brown, Kevin R.
- Fan, Zi Peng
- Hui, Shirley
- Krall, Jordan A.
- Simons, Donald M.
- Slater, Chloe J.
- Goldford, Joshua E.
- Huang, Qian
- Francis, Elizabeth A.
- Tieu, David
- Wei, Jiarun
- Tong, Amy Hin Yan
- Aregger, Michael
- Chan, Katherine S.
- Han, Hong
- Wang, Xiaowei
- Brumell, John H.
- Finelli, Antonio
- Ailles, Laurie
- Bader, Gary
- Smolen, Gromoslaw A.
- Kingsbury, Gillian A.
- Hart, Traver
- Moffat, Jason
- Venue
- Nature
- Published
- 2020-09-23
- Volume
- 586
- Issue
- 7827
- Pages
- 120-126
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC9014559
- OpenAlex
- W3088246260
- Cited by
- 443
- References
- 44
- Citations by year
- 2026: 50 · 2025: 80 · 2024: 80 · 2023: 78 · 2022: 89 · 2021: 59 · 2020: 6
- FWCI
- 21.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Cancer Institute (P30CA016672)
- National Institute of General Medical Sciences (R35GM130119)
- 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 › interferon and immune responses
- Keywords
- tumor immune evasion, cytotoxic T lymphocytes, CTL-mediated killing, interferon-gamma, TNF-α, autophagy, lipid droplets, PTPN2, SOCS1, ADAR1, tumor microenvironment, genetic interactions
- MeSH terms
- Animals, Autophagy, Female, Humans, Interferon-gamma, Male, Neoplasms, T-Lymphocytes, Cytotoxic, Reproducibility of Results, Signal Transduction, NF-kappa B, Genome, Tumor Escape, Genomics, Cell Line, Tumor, Mice, Genes, Neoplasm
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