β-Catenin Activation Promotes Immune Escape and Resistance to Anti–PD-1 Therapy in Hepatocellular Carcinoma
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Abstract
PD-1 immune checkpoint inhibitors have produced encouraging results in patients with hepatocellular carcinoma (HCC). However, what determines resistance to anti–PD-1 therapies is unclear. We created a novel genetically engineered mouse model of HCC that enables interrogation of how different genetic alterations affect immune surveillance and response to immunotherapies. Expression of exogenous antigens in MYC;Trp53−/− HCCs led to T cell–mediated immune surveillance, which was accompanied by decreased tumor formation and increased survival. Some antigen-expressing MYC;Trp53−/− HCCs escaped the immune system by upregulating the β-catenin (CTNNB1) pathway. Accordingly, expression of exogenous antigens in MYC;CTNNB1 HCCs had no effect, demonstrating that β-catenin promoted immune escape, which involved defective recruitment of dendritic cells and consequently impaired T-cell activity. Expression of chemokine CCL5 in antigen-expressing MYC;CTNNB1 HCCs restored immune surveillance. Finally, β-catenin–driven tumors were resistant to anti–PD-1. In summary, β-catenin activation promotes immune escape and resistance to anti–PD-1 and could represent a novel biomarker for HCC patient exclusion. Significance: Determinants of response to anti–PD-1 immunotherapies in HCC are poorly understood. Using a novel mouse model of HCC, we show that β-catenin activation promotes immune evasion and resistance to anti–PD-1 therapy and could potentially represent a novel biomarker for HCC patient exclusion. See related commentary by Berraondo et al., p. 1003. This article is highlighted in the In This Issue feature, p. 983
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In a mouse model of hepatocellular carcinoma, activation of WNT-β-catenin signalling promotes immune escape by impairing dendritic cell recruitment and natural killer cell recognition.
“In a mouse model of HCC, activation of WNT–β-catenin signalling promotes immune escape by impairing recruitment of dendritic cells and interfering with recognition by natural killer cells73.”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [73]
The Results and Discussion report that β-catenin activation promotes immune escape in the mouse HCC model by impairing recruitment of CD103+ dendritic cells and the ensuing antigen-specific CD8+ T-cell response. The Results report no significant difference in natural killer cell numbers between the compared livers, but do not establish impaired recognition by those cells. Page numbers were not available in our copy. (LLM, conf=0.90)
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- Authors
- Ruiz de Galarreta, M., Bresnahan, E., Molina-Sánchez, P., Lindblad, K. E., Maier, B., Sia, D., Puigvehi, M., Miguela, V., Casanova-Acebes, M., Dhainaut, M., Villacorta-Martin, C., Singhi, A. D., Moghe, A., von Felden, J., Tal Grinspan, L., Wang, S., Kamphorst, A. O., Monga, S. P., Brown, B. D., Villanueva, A., Llovet, J. M., Merad, M., & Lujambio, A.
- Affiliations
- 1Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, New York.
- Tisch Cancer Institute (US)
- Icahn School of Medicine at Mount Sinai (US)
- 2Liver Cancer Program, Division of Liver Diseases, Department of Medicine, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, New York.
- University of Pittsburgh (US)
- Institució Catalana de Recerca i Estudis Avançats (ES)
- Corresponding author
- Lujambio, Amaia
- ORCID
- Ruiz de Galarreta, Marina
- Molina-Sánchez, Pedro
- Lindblad, Katherine E.
- Maier, Barbara
- Sia, Daniela
- Puigvehi, Marc
- Miguela, Verónica
- Casanova-Acebes, María
- Dhainaut, Maxime
- Singhi, Aatur D.
- Moghe, Akshata
- von Felden, Johann
- Wang, Shuang
- Kamphorst, Alice O.
- Monga, Satdarshan P.
- Brown, Brian D.
- Villanueva, Augusto
- Llovet, Josep M.
- Lujambio, Amaia
- Venue
- Cancer Discovery
- Published
- 2019-08-01
- Volume
- 9
- Issue
- 8
- Pages
- 1124-1141
- ISSN
- 2159-8274 (ISSN-L)
- 2159-8290
- PMC
- PMC6677618
- OpenAlex
- W2952311394
- Cited by
- 912
- References
- 67
- Citations by year
- 2026: 114 · 2025: 121 · 2024: 158 · 2023: 169 · 2022: 156 · 2021: 116 · 2020: 67 · 2019: 11
- FWCI
- 36.78
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Cancer Discovery (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Damon Runyon Cancer Research FoundationDamon Runyon Cancer Research Foundation (Damon Runyon) (DR52-18)
- HHS | NIH | National Cancer InstituteHHS | NIH | National Cancer Institute (NCI) (R37CA230636, P30 CA196521)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- β-catenin signaling, hepatocellular carcinoma, immune evasion, anti-PD-1 resistance, PD-1 inhibitors, tumor surveillance, c-Myc, Trp53, dendritic cell recruitment, T cell function, RANTES, chemokines, genetically engineered mouse models, immunotherapy biomarkers
- MeSH terms
- Antineoplastic Agents, Immunological, Animals, Dendritic Cells, Disease Models, Animal, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Oncogenes, Biomarkers, Tumor, Signal Transduction, Gene Expression, Treatment Outcome, CD8-Positive T-Lymphocytes, Drug Resistance, Neoplasm, Tumor Escape, Xenograft Model Antitumor Assays, Cell Line, Tumor, beta Catenin, 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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