Inactivation of AMPK leads to attenuation of antigen presentation and immune evasion in lung adenocarcinoma
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Abstract
Purpose: Mutations in STK11 (LKB1) occur in 17% of lung adenocarcinoma (LUAD) and drive a suppressive (cold) tumor immune microenvironment (TIME) and resistance to immunotherapy. The mechanisms underpinning the establishment and maintenance of a cold TIME in LKB1-mutant LUAD remain poorly understood. In this study, we investigated the role of the LKB1 substrate AMPK in immune evasion in human non—small cell lung cancer (NSCLC) and mouse models and explored the mechanisms involved. Experimental Design: We addressed the role of AMPK in immune evasion in NSCLC by correlating AMPK phosphorylation and immune-suppressive signatures and by deleting AMPKα1 (Prkaa1) and AMPKα2 (Prkaa2) in a KrasG12D-driven LUAD. Furthermore, we dissected the molecular mechanisms involved in immune evasion by comparing gene-expression signatures, AMPK activity, and immune infiltration in mouse and human LUAD and gain or loss-of-function experiments with LKB1- or AMPK-deficient cell lines. Results: Inactivation of both AMPKα1 and AMPKα2 together with Kras activation accelerated tumorigenesis and led to tumors with reduced infiltration of CD8+/CD4+ T cells and gene signatures associated with a suppressive TIME. These signatures recapitulate those in Lkb1-deleted murine LUAD and in LKB1-deficient human NSCLC. Interestingly, a similar signature is noted in human NSCLC with low AMPK activity. In mechanistic studies, we find that compromised LKB1 and AMPK activity leads to attenuated antigen presentation in both LUAD mouse models and human NSCLC. Conclusions: The results provide evidence that the immune evasion noted in LKB1-inactivated lung cancer is due to subsequent inactivation of AMPK and attenuation of antigen presentation.
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STK11-mutant tumors are characterized by low levels of antigen presentation compared with tumors wild-type for STK11.
“STK11-mutant tumors are characterized by lower T-cell infiltration (1, 7, 8), higher levels of immune-suppressive neutrophils (8), and low levels of antigen presentation (9, 10) compared with those wild-type for STK11, contributing to their immune evasive phenotype.”
From TNG260 Is a Small-Molecule CoREST Inhibitor That Sensitizes <i>STK11</i> -Mutant Tumors to Anti–PD-1 Immunotherapy (2025) · cites this paper as [10]
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- Authors
- Gao, Y., Päivinen, P., Tripathi, S., Domènech-Moreno, E., Wong, I. P. L., Vaahtomeri, K., Nagaraj, A. S., Talwelkar, S. S., Foretz, M., Verschuren, E. W., Viollet, B., Yan, Y., & Mäkelä, T. P.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- University of Helsinki (FI)
- 4Institute for Molecular Medicine Finland (FIMM), HiLIFE, University of Helsinki, Helsinki, Finland.
- Centre National de la Recherche Scientifique (FR)
- 5Université de Paris, Institut Cochin, CNRS, INSERM, Paris, France.
- Corresponding author
- Yan, Yan
- ORCID
- Venue
- Clinical Cancer Research
- Published
- 2022-01-01
- Volume
- 28
- Issue
- 1
- Pages
- 227-237
- ISSN
- 1078-0432 (ISSN-L)
- 1557-3265
- OpenAlex
- W3205833360
- Cited by
- 40
- References
- 47
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 2 · 2023: 20 · 2022: 3
- FWCI
- 2.73
- Type
- journal article
- Language
- en
- Open access
- green
- hal.science
- Licence
- other-oa
- Locations
- Clinical Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Työväentutkimus Vuosikirja (submittedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- AMPK, LKB1, STK11 mutation, lung adenocarcinoma, non-small cell lung cancer, tumor immune microenvironment, immune evasion, antigen presentation, cold tumors, KRAS G12D, PRKAA1, PRKAA2, CD8+ T cell infiltration, immunotherapy resistance
- MeSH terms
- Adenocarcinoma of Lung, Animals, Carcinoma, Non-Small-Cell Lung, Humans, Lung Neoplasms, Antigen Presentation, Mice, AMP-Activated Protein Kinases, Immune Evasion, Tumor Microenvironment
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