Cited by 407Cancer Immunotherapy and BiomarkersCancer, Hypoxia, and MetabolismT-cell and B-cell Immunology

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Cancer mediates effector T cell dysfunction by targeting microRNAs and EZH2 via glycolysis restriction

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Zhao, Ende, Maj, Tomasz, Kryczek, Ilona, Li, Wei, Wu, Ke, Zhao, Lili, Wei, Shuang, Crespo, Joel, Wan, Shanshan, Vatan, Linda, Szeliga, Wojciech, Shao, Irene, Wang, Yin, Liu, Yan, Varambally, Sooryanarayana, Chinnaiyan, Arul M, Welling, Theodore H, Marquez, Victor, Kotarski, Jan, Wang, Hongbo, Wang, Zehua, Zhang, Yi, Liu, Rebecca, Wang, Guobin, Zou, Weiping·2016·Nature Immunology

DOI 10.1038/ni.3313PMC PMC4684796

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Abstract

Aerobic glycolysis regulates T cell function. However, whether and how primary cancer alters T cell glycolytic metabolism and affects tumor immunity in cancer patients remains a question. Here we found that ovarian cancers imposed glucose restriction on T cells and dampened their function via maintaining high expression of microRNAs miR-101 and miR-26a, which constrained expression of the methyltransferase EZH2. EZH2 activated the Notch pathway by suppressing Notch repressors Numb and Fbxw7 via trimethylation of histone H3 at Lys27 and, consequently, stimulated T cell polyfunctional cytokine expression and promoted their survival via Bcl-2 signaling. Moreover, small hairpin RNA-mediated knockdown of human EZH2 in T cells elicited poor antitumor immunity. EZH2(+)CD8(+) T cells were associated with improved survival in patients. Together, these data unveil a metabolic target and mechanism of cancer immune evasion.

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Authors: Zhao, E., Maj, T., Kryczek, I., Li, W., Wu, K., Zhao, L., Wei, S., Crespo, J., Wan, S., Vatan, L., Szeliga, W., Shao, I., Wang, Y., Liu, Y., Varambally, S., Chinnaiyan, A. M., Welling, T. H., Marquez, V., Kotarski, J., Wang, H., Wang, Z., Zhang, Y., Liu, R., Wang, G., & Zou, W.
Affiliations: University of Michigan (US)
Medical University of Lublin (PL)
Wuhan Union Hospital (CN)
Corresponding author: Wang, Guobin
Zou, Weiping
ORCID: Zhao, Ende
Maj, Tomasz
Kryczek, Ilona
Li, Wei
Wu, Ke
Zhao, Lili
Wei, Shuang
Crespo, Joel
Wan, Shanshan
Vatan, Linda
Szeliga, Wojciech
Liu, Yan
Varambally, Sooryanarayana
Chinnaiyan, Arul M
Kotarski, Jan
Wang, Hongbo
Wang, Zehua
Liu, Rebecca
Wang, Guobin
Zou, Weiping
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2015-11-02
Volume: 17
Issue: 1
Pages: 95-103
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni.3313
PMC: PMC4684796
OpenAlex: W2202401513
Cited by: 405
References: 50
Citations by year: 2026: 19 · 2025: 30 · 2024: 37 · 2023: 35 · 2022: 54 · 2021: 51 · 2020: 42 · 2019: 34 · 2018: 38 · 2017: 35 · 2016: 29 · 2015: 1
FWCI: 15.00
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Heart, Lung, and Blood Institute (R01HL127351)
National Cancer Institute (R01CA092562, CA099985, R01CA123088, R01CA152470, R01CA156685, R01CA172106, CA123088, 5P30 CA 46592, CA156685, R01CA171306, R01CA193136, CA171306, R01CA099985, R01CA190176, P30CA046592)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: tumor immune evasion, EZH2, microRNA, miR-101, miR-26a, glycolysis, glucose restriction, Notch signaling, H3K27me3, Numb, FBXW7, T cell apoptosis, ovarian cancer, antitumor immunity, CD8+ T cells
MeSH terms: Enhancer of Zeste Homolog 2 Protein, Animals, Cell Separation, Female, Flow Cytometry, Fluorescent Antibody Technique, Glycolysis, Humans, Melanoma, Experimental, Mice, Inbred C57BL, Neoplasms, Ovarian Neoplasms, T-Lymphocytes, Transfection, Immunoblotting, Gene Expression Regulation, Neoplastic, Tumor Escape, MicroRNAs, Tissue Array Analysis, Chromatin Immunoprecipitation, Real-Time Polymerase Chain Reaction, Polycomb Repressive Complex 2

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Cancer mediates effector T cell dysfunction by targeting microRNAs and EZH2 via glycolysis restriction

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