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

Glucose availability is limiting in tumor environments. Zou and colleagues show that reduced glycolytic metabolism in T cells within tumors suppresses expression of the methyltransferase EZH2, which limits production of antitumor effector molecules and enhances T cell apoptosis. Aerobic glycolysis r...

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Published inNature immunology Vol. 17; no. 1; pp. 95 - 103
Main Authors 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
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.01.2016
Nature Publishing Group
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Abstract Glucose availability is limiting in tumor environments. Zou and colleagues show that reduced glycolytic metabolism in T cells within tumors suppresses expression of the methyltransferase EZH2, which limits production of antitumor effector molecules and enhances T cell apoptosis. 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.
AbstractList 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.
Aerobic glycolysis regulates T cell function. However, if and how primary cancer alters T cell glycolytic metabolism and affects tumor immunity remains a question in cancer patients. Here we report that ovarian cancers imposed glucose restriction on T cells and dampened their function via maintaining high expression of microRNA101 and microRNA26a, which constrained expression of the methyltransferase EZH2. EZH2 activated the Notch pathway by suppressing Notch repressors, Numb and Fbxw7, via H3K27me3, and consequently stimulated T cell polyfunctional cytokine expression and promoted their survival via Bcl-2 signaling. Moreover, human shRNA-knockdown- EZH2 -deficient T cells elicited poor anti-tumor immunity. EZH2 + CD8 + T cells were associated with improved cancer patient survival. Together, the data unveil a novel metabolic target and mechanism of cancer immune evasion.
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 super(+)CD8 super(+) T cells were associated with improved survival in patients. Together, these data unveil a metabolic target and mechanism of cancer immune evasion.
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.sup.+][CD8.sup.+] T cells were associated with improved survival in patients. Together, these data unveil a metabolic target and mechanism of cancer immune evasion.
Glucose availability is limiting in tumor environments. Zou and colleagues show that reduced glycolytic metabolism in T cells within tumors suppresses expression of the methyltransferase EZH2, which limits production of antitumor effector molecules and enhances T cell apoptosis. 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.
Audience Academic
Author Wan, Shanshan
Kryczek, Ilona
Wang, Hongbo
Zhao, Ende
Wang, Yin
Li, Wei
Zhao, Lili
Zhang, Yi
Wang, Zehua
Shao, Irene
Liu, Rebecca
Chinnaiyan, Arul M
Kotarski, Jan
Zou, Weiping
Maj, Tomasz
Wu, Ke
Crespo, Joel
Varambally, Sooryanarayana
Vatan, Linda
Welling, Theodore H
Szeliga, Wojciech
Marquez, Victor
Liu, Yan
Wei, Shuang
Wang, Guobin
AuthorAffiliation 1 Department of Surgery, University of Michigan School of Medicine, Ann Arbor, MI
3 Department of Biostatistics, University of Michigan School of Medicine, Ann Arbor, MI
6 The First Department of Gynecologic Oncology and Gynecology, Medical University of Lublin, Poland, 20-081
7 Department of Internal Medicine, University of Michigan School of Medicine, Ann Arbor, MI
2 Departments of Surgery, and Obstetrics and Gynecology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
4 Department of Pathology, University of Michigan School of Medicine, Ann Arbor, MI
9 Graduate Programs in Immunology and Cancer Biology, University of Michigan, Ann Arbor, MI
10 Comprehensive Cancer Center, University of Michigan, Ann Arbor, MI
5 Chemical Biology Laboratory, Center for Cancer Research, NCI-Frederick, Frederick, Maryland
8 Department of Obstetrics and Gynecology, University of Michigan School of Medicine, Ann Arbor, MI
AuthorAffiliation_xml – name: 6 The First Department of Gynecologic Oncology and Gynecology, Medical University of Lublin, Poland, 20-081
– name: 9 Graduate Programs in Immunology and Cancer Biology, University of Michigan, Ann Arbor, MI
– name: 1 Department of Surgery, University of Michigan School of Medicine, Ann Arbor, MI
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– name: 10 Comprehensive Cancer Center, University of Michigan, Ann Arbor, MI
– name: 3 Department of Biostatistics, University of Michigan School of Medicine, Ann Arbor, MI
– name: 2 Departments of Surgery, and Obstetrics and Gynecology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
– name: 8 Department of Obstetrics and Gynecology, University of Michigan School of Medicine, Ann Arbor, MI
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26523864$$D View this record in MEDLINE/PubMed
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Snippet Glucose availability is limiting in tumor environments. Zou and colleagues show that reduced glycolytic metabolism in T cells within tumors suppresses...
Aerobic glycolysis regulates T cell function. However, whether and how primary cancer alters T cell glycolytic metabolism and affects tumor immunity in cancer...
Aerobic glycolysis regulates T cell function. However, if and how primary cancer alters T cell glycolytic metabolism and affects tumor immunity remains a...
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SubjectTerms 13/1
13/106
13/109
13/2
13/21
13/31
13/44
13/51
13/89
13/95
631/250/1619/554/1834/1269
631/250/2502/2170
631/250/580/1884
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Animals
Biomedicine
Cell metabolism
Cell Separation
Chromatin Immunoprecipitation
Development and progression
Enhancer of Zeste Homolog 2 Protein
Female
Flow Cytometry
Fluorescent Antibody Technique
Gene Expression Regulation, Neoplastic - immunology
Genetic aspects
Glycolysis
Humans
Immunoblotting
Immunology
Infectious Diseases
Melanoma, Experimental - immunology
Mice, Inbred C57BL
MicroRNA
MicroRNAs
Neoplasms - immunology
Ovarian cancer
Ovarian Neoplasms - immunology
Polycomb Repressive Complex 2 - immunology
Properties
Real-Time Polymerase Chain Reaction
T cells
T-Lymphocytes - immunology
Tissue Array Analysis
Transfection
Tumor Escape - immunology
Title Cancer mediates effector T cell dysfunction by targeting microRNAs and EZH2 via glycolysis restriction
URI https://link.springer.com/article/10.1038/ni.3313
https://www.ncbi.nlm.nih.gov/pubmed/26523864
https://www.proquest.com/docview/1767083597
https://search.proquest.com/docview/1750435876
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https://pubmed.ncbi.nlm.nih.gov/PMC4684796
Volume 17
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