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         headline:Cancer SLC43A2 alters T cell methionine metabolism and histone methylation
         description:Abnormal epigenetic patterns correlate with effector T cell malfunction in tumours1–4, but the cause of this link is unknown. Here we show that tumour cells disrupt methionine metabolism in CD8+ T cells, thereby lowering intracellular levels of methionine and the methyl donor S-adenosylmethionine (SAM) and resulting in loss of dimethylation at lysine 79 of histone H3 (H3K79me2). Loss of H3K79me2 led to low expression of STAT5 and impaired T cell immunity. Mechanistically, tumour cells avidly consumed methionine and outcompeted T cells for methionine by expressing high levels of the methionine transporter SLC43A2. Genetic and biochemical inhibition of tumour SLC43A2 restored H3K79me2 in T cells, thereby boosting spontaneous and checkpoint-induced tumour immunity. Moreover, methionine supplementation improved the expression of H3K79me2 and STAT5 in T cells, and this was accompanied by increased T cell immunity in tumour-bearing mice and patients with colon cancer. Clinically, tumour SLC43A2 correlated negatively with T cell histone methylation and functional gene signatures. Our results identify a mechanistic connection between methionine metabolism, histone patterns, and T cell immunity in the tumour microenvironment. Thus, cancer methionine consumption is an immune evasion mechanism, and targeting cancer methionine signalling may provide an immunotherapeutic approach. Expression of the transporter SLC43A2 by tumour cells allows them to outcompete T cells for methionine and thereby disrupt the survival and function of tumour-infiltrating T cells.
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      headline:Cancer SLC43A2 alters T cell methionine metabolism and histone methylation
      description:Abnormal epigenetic patterns correlate with effector T cell malfunction in tumours1–4, but the cause of this link is unknown. Here we show that tumour cells disrupt methionine metabolism in CD8+ T cells, thereby lowering intracellular levels of methionine and the methyl donor S-adenosylmethionine (SAM) and resulting in loss of dimethylation at lysine 79 of histone H3 (H3K79me2). Loss of H3K79me2 led to low expression of STAT5 and impaired T cell immunity. Mechanistically, tumour cells avidly consumed methionine and outcompeted T cells for methionine by expressing high levels of the methionine transporter SLC43A2. Genetic and biochemical inhibition of tumour SLC43A2 restored H3K79me2 in T cells, thereby boosting spontaneous and checkpoint-induced tumour immunity. Moreover, methionine supplementation improved the expression of H3K79me2 and STAT5 in T cells, and this was accompanied by increased T cell immunity in tumour-bearing mice and patients with colon cancer. Clinically, tumour SLC43A2 correlated negatively with T cell histone methylation and functional gene signatures. Our results identify a mechanistic connection between methionine metabolism, histone patterns, and T cell immunity in the tumour microenvironment. Thus, cancer methionine consumption is an immune evasion mechanism, and targeting cancer methionine signalling may provide an immunotherapeutic approach. Expression of the transporter SLC43A2 by tumour cells allows them to outcompete T cells for methionine and thereby disrupt the survival and function of tumour-infiltrating T cells.
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         Tumour immunology
         Science
         Humanities and Social Sciences
         multidisciplinary
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            name:University of Michigan Medical School
            address:
               name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
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      name:Shasha Li
      affiliation:
            name:University of Michigan School of Medicine
            address:
               name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
               type:PostalAddress
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            name:University of Michigan Rogel Cancer Center, University of Michigan School of Medicine
            address:
               name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
               type:PostalAddress
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            name:University of Michigan
            address:
               name:Department of Computational Medicine & Bioinformatics, University of Michigan, Ann Arbor, USA
               type:PostalAddress
            type:Organization
      name:Joel Crespo
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            name:University of Michigan School of Medicine
            address:
               name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
               type:PostalAddress
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            name:University of Michigan Rogel Cancer Center, University of Michigan School of Medicine
            address:
               name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
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      name:Zeribe C. Nwosu
      url:http://orcid.org/0000-0003-1641-2045
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            address:
               name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
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      name:Li Zhang
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            name:University of Michigan Medical School
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               name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
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      name:Arkadiusz Czerwonka
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      name:Anna Pawłowska
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            name:University of Michigan School of Medicine
            address:
               name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
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            name:University of Michigan Rogel Cancer Center, University of Michigan School of Medicine
            address:
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               name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
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            name:University of Michigan School of Medicine
            address:
               name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
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            name:University of Michigan Rogel Cancer Center, University of Michigan School of Medicine
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            name:University of Michigan School of Medicine
            address:
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               type:PostalAddress
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            address:
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            name:University of Michigan School of Medicine
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            address:
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            address:
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            address:
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               type:PostalAddress
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            name:University of Michigan
            address:
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               type:PostalAddress
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            name:University of Michigan
            address:
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      name:Arul M. Chinnaiyan
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            name:University of Michigan
            address:
               name:Department of Pathology, University of Michigan, Ann Arbor, USA
               type:PostalAddress
            type:Organization
            name:University of Michigan
            address:
               name:Department of Urology, University of Michigan, Ann Arbor, USA
               type:PostalAddress
            type:Organization
            name:University of Michigan
            address:
               name:Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, USA
               type:PostalAddress
            type:Organization
            name:University of Michigan
            address:
               name:Howard Hughes Medical Institute, University of Michigan, Ann Arbor, USA
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            type:Organization
      name:Witold Zgodziński
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            name:Medical University of Lublin
            address:
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            address:
               name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
               type:PostalAddress
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            name:University of Michigan Medical School
            address:
               name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
               type:PostalAddress
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            address:
               name:Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, USA
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            name:University of Michigan School of Medicine
            address:
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            address:
               name:Graduate Program in Cancer Biology, University of Michigan School of Medicine, Ann Arbor, USA
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      name:Weiping Zou
      url:http://orcid.org/0000-0001-7952-3549
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            address:
               name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
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            address:
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            address:
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            type:Organization
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            address:
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            name:University of Michigan School of Medicine
            address:
               name:Graduate Program in Cancer Biology, University of Michigan School of Medicine, Ann Arbor, USA
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      email:[email protected]
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      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
      name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Computational Medicine & Bioinformatics, University of Michigan, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
      name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
      name:Department of Virology and Immunology, Maria Curie-Skłodowska University, Lublin, Poland
      name:First Chair and Department of Oncological Gynecology and Gynecology, Medical University of Lublin, Lublin, Poland
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, USA
      name:Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, USA
      name:Department of Computational Medicine & Bioinformatics, University of Michigan, Ann Arbor, USA
      name:Department of Pathology, University of Michigan, Ann Arbor, USA
      name:Department of Pathology, University of Michigan, Ann Arbor, USA
      name:Department of Urology, University of Michigan, Ann Arbor, USA
      name:Michigan Center for Translational Pathology, University of Michigan, Ann Arbor, USA
      name:Howard Hughes Medical Institute, University of Michigan, Ann Arbor, USA
      name:Second Department of General, Gastrointestinal Surgery and Surgical Oncology of the Alimentary Tract, Medical University of Lublin, Lublin, Poland
      name:Second Department of General, Gastrointestinal Surgery and Surgical Oncology of the Alimentary Tract, Medical University of Lublin, Lublin, Poland
      name:First Chair and Department of Oncological Gynecology and Gynecology, Medical University of Lublin, Lublin, Poland
      name:First Chair and Department of Oncological Gynecology and Gynecology, Medical University of Lublin, Lublin, Poland
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, USA
      name:Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, USA
      name:Graduate Program in Immunology, University of Michigan School of Medicine, Ann Arbor, USA
      name:Graduate Program in Cancer Biology, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Surgery, University of Michigan School of Medicine, Ann Arbor, USA
      name:Center of Excellence for Cancer Immunology and Immunotherapy, University of Michigan Rogel Cancer Center, University of Michigan School of Medicine, Ann Arbor, USA
      name:Department of Pathology, University of Michigan, Ann Arbor, USA
      name:Graduate Program in Immunology, University of Michigan School of Medicine, Ann Arbor, USA
      name:Graduate Program in Cancer Biology, University of Michigan School of Medicine, Ann Arbor, USA
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