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         description:A report of RNA 5-methylcytosine oxidation by mammalian Tet2, showing that Tet2 promotes infection-induced myelopoiesis in mice via a mechanism involving the repression of Socs3 mRNA, a previously unknown regulatory role of Tet2 at the epitranscriptomic level. Messenger RNA (mRNA) can be modified biochemically without changing its ribonucleotide sequence. These mRNA modifications are essential for post-transcriptional regulation of gene expression. Xuetao Cao and colleagues report the oxidation of the RNA base 5-methylcytosine (5-mC) into 5-hydroxymethylcytosine (5-hmC) by the mammalian Tet2 enzyme. The authors also show that Tet2 promotes infection-induced myelopoiesis—generation of innate immune cells from the bone marrow—in mice. This effect occurs through a mechanism involving the destabilization of Socs3 mRNA caused by decreased levels of 5-mC. These findings highlight the role of epitranscriptome modifications in mammalian physiology. Varieties of RNA modification form the epitranscriptome for post-transcriptional regulation1. 5-Methylcytosine (5-mC) is a sparse RNA modification in messenger RNA (mRNA) under physiological conditions2. The function of RNA 5-hydroxymethylcytosine (5-hmC) oxidized by ten-eleven translocation (Tet) proteins in Drosophila has been revealed more recently3,4. However, the turnover and function of 5-mC in mammalian mRNA have been largely unknown. Tet2 suppresses myeloid malignancies mostly in an enzymatic activity-dependent manner5, and is important in resolving inflammatory response in an enzymatic activity-independent way6. Myelopoiesis is a common host immune response in acute and chronic infections; however, its epigenetic mechanism needs to be identified. Here we demonstrate that Tet2 promotes infection-induced myelopoiesis in an mRNA oxidation-dependent manner through Adar1-mediated repression of Socs3 expression at the post-transcription level. Tet2 promotes both abdominal sepsis-induced emergency myelopoiesis and parasite-induced mast cell expansion through decreasing mRNA levels of Socs3, a key negative regulator of the JAK–STAT pathway that is critical for cytokine-induced myelopoiesis. Tet2 represses Socs3 expression through Adar1, which binds and destabilizes Socs3 mRNA in a RNA editing-independent manner. For the underlying mechanism of Tet2 regulation at the mRNA level, Tet2 mediates oxidation of 5-mC in mRNA. Tet2 deficiency leads to the transcriptome-wide appearance of methylated cytosines, including ones in the 3′ untranslated region of Socs3, which influences double-stranded RNA formation for Adar1 binding, probably through cytosine methylation-specific readers, such as RNA helicases. Our study reveals a previously unknown regulatory role of Tet2 at the epitranscriptomic level, promoting myelopoiesis during infection in the mammalian system by decreasing 5-mCs in mRNAs. Moreover, the inhibitory function of cytosine methylation on double-stranded RNA formation and Adar1 binding in mRNA reveals its new physiological role in the mammalian system.
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            name:Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences
            address:
               name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
               type:PostalAddress
            type:Organization
      name:Kai Zhao
      affiliation:
            name:Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences
            address:
               name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
               type:PostalAddress
            type:Organization
      name:Chunmei Wang
      affiliation:
            name:Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences
            address:
               name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
               type:PostalAddress
            type:Organization
      name:Nan Li
      affiliation:
            name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University
            address:
               name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
               type:PostalAddress
            type:Organization
      name:Xuetao Cao
      affiliation:
            name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University
            address:
               name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
               type:PostalAddress
            type:Organization
            name:Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences
            address:
               name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
               type:PostalAddress
            type:Organization
      email:[email protected]
PostalAddress:
      name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
      name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
      name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
      name:Institute of Immunology, Zhejiang University School of Medicine, Hangzhou, China
      name:Institute of Immunology, Zhejiang University School of Medicine, Hangzhou, China
      name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
      name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
      name:Institute of Immunology, Zhejiang University School of Medicine, Hangzhou, China
      name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
      name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
      name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
      name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
      name:National Key Laboratory of Medical Immunology & Institute of Immunology, Second Military Medical University, Shanghai, China
      name:Department of Immunology & Center for Immunotherapy, Institute of Basic Medical Sciences, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
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