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Iron-dependent histone 3 lysine 9 demethylation controls B cell proliferation and humoral immune responses

Author

Listed:
  • Yuhang Jiang

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Cuifeng Li

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Qian Wu

    (Zhejiang University School of Medicine
    China Agricultural University
    Zhengzhou University)

  • Peng An

    (Zhejiang University School of Medicine
    China Agricultural University
    Zhengzhou University)

  • Laiquan Huang

    (The First Affiliated Hospital of Wannan Medical College)

  • Jia Wang

    (Zhejiang University School of Medicine
    China Agricultural University
    Zhengzhou University)

  • Chen Chen

    (Zhongshan Hospital Fudan University)

  • Xi Chen

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Fan Zhang

    (Zhejiang University School of Medicine
    China Agricultural University
    Zhengzhou University)

  • Li Ma

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Sanhong Liu

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Hanqing He

    (Zhejiang Provincial Center for Disease Control and Prevention)

  • Shuyun Xie

    (Zhejiang Provincial Center for Disease Control and Prevention)

  • Yangbai Sun

    (Zhejiang Provincial Center for Disease Control and Prevention)

  • Hanshao Liu

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Yu Zhan

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Yu Tao

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Zhi Liu

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Xiaohua Sun

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Yiming Hu

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Qi Wang

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Deji Ye

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Jie Zhang

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Shanhua Zou

    (Zhongshan Hospital Fudan University)

  • Ying Wang

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Gang Wei

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Yongzhong Liu

    (Shanghai Jiao-Tong University School of Medicine)

  • Yufang Shi

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Y. Eugene Chin

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Yongqiang Hao

    (Shanghai JiaoTong University School of Medicine)

  • Fudi Wang

    (Zhejiang University School of Medicine
    China Agricultural University
    Zhengzhou University)

  • Xiaoren Zhang

    (Guangzhou Medical University
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

Abstract

Trace elements play important roles in human health, but little is known about their functions in humoral immunity. Here, we show an important role for iron in inducing cyclin E and B cell proliferation. We find that iron-deficient individuals exhibit a significantly reduced antibody response to the measles vaccine when compared to iron-normal controls. Mice with iron deficiency also exhibit attenuated T-dependent or T-independent antigen-specific antibody responses. We show that iron is essential for B cell proliferation; both iron deficiency and α-ketoglutarate inhibition could suppress cyclin E1 induction and S phase entry of B cells upon activation. Finally, we demonstrate that three demethylases, KDM2B, KDM3B and KDM4C, are responsible for histone 3 lysine 9 (H3K9) demethylation at the cyclin E1 promoter, cyclin E1 induction and B cell proliferation. Thus, our data reveal a crucial role of H3K9 demethylation in B cell proliferation, and the importance of iron in humoral immunity.

Suggested Citation

  • Yuhang Jiang & Cuifeng Li & Qian Wu & Peng An & Laiquan Huang & Jia Wang & Chen Chen & Xi Chen & Fan Zhang & Li Ma & Sanhong Liu & Hanqing He & Shuyun Xie & Yangbai Sun & Hanshao Liu & Yu Zhan & Yu Ta, 2019. "Iron-dependent histone 3 lysine 9 demethylation controls B cell proliferation and humoral immune responses," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-11002-5
    DOI: 10.1038/s41467-019-11002-5
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    Cited by:

    1. Lizhen Zhu & Geng Li & Zhixin Liang & Tuan Qi & Kui Deng & Jiancheng Yu & Yue Peng & Jusheng Zheng & Yan Song & Xing Chang, 2023. "Microbiota-assisted iron uptake promotes immune tolerance in the intestine," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Kai Zhang & Kaiyuan Liu & Benxia Hu & Genyu Du & Xinyu Chen & Lingling Xiao & Yingchao Zhang & Luyao Jiang & Na Jing & Chaping Cheng & Jinming Wang & Penghui Xu & You Wang & Pengfei Ma & Guanglei Zhua, 2024. "Iron-loaded cancer-associated fibroblasts induce immunosuppression in prostate cancer," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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