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Ca2+ transients on the T cell surface trigger rapid integrin activation in a timescale of seconds

Author

Listed:
  • Yue Li

    (Chinese Academy of Sciences)

  • ShiHui Wang

    (Chinese Academy of Sciences)

  • YouHua Zhang

    (Tongji University)

  • ZhaoYuan Liu

    (Chinese Academy of Sciences)

  • YunZhe Zheng

    (Chinese Academy of Sciences)

  • Kun Zhang

    (Chinese Academy of Sciences)

  • ShiYang Chen

    (University of Chinese Academy of Sciences)

  • XiaoYing Lv

    (Tongji University)

  • MengWen Huang

    (University of Chinese Academy of Sciences)

  • XingChao Pan

    (Chinese Academy of Sciences)

  • YaJuan Zheng

    (Chinese Academy of Sciences)

  • MengYa Yuan

    (Chinese Academy of Sciences)

  • GaoXiang Ge

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

  • Yi Arial Zeng

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

  • ChangDong Lin

    (Tongji University
    Tongji University)

  • JianFeng Chen

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

Abstract

One question in lymphocyte homing is how integrins are rapidly activated to enable immediate arrest of fast rolling lymphocytes upon encountering chemokines at target vascular beds given the slow chemokine-induced integrin inside-out activation. Herein we demonstrate that chemokine CCL25-triggered Ca2+ influx induces T cell membrane-proximal external Ca2+ concentration ([Ca2+]ex) drop in 6 s from physiological concentration 1.2 mM to 0.3 mM, a critical extracellular Ca2+ threshold for inducing αLβ2 activation, triggering rapid αLβ2 activation and T cell arrest before occurrence of αLβ2 inside-out activation. Talin knockdown inhibits the slow inside-out activation of αLβ2 but not [Ca2+]ex drop-triggered αLβ2 quick activation. Blocking Ca2+ influx significantly suppresses T cell rolling-to-arrest transition and homing to skin lesions in a mouse psoriasis model, thus alleviating skin inflammation. [Ca2+]ex decrease-triggered rapid integrin activation bridges the gap between initial chemokine stimulation and slow integrin inside-out activation, ensuring immediate lymphocyte arrest and subsequent diapedesis on the right location.

Suggested Citation

  • Yue Li & ShiHui Wang & YouHua Zhang & ZhaoYuan Liu & YunZhe Zheng & Kun Zhang & ShiYang Chen & XiaoYing Lv & MengWen Huang & XingChao Pan & YaJuan Zheng & MengYa Yuan & GaoXiang Ge & Yi Arial Zeng & C, 2024. "Ca2+ transients on the T cell surface trigger rapid integrin activation in a timescale of seconds," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50464-0
    DOI: 10.1038/s41467-024-50464-0
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    References listed on IDEAS

    as
    1. Junji Suzuki & Kazunori Kanemaru & Kuniaki Ishii & Masamichi Ohkura & Yohei Okubo & Masamitsu Iino, 2014. "Imaging intraorganellar Ca2+ at subcellular resolution using CEPIA," Nature Communications, Nature, vol. 5(1), pages 1-13, September.
    2. Michelle A. Lowes & Anne M. Bowcock & James G. Krueger, 2007. "Pathogenesis and therapy of psoriasis," Nature, Nature, vol. 445(7130), pages 866-873, February.
    3. Zhenghui Liu & Tadayuki Yago & Nan Zhang & Sumith R. Panicker & Ying Wang & Longbiao Yao & Padmaja Mehta-D’souza & Lijun Xia & Cheng Zhu & Rodger P. McEver, 2017. "L-selectin mechanochemistry restricts neutrophil priming in vivo," Nature Communications, Nature, vol. 8(1), pages 1-14, August.
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