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Exosomal secreted SCIMP regulates communication between macrophages and neutrophils in pneumonia

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  • Xiaolei Pei

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Li Liu

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Jieru Wang

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Changyuan Guo

    (Peking University)

  • Qingqing Li

    (Peking University)

  • Jia Li

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Qian Ren

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Runzhi Ma

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Yi Zheng

    (Peking University)

  • Yan Zhang

    (Peking University)

  • Li Liu

    (Tianjin Medical University)

  • Danfeng Zheng

    (Peking University)

  • Pingzhang Wang

    (Peking University)

  • Ping Jiang

    (Tianjin Medical University)

  • Xiaoming Feng

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Erlie Jiang

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

  • Ying Wang

    (Peking University)

  • Sizhou Feng

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Tianjin Institutes of Health Science)

Abstract

In pneumonia, the deficient or delayed pathogen clearance can lead to pathogen proliferation and subsequent overactive immune responses, inducing acute lung injury (ALI). While screening human genome coding genes using our peripheral blood cell chemotactic platform, we unexpectedly find SLP adaptor and CSK interacting membrane protein (SCIMP), a protein with neutrophil chemotactic activity secreted during ALI. However, the specific role of SCIMP in ALI remains unclear. In this study, we investigate the secretion of SCIMP in exosomes (SCIMPexo) by macrophages after bacterial stimulation, both in vitro and in vivo. We observe a significant increase in the levels of SCIMPexo in bronchoalveolar lavage fluid and serum of pneumonia patients. We also find that bronchial perfusion with SCIMPexo or SCIMP N-terminal peptides increases the survival rate of the ALI model. This occurs due to the chemoattraction and activation of peripheral neutrophils dependent on formyl peptide receptor 1/2 (FPR1/2). Conversely, exosome suppressors and FPR1/2 antagonists decrease the survival rate in the lethal ALI model. Scimp-deficient and Fpr1/2-deficient mice also have lower survival rates and shorter survival times than wild-type mice. However, bronchial perfusion of SCIMP rescues Scimp-deficient mice but not Fpr1/2-deficient mice. Collectively, our findings suggest that the macrophage-SCIMP-FPRs-neutrophil axis plays a vital role in the innate immune process underlying ALI.

Suggested Citation

  • Xiaolei Pei & Li Liu & Jieru Wang & Changyuan Guo & Qingqing Li & Jia Li & Qian Ren & Runzhi Ma & Yi Zheng & Yan Zhang & Li Liu & Danfeng Zheng & Pingzhang Wang & Ping Jiang & Xiaoming Feng & Erlie Ji, 2024. "Exosomal secreted SCIMP regulates communication between macrophages and neutrophils in pneumonia," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44714-4
    DOI: 10.1038/s41467-024-44714-4
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    References listed on IDEAS

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    1. Weiwei Liang & Xinjian Peng & Qingqing Li & Pingzhang Wang & Ping Lv & Quansheng Song & Shaoping She & Shiyang Huang & Keqiang Chen & Wanghua Gong & Wuxing Yuan & Vishal Thovarai & Teizo Yoshimura & C, 2020. "FAM3D is essential for colon homeostasis and host defense against inflammation associated carcinogenesis," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. Rogan A. Grant & Luisa Morales-Nebreda & Nikolay S. Markov & Suchitra Swaminathan & Melissa Querrey & Estefany R. Guzman & Darryl A. Abbott & Helen K. Donnelly & Alvaro Donayre & Isaac A. Goldberg & Z, 2021. "Circuits between infected macrophages and T cells in SARS-CoV-2 pneumonia," Nature, Nature, vol. 590(7847), pages 635-641, February.
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