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Inhibition of neutrophil swarming by type I interferon promotes intracellular bacterial evasion

Author

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  • Shimin Li

    (University of Science and Technology of China)

  • Qi Yao

    (University of Science and Technology of China)

  • Jiajia Li

    (University of Science and Technology of China)

  • Haoxiang Yang

    (University of Science and Technology of China)

  • Rui Qian

    (First Affiliated Hospital of Anhui Medical University)

  • Meijuan Zheng

    (First Affiliated Hospital of Anhui Medical University)

  • Ning Wu

    (The First Affiliated Hospital of Anhui Medical University and Institute of Clinical Immunology Anhui Medical University)

  • Hongyuan Jiang

    (University of Science and Technology of China)

  • Lu Li

    (University of Science and Technology of China)

  • Zhutian Zeng

    (University of Science and Technology of China
    University of Science and Technology of China)

Abstract

Listeria monocytogenes (LM) possesses the ability to breach multiple barriers and elicit intricate immune responses. However, there remains a lack of explicit understanding regarding how LM evades innate immune surveillance within the body. Here, we utilized liver intravital imaging to elucidate the dynamic process of LM during infection in the liver. We discovered that LM can rapidly escape from Kupffer cells (KCs) through listeriolysin O (LLO) and proliferate within hepatocytes. Upon LM exposure to the hepatic sinusoids, neutrophils rapidly aggregate at the site of infection. Subsequently, LM can induce type I interferon (IFN-I) production primarily in the spleen, which acts systemically on neutrophils to hamper their swarming by deactivating the ERK pathway, thus evading neutrophil-mediated eradication. Furthermore, our findings suggest that virus-induced IFN-I suppresses neutrophil swarming, and COVID-19 patients exhibit impaired neutrophil aggregation function. In conclusion, our findings provide compelling evidence demonstrating that intracellular bacteria represented by LM can hijack host defense mechanisms against viral infections to evade immune surveillance. Additionally, impaired neutrophil swarming caused by IFN-I is one of the significant factors contributing to the increased susceptibility to bacterial infections following viral infections.

Suggested Citation

  • Shimin Li & Qi Yao & Jiajia Li & Haoxiang Yang & Rui Qian & Meijuan Zheng & Ning Wu & Hongyuan Jiang & Lu Li & Zhutian Zeng, 2024. "Inhibition of neutrophil swarming by type I interferon promotes intracellular bacterial evasion," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53060-4
    DOI: 10.1038/s41467-024-53060-4
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    References listed on IDEAS

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    1. Claire Maudet & Marouane Kheloufi & Sylvain Levallois & Julien Gaillard & Lei Huang & Charlotte Gaultier & Yu-Huan Tsai & Olivier Disson & Marc Lecuit, 2022. "Bacterial inhibition of Fas-mediated killing promotes neuroinvasion and persistence," Nature, Nature, vol. 603(7903), pages 900-906, March.
    2. Mark A. Czuczman & Ramzi Fattouh & Jorik M. van Rijn & Veronica Canadien & Suzanne Osborne & Aleixo M. Muise & Vijay K. Kuchroo & Darren E. Higgins & John H. Brumell, 2014. "Listeria monocytogenes exploits efferocytosis to promote cell-to-cell spread," Nature, Nature, vol. 509(7499), pages 230-234, May.
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