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Neutrophil-derived extracellular vesicles: proinflammatory trails and anti-inflammatory microvesicles

Young-Jin Youn, Sanjeeb Shrestha, Jun-Kyu Kim, Yu-Bin Lee, Jee Hyun Lee, Keun Hur, Nanda Maya Mali, Sung-Wook Nam, Sun-Hwa Kim, Dong-Keun Song, Hee Kyung Jin, Jae-sung Bae, Chang-Won Hong
doi: https://doi.org/10.1101/583435
Young-Jin Youn
Department of Physiology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Sanjeeb Shrestha
Department of Physiology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Jun-Kyu Kim
Department of Physiology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Yu-Bin Lee
Department of Physiology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Jee Hyun Lee
Department of Biochemistry and Cell Biology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Keun Hur
Department of Biochemistry and Cell Biology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Nanda Maya Mali
Department of Anatomy, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Sung-Wook Nam
Department of Molecular Medicine, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Sun-Hwa Kim
Department of Physiology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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Dong-Keun Song
Department of Pharmacology, College of Medicine, Hallym University, Chuncheon, 24252, Republic of Korea
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Hee Kyung Jin
Department of Laboratory Animal Medicine, College of Veterinary Medicine, Kyungpook National University, Daegu, 41944, Republic of KoreaStem Cell Neuroplasticity Research Group, Kyungpook National University, Daegu, 41944, Republic of Korea
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Jae-sung Bae
Department of Physiology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of KoreaStem Cell Neuroplasticity Research Group, Kyungpook National University, Daegu, 41944, Republic of Korea
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Chang-Won Hong
Department of Physiology, School of Medicine, Kyungpook National University, Daegu, 41944, Republic of Korea
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  • For correspondence: cwhong@knu.ac.kr
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SUMMARY

Extracellular vesicles (EVs) are membrane-derived vesicles that mediate intercellular communications. Neutrophils produce different subtypes of EVs during inflammatory responses. Neutrophil-derived trails (NDTRs) are generated by neutrophils migrating toward inflammatory foci, whereas neutrophil-derived microvesicles (NDMVs) are thought to be generated by neutrophils that have arrived at the inflammatory foci. However, the physical and functional characteristics of neutrophil-derived EVs are incompletely understood. In this study, we investigated the similarities and differences between neutrophil-derived EV subtypes. Neutrophil-derived EVs shared similar characteristics regarding stimulators, generation mechanisms, and surface marker expression. Both neutrophil-derived EV subtypes exhibited similar functions, such as direct bactericidal activity and induction of monocyte chemotaxis via MCP-1. However, NDTR generation was dependent on the integrin signaling, while NDMV generation was dependent on the PI3K pathway. The CD16 expression level differentiated the neutrophil-derived EV subtypes. Interestingly, both subtypes showed different patterns of miRNA expression and were easily phagocytosed by monocytes. NDTRs induced M1 macrophage polarization, whereas NDMVs induced M2 macrophage polarization. Moreover, NDTRs but not NDMVs exerted protective effects against sepsis-induced lethality in a murine sepsis model and pathological changes in a murine chronic colitis model. These results suggest a new insight into neutrophil-derived EV subtypes: proinflammatory NDTRs and anti-inflammatory NDMVs.

Key points

  • Neutrophil-derived trails are proinflammatory extracellular vesicles that induce M1 macrophage polarization and protect against inflammation

  • Neutrophil-derived microvesicles are anti-inflammatory extracellular vesicles that induce M2 macrophage polarization

  • Abbreviations

    EV
    extracellular vesicle
    NDMV
    neutrophil-derived microvesicles
    NDTR
    neutrophil-derived trails
    NK cells
    natural killer cells
    MoDCs
    monocyte-derived dendritic cells
    CXCL12
    CXC-chemokine ligand 12
    PAMPs
    pathogen-associated molecular patterns
    fMLP
    formyl-methionyl-leucyl-phenylalanine
    LPS
    lipopolysaccharide
    E. coli
    Escherichia coli
    S. aureus
    Staphylococcus aureus
    DAMPs
    danger-associated molecular patterns
    HMGB1
    high mobility group box 1
    TNF-α
    tumor necrosis factor-α
    IFN-γ
    interferon-γ
    TGF-β
    tumor growth factor-β
    IL-4
    interleukin-4
    L-NAME
    N(γ)-nitro-L-arginine methyl ester
    PMA
    phorbol 12-myristate 13-acetate
    MCP-1
    monocyte chemoattractant protein 1
    iNOS
    inducible nitric oxide synthase
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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    Posted March 20, 2019.
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    Neutrophil-derived extracellular vesicles: proinflammatory trails and anti-inflammatory microvesicles
    Young-Jin Youn, Sanjeeb Shrestha, Jun-Kyu Kim, Yu-Bin Lee, Jee Hyun Lee, Keun Hur, Nanda Maya Mali, Sung-Wook Nam, Sun-Hwa Kim, Dong-Keun Song, Hee Kyung Jin, Jae-sung Bae, Chang-Won Hong
    bioRxiv 583435; doi: https://doi.org/10.1101/583435
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    Neutrophil-derived extracellular vesicles: proinflammatory trails and anti-inflammatory microvesicles
    Young-Jin Youn, Sanjeeb Shrestha, Jun-Kyu Kim, Yu-Bin Lee, Jee Hyun Lee, Keun Hur, Nanda Maya Mali, Sung-Wook Nam, Sun-Hwa Kim, Dong-Keun Song, Hee Kyung Jin, Jae-sung Bae, Chang-Won Hong
    bioRxiv 583435; doi: https://doi.org/10.1101/583435

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