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Neutrophil breaching of the blood vessel pericyte layer during diapedesis requires mast cell-derived IL-17A

Author

Listed:
  • Régis Joulia

    (Queen Mary University of London, Charterhouse Square
    NHLI, Imperial College London)

  • Idaira María Guerrero-Fonseca

    (Queen Mary University of London, Charterhouse Square
    CINVESTAV-IPN)

  • Tamara Girbl

    (Queen Mary University of London, Charterhouse Square
    University of Würzburg)

  • Jonathon A. Coates

    (Queen Mary University of London, Charterhouse Square)

  • Monja Stein

    (Queen Mary University of London, Charterhouse Square)

  • Laura Vázquez-Martínez

    (Queen Mary University of London, Charterhouse Square)

  • Eleanor Lynam

    (Queen Mary University of London, Charterhouse Square)

  • James Whiteford

    (Queen Mary University of London, Charterhouse Square)

  • Michael Schnoor

    (CINVESTAV-IPN)

  • David Voehringer

    (University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg (FAU))

  • Axel Roers

    (Heidelberg University Hospital)

  • Sussan Nourshargh

    (Queen Mary University of London, Charterhouse Square
    Queen Mary University of London)

  • Mathieu-Benoit Voisin

    (Queen Mary University of London, Charterhouse Square
    Queen Mary University of London)

Abstract

Neutrophil diapedesis is an immediate step following infections and injury and is driven by complex interactions between leukocytes and various components of the blood vessel wall. Here, we show that perivascular mast cells (MC) are key regulators of neutrophil behaviour within the sub-endothelial space of inflamed venules. Using confocal intravital microscopy, we observe directed abluminal neutrophil motility along pericyte processes towards perivascular MCs, a response that created neutrophil extravasation hotspots. Conversely, MC-deficiency and pharmacological or genetic blockade of IL-17A leads to impaired neutrophil sub-endothelial migration and breaching of the pericyte layer. Mechanistically, identifying MCs as a significant cellular source of IL-17A, we establish that MC-derived IL-17A regulates the enrichment of key effector molecules ICAM-1 and CXCL1 in nearby pericytes. Collectively, we identify a novel MC-IL-17A-pericyte axis as modulator of the final steps of neutrophil diapedesis, with potential translational implications for inflammatory disorders driven by increased neutrophil diapedesis.

Suggested Citation

  • Régis Joulia & Idaira María Guerrero-Fonseca & Tamara Girbl & Jonathon A. Coates & Monja Stein & Laura Vázquez-Martínez & Eleanor Lynam & James Whiteford & Michael Schnoor & David Voehringer & Axel Ro, 2022. "Neutrophil breaching of the blood vessel pericyte layer during diapedesis requires mast cell-derived IL-17A," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34695-7
    DOI: 10.1038/s41467-022-34695-7
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    References listed on IDEAS

    as
    1. Tim Lämmermann & Philippe V. Afonso & Bastian R. Angermann & Ji Ming Wang & Wolfgang Kastenmüller & Carole A. Parent & Ronald N. Germain, 2013. "Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo," Nature, Nature, vol. 498(7454), pages 371-375, June.
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