SLAM-family receptors promote resolution of ILC2-mediated inflammation

Nat Commun. 2024 Jun 13;15(1):5056. doi: 10.1038/s41467-024-49466-9.

Abstract

Type 2 innate lymphoid cells (ILC2) initiate early allergic inflammation in the lung, but the factors that promote subsequent resolution of type 2 inflammation and prevent prolonged ILC2 activation are not fully known. Here we show that SLAM-family receptors (SFR) play essential roles in this process. We demonstrate dynamic expression of several SFRs on ILC2s during papain-induced type 2 immunity in mice. SFR deficiency exacerbates ILC2-driven eosinophil infiltration in the lung, and results in a significant increase in IL-13 production by ILC2s exclusively in mediastinal lymph nodes (MLN), leading to increased dendritic cell (DC) and TH2 cell numbers. In MLNs, we observe more frequent interaction between ILC2s and bystander T cells, with T cell-expressed SFRs (especially SLAMF3 and SLAMF5) acting as self-ligands to suppress IL-13 production by ILC2s. Mechanistically, homotypic engagement of SFRs at the interface between ILC2s and T cells delivers inhibitory signaling primarily mediated by SHIP-1. This prevents activation of NF-κB, driven by IL-7 and IL-33, two major drivers of ILC2-mediated type 2 immunity. Thus, our study shows that an ILC2-DC-TH2 regulatory axis may promote the resolution of pulmonary type 2 immune responses, and highlights SLAMF3/SLAMF5 as potential therapeutic targets for ameliorating type 2 immunity.

MeSH terms

  • Animals
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Immunity, Innate*
  • Inflammation* / immunology
  • Inflammation* / metabolism
  • Interleukin-13 / immunology
  • Interleukin-13 / metabolism
  • Interleukin-33 / metabolism
  • Lung* / immunology
  • Lung* / pathology
  • Lymph Nodes / immunology
  • Lymph Nodes / metabolism
  • Lymphocytes* / immunology
  • Lymphocytes* / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout
  • NF-kappa B / metabolism
  • Papain
  • Signal Transduction
  • Signaling Lymphocytic Activation Molecule Family* / genetics
  • Signaling Lymphocytic Activation Molecule Family* / metabolism
  • Th2 Cells / immunology

Substances

  • Signaling Lymphocytic Activation Molecule Family
  • Papain
  • Interleukin-13
  • Interleukin-33
  • NF-kappa B