Interleukin-33 Induces the Enzyme Tryptophan Hydroxylase 1 to Promote Inflammatory Group 2 Innate Lymphoid Cell-Mediated Immunity

Immunity. 2020 Apr 14;52(4):606-619.e6. doi: 10.1016/j.immuni.2020.02.009. Epub 2020 Mar 10.

Abstract

Group 2 innate lymphoid cells (ILC2s) regulate immunity, inflammation, and tissue homeostasis. Two distinct subsets of ILC2s have been described: steady-state natural ILC2s and inflammatory ILC2s, which are elicited following helminth infection. However, how tissue-specific cues regulate these two subsets of ILC2s and their effector functions remains elusive. Here, we report that interleukin-33 (IL-33) promotes the generation of inflammatory ILC2s (ILC2INFLAM) via induction of the enzyme tryptophan hydroxylase 1 (Tph1). Tph1 expression was upregulated in ILC2s upon activation with IL-33 or following helminth infection in an IL-33-dependent manner. Conditional deletion of Tph1 in lymphocytes resulted in selective impairment of ILC2INFLAM responses and increased susceptibility to helminth infection. Further, RNA sequencing analysis revealed altered gene expression in Tph1 deficient ILC2s including inducible T cell co-stimulator (Icos). Collectively, these data reveal a previously unrecognized function for IL-33, Tph1, and ICOS in promoting inflammatory ILC2 responses and type 2 immunity at mucosal barriers.

Keywords: IL-33; ILC2s; Tph1; group 2 innate lymphoid cells; helminth infection; inflammatory ILC2s; tryptophan hydroxylase 1; type 2 immunity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Lineage / genetics
  • Cell Lineage / immunology
  • Disease Susceptibility
  • Gene Expression Regulation / immunology
  • Immunity, Cellular*
  • Immunity, Innate
  • Immunity, Mucosal
  • Inducible T-Cell Co-Stimulator Protein / genetics
  • Inducible T-Cell Co-Stimulator Protein / immunology*
  • Interleukin-33 / genetics
  • Interleukin-33 / immunology*
  • Larva / growth & development
  • Larva / immunology
  • Larva / pathogenicity
  • Lymph Nodes / immunology
  • Lymph Nodes / parasitology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nippostrongylus / growth & development
  • Nippostrongylus / immunology*
  • Nippostrongylus / pathogenicity
  • Primary Cell Culture
  • Signal Transduction
  • Strongylida Infections / genetics
  • Strongylida Infections / immunology*
  • Strongylida Infections / parasitology
  • Strongylida Infections / pathology
  • T-Lymphocyte Subsets / classification
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / parasitology
  • Tryptophan Hydroxylase / genetics
  • Tryptophan Hydroxylase / immunology*

Substances

  • Icos protein, mouse
  • Il33 protein, mouse
  • Inducible T-Cell Co-Stimulator Protein
  • Interleukin-33
  • Tph1 protein, mouse
  • Tryptophan Hydroxylase