Tuft-Cell-Derived Leukotrienes Drive Rapid Anti-helminth Immunity in the Small Intestine but Are Dispensable for Anti-protist Immunity

Immunity. 2020 Mar 17;52(3):528-541.e7. doi: 10.1016/j.immuni.2020.02.005. Epub 2020 Mar 10.

Abstract

Helminths, allergens, and certain protists induce type 2 immune responses, but the underlying mechanisms of immune activation remain poorly understood. In the small intestine, chemosensing by epithelial tuft cells results in the activation of group 2 innate lymphoid cells (ILC2s), which subsequently drive increased tuft cell frequency. This feedforward circuit is essential for intestinal remodeling and helminth clearance. ILC2 activation requires tuft-cell-derived interleukin-25 (IL-25), but whether additional signals regulate the circuit is unclear. Here, we show that tuft cells secrete cysteinyl leukotrienes (cysLTs) to rapidly activate type 2 immunity following chemosensing of helminth infection. CysLTs cooperate with IL-25 to activate ILC2s, and tuft-cell-specific ablation of leukotriene synthesis attenuates type 2 immunity and delays helminth clearance. Conversely, cysLTs are dispensable for the tuft cell response induced by intestinal protists. Our findings identify an additional tuft cell effector function and suggest context-specific regulation of tuft-ILC2 circuits within the small intestine.

Keywords: Heligmosomoides polygyrus; ILC2; Nippostrongylus brasiliensis; brush cell; helminth; intestine; leukotriene; protist; succinate; tuft cell.

Publication types

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

MeSH terms

  • Animals
  • Arachidonate 5-Lipoxygenase / genetics
  • Arachidonate 5-Lipoxygenase / immunology
  • Arachidonate 5-Lipoxygenase / metabolism
  • Cysteine / immunology*
  • Cysteine / metabolism
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism
  • Epithelial Cells / parasitology
  • Immunity, Innate / immunology
  • Interleukin-17 / genetics
  • Interleukin-17 / immunology
  • Interleukin-17 / metabolism
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / parasitology
  • Intestine, Small / cytology
  • Intestine, Small / immunology*
  • Intestine, Small / metabolism
  • Leukotrienes / immunology*
  • Leukotrienes / metabolism
  • Lymphocytes / immunology
  • Lymphocytes / metabolism
  • Lymphocytes / parasitology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Nippostrongylus / immunology*
  • Nippostrongylus / physiology
  • Strongylida Infections / immunology*
  • Strongylida Infections / parasitology

Substances

  • Interleukin-17
  • Leukotrienes
  • cysteinyl-leukotriene
  • Arachidonate 5-Lipoxygenase
  • Cysteine