Distal colonocytes targeted by C. rodentium recruit T-cell help for barrier defence

Nature. 2024 May;629(8012):669-678. doi: 10.1038/s41586-024-07288-1. Epub 2024 Apr 10.

Abstract

Interleukin 22 (IL-22) has a non-redundant role in immune defence of the intestinal barrier1-3. T cells, but not innate lymphoid cells, have an indispensable role in sustaining the IL-22 signalling that is required for the protection of colonic crypts against invasion during infection by the enteropathogen Citrobacter rodentium4 (Cr). However, the intestinal epithelial cell (IEC) subsets targeted by T cell-derived IL-22, and how T cell-derived IL-22 sustains activation in IECs, remain undefined. Here we identify a subset of absorptive IECs in the mid-distal colon that are specifically targeted by Cr and are differentially responsive to IL-22 signalling. Major histocompatibility complex class II (MHCII) expression by these colonocytes was required to elicit sustained IL-22 signalling from Cr-specific T cells, which was required to restrain Cr invasion. Our findings explain the basis for the regionalization of the host response to Cr and demonstrate that epithelial cells must elicit MHCII-dependent help from IL-22-producing T cells to orchestrate immune protection in the intestine.

MeSH terms

  • Animals
  • Citrobacter rodentium* / immunology
  • Colon* / cytology
  • Colon* / immunology
  • Colon* / microbiology
  • Enterobacteriaceae Infections / immunology
  • Enterobacteriaceae Infections / microbiology
  • Epithelial Cells* / immunology
  • Epithelial Cells* / metabolism
  • Epithelial Cells* / microbiology
  • Female
  • Histocompatibility Antigens Class II / immunology
  • Histocompatibility Antigens Class II / metabolism
  • Interleukin-22 / immunology
  • Interleukin-22 / metabolism
  • Intestinal Mucosa* / cytology
  • Intestinal Mucosa* / immunology
  • Intestinal Mucosa* / microbiology
  • Male
  • Mice
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Signal Transduction / immunology
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism

Substances

  • Histocompatibility Antigens Class II
  • Interleukin-22
  • interleukin-22, mouse