CD11c(+) monocyte/macrophages promote chronic Helicobacter hepaticus-induced intestinal inflammation through the production of IL-23

Mucosal Immunol. 2016 Mar;9(2):352-63. doi: 10.1038/mi.2015.65. Epub 2015 Aug 5.

Abstract

In inflammatory bowel diseases, a breakdown in host microbial interactions accompanies sustained activation of immune cells in the gut. Functional studies suggest a key role for interleukin-23 (IL-23) in orchestrating intestinal inflammation. IL-23 can be produced by various mononuclear phagocytes (MNPs) following acute microbial stimulation, but little is known about the key cellular sources of IL-23 that drive chronic intestinal inflammation. Here we have addressed this question using a physiological model of bacteria-driven colitis. By combining conditional gene ablation and gene expression profiling, we found that IL-23 production by CD11c(+) MNPs was essential to trigger intestinal immunopathology and identified MHCII(+) monocytes and macrophages as the major source of IL-23. Expression of IL-23 by monocytes was acquired during their differentiation in the intestine and correlated with the expression of major histocompatibility complex class II (MHCII) and CD64. In contrast, Batf3-dependent CD103(+) CD11b(-) dendritic cells were dispensable for bacteria-induced colitis in this model. These studies reinforce the pathogenic role of monocytes in dysregulated responses to intestinal bacteria and identify production of IL-23 as a key component of this response. Further understanding of the functional sources of IL-23 in diverse forms of intestinal inflammation may lead to novel therapeutic strategies aimed at interrupting IL-23-driven immune pathology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / immunology
  • Basic-Leucine Zipper Transcription Factors / genetics
  • Basic-Leucine Zipper Transcription Factors / immunology
  • CD11c Antigen / genetics
  • CD11c Antigen / immunology*
  • Chronic Disease
  • Colitis / genetics
  • Colitis / immunology*
  • Colitis / microbiology
  • Colitis / pathology
  • Colon / immunology
  • Colon / pathology
  • Dendritic Cells / immunology
  • Dendritic Cells / microbiology
  • Dendritic Cells / pathology
  • Epithelial Cells / immunology
  • Epithelial Cells / microbiology
  • Epithelial Cells / pathology
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Helicobacter Infections / genetics
  • Helicobacter Infections / immunology*
  • Helicobacter Infections / microbiology
  • Helicobacter Infections / pathology
  • Helicobacter hepaticus / immunology
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / immunology
  • Integrin alpha Chains / genetics
  • Integrin alpha Chains / immunology
  • Interleukin-23 / genetics
  • Interleukin-23 / immunology*
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / microbiology
  • Intestinal Mucosa / pathology
  • Lectins, C-Type / genetics
  • Lectins, C-Type / immunology
  • Macrophages / immunology*
  • Macrophages / microbiology
  • Macrophages / pathology
  • Mice
  • Mice, Transgenic
  • Monocytes / immunology*
  • Monocytes / microbiology
  • Monocytes / pathology
  • Receptors, IgG / genetics
  • Receptors, IgG / immunology
  • Receptors, Immunologic / genetics
  • Receptors, Immunologic / immunology
  • Repressor Proteins / genetics
  • Repressor Proteins / immunology
  • Signal Transduction

Substances

  • Antigens, CD
  • Basic-Leucine Zipper Transcription Factors
  • CD11c Antigen
  • Clec9a protein, mouse
  • Histocompatibility Antigens Class II
  • Integrin alpha Chains
  • Interleukin-23
  • Lectins, C-Type
  • Receptors, IgG
  • Receptors, Immunologic
  • Repressor Proteins
  • SNFT protein, mouse
  • alpha E integrins