Activation of the receptor NKG2D leads to production of Th17 cytokines in CD4+ T cells of patients with Crohn's disease

Gastroenterology. 2011 Jul;141(1):217-26, 226.e1-2. doi: 10.1053/j.gastro.2011.03.061. Epub 2011 Apr 7.

Abstract

Background & aims: The natural killer group 2 member D (NKG2D) is a stimulatory receptor expressed on a subset of mucosal and peripheral CD4+ T cells in patients with Crohn's disease (CD) and other inflammatory diseases. Ligand activation of NKG2D in patients induces CD4+ T cells to release T-helper (Th) 1 cytokines and become cytotoxic. We investigated the Th17 cytokines produced by T cells that express NKG2D in blood and intestinal mucosa samples from patients with CD.

Methods: We isolated CD4+ T cells from peripheral blood and lamina propria samples of patients with CD or ulcerative colitis (UC) and healthy individuals (controls). We analyzed the phenotype and functions of the CD4+NKG2D+ T cells and the cytokines they produce in response to NKG2D stimulation.

Results: In patients with CD, CD4+ T cells that express NKG2D produced high levels of interleukin (IL)-17 and IL-22 and expressed high levels of CCR6, the IL-23 receptor, CD161, and RORC (a transcription factor that regulates expression of Th17 cytokines). CD4+ T cells that produced IL-17 expressed high levels of NKG2D and CD161. Costimulation of NKG2D and the T-cell receptor (TCR) significantly increased production of IL-17 and tumor necrosis factor α by CD4+ T cells, compared with activation of only the TCR. CD4+NKG2D+ T cells also responded to Th17 polarization.

Conclusions: NKG2D is a functional marker of CD4+ T cells that produce IL-17 in patients with CD, via costimulation of the TCR and NKG2D. Reagents developed to block NKG2D might reduce gastrointestinal inflammation in patients with CD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Case-Control Studies
  • Cell Line, Tumor
  • Colitis, Ulcerative / blood
  • Colitis, Ulcerative / genetics
  • Colitis, Ulcerative / immunology*
  • Crohn Disease / blood
  • Crohn Disease / genetics
  • Crohn Disease / immunology*
  • Cytokines / genetics
  • Cytokines / metabolism*
  • Female
  • Flow Cytometry
  • France
  • Humans
  • Immunophenotyping / methods
  • Inflammation Mediators / metabolism*
  • Intestinal Mucosa / immunology*
  • Ligands
  • Male
  • Mice
  • Middle Aged
  • NK Cell Lectin-Like Receptor Subfamily B / immunology
  • NK Cell Lectin-Like Receptor Subfamily K / agonists*
  • Phenotype
  • Receptors, Antigen, T-Cell / agonists
  • Th17 Cells / immunology*
  • Young Adult

Substances

  • Cytokines
  • Inflammation Mediators
  • KLRB1 protein, human
  • KLRK1 protein, human
  • Ligands
  • NK Cell Lectin-Like Receptor Subfamily B
  • NK Cell Lectin-Like Receptor Subfamily K
  • Receptors, Antigen, T-Cell