Colitogenic effector T cells: roles of gut-homing integrin, gut antigen specificity and γδ T cells

Immunol Cell Biol. 2014 Jan;92(1):90-8. doi: 10.1038/icb.2013.70. Epub 2013 Nov 5.

Abstract

Disturbance of T-cell homeostasis could lead to intestinal inflammation. Naive CD4 T cells undergoing spontaneous proliferation, a robust proliferative response that occurs under severe lymphopenic conditions, differentiate into effector cells producing Th1- and/or Th17-type cytokines and induce a chronic inflammation in the intestine that resembles human inflammatory bowel disease. In this study, we investigated the key properties of CD4 T cells necessary to induce experimental colitis. α4β7 upregulation was primarily induced by mesenteric lymph node (mLN) resident CD11b(+) dendritic cell subsets via transforming growth factor beta (TGFβ)/retinoic acid-dependent mechanism. Interestingly, α4β7 expression was essential but not sufficient to induce inflammation. In addition to gut-homing specificity, expression of gut Ag specificity was also crucial. T-cell acquisition of the specificity was dramatically enhanced by the presence of γδ T cells, a population previously shown to exacerbate T-cell-mediated colitis. Importantly, interleukin (IL)-23-mediated γδ T cell stimulation was necessary to enhance colitogenicity but not gut antigen reactivity of proliferating CD4 T cells. These findings demonstrate that T-cell colitogenicity is achieved through multiple processes, offering a therapeutic rationale by intervening these pathways.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • CD4-Positive T-Lymphocytes / cytology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • Colitis / immunology*
  • Colitis / metabolism
  • Colitis / pathology
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Gastrointestinal Tract / immunology*
  • Gastrointestinal Tract / metabolism
  • Gastrointestinal Tract / pathology
  • Genes, T-Cell Receptor beta / physiology
  • Homeodomain Proteins / physiology
  • Humans
  • Inflammation / immunology
  • Inflammation / metabolism
  • Inflammation / pathology
  • Integrins / metabolism*
  • Interleukin-16 / physiology
  • Interleukin-23 Subunit p19 / physiology
  • Lymph Nodes / immunology
  • Lymph Nodes / metabolism
  • Lymph Nodes / pathology
  • Mesenteric Veins / immunology
  • Mesenteric Veins / metabolism
  • Mesenteric Veins / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptors, Antigen, T-Cell, gamma-delta / genetics
  • Receptors, Antigen, T-Cell, gamma-delta / immunology
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism*
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • T-Lymphocytes, Regulatory / pathology
  • Th17 Cells / cytology
  • Th17 Cells / immunology*
  • Th17 Cells / metabolism
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism
  • Tretinoin / pharmacology

Substances

  • Antineoplastic Agents
  • Homeodomain Proteins
  • Il23a protein, mouse
  • Integrins
  • Interleukin-16
  • Interleukin-23 Subunit p19
  • RNA, Messenger
  • Receptors, Antigen, T-Cell, gamma-delta
  • Transforming Growth Factor beta
  • integrin alpha4beta7
  • RAG-1 protein
  • Tretinoin