Chemokine receptor CCR7 regulates the intestinal TH1/TH17/Treg balance during Crohn's-like murine ileitis

J Leukoc Biol. 2015 Jun;97(6):1011-22. doi: 10.1189/jlb.3HI0614-303R. Epub 2015 Jan 30.

Abstract

The regulation of T cell and DC retention and lymphatic egress within and from the intestine is critical for intestinal immunosurveillance; however, the cellular processes that orchestrate this balance during IBD remain poorly defined. With the use of a mouse model of TNF-driven Crohn's-like ileitis (TNF(Δ) (ARE)), we examined the role of CCR7 in the control of intestinal T cell and DC retention/egress during experimental CD. We observed that the frequency of CCR7-expressing TH1/TH17 effector lymphocytes increased during active disease in TNF(Δ) (ARE) mice and that ΔARE/CCR7(-/-) mice developed exacerbated ileitis and multiorgan inflammation, with a marked polarization and ileal retention of TH1 effector CD4(+) T cells. Furthermore, adoptive transfer of ΔARE/CCR7(-/-) effector CD4(+) into lymphopenic hosts resulted in ileo-colitis, whereas those transferred with ΔARE/CCR7(+/+) CD4(+) T cells developed ileitis. ΔARE/CCR7(-/-) mice had an acellular draining MLN, decreased CD103(+) DC, and decreased expression of RALDH enzymes and of CD4(+)CD25(+)FoxP3(+) Tregs. Lastly, a mAb against CCR7 exacerbated ileitis in TNF(Δ) (ARE) mice, phenocopying the effects of congenital CCR7 deficiency. Our data underscore a critical role for the lymphoid chemokine receptor CCR7 in orchestrating immune cell traffic and TH1 versus TH17 bias during chronic murine ileitis.

Keywords: CD103+ dendritic cells; Crohn’s disease; effector memory T cells; inflammatory bowel disease; lymphatics.

Publication types

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

MeSH terms

  • Adoptive Transfer
  • Aldehyde Dehydrogenase / genetics
  • Aldehyde Dehydrogenase / immunology
  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Antigens, CD / genetics
  • Antigens, CD / immunology
  • Cell Movement / drug effects
  • Crohn Disease / genetics
  • Crohn Disease / immunology
  • Crohn Disease / pathology
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology
  • Dendritic Cells / pathology
  • Disease Models, Animal
  • Gene Expression Regulation
  • Humans
  • Ileitis / genetics
  • Ileitis / immunology*
  • Ileitis / pathology
  • Ileum / immunology*
  • Ileum / pathology
  • Isoenzymes / genetics
  • Isoenzymes / immunology
  • Mice
  • Mice, Transgenic
  • Receptors, CCR7 / antagonists & inhibitors
  • Receptors, CCR7 / deficiency
  • Receptors, CCR7 / genetics
  • Receptors, CCR7 / immunology*
  • Signal Transduction
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / pathology
  • Th1 Cells / drug effects
  • Th1 Cells / immunology*
  • Th1 Cells / pathology
  • Th1 Cells / transplantation
  • Th17 Cells / drug effects
  • Th17 Cells / immunology*
  • Th17 Cells / pathology
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Antibodies, Monoclonal
  • Antigens, CD
  • Ccr7 protein, mouse
  • Isoenzymes
  • Receptors, CCR7
  • Tumor Necrosis Factor-alpha
  • Aldehyde Dehydrogenase