Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice

Gastroenterology. 2010 Mar;138(3):1046-54. doi: 10.1053/j.gastro.2009.11.043. Epub 2009 Nov 18.

Abstract

Background & aims: Helicobacter pylori infection increases gastric regulatory T cell (Treg) response, which may contribute to H pylori immune escape. We hypothesize that H pylori directs Treg skewing by way of dendritic cells (DCs) and thus inhibits interleukin-17(+) helper T cells (Th17) immunity.

Methods: Two-photon microscopy was used to locate DCs in gastric lamina propria of mice. The induction of Th17 and Treg responses by bacteria-pulsed murine bone marrow-derived DCs was analyzed by cytokine production and stimulation of T-cell proliferation. The effect of VacA, CagA, transforming growth factor-beta (TGF-beta), and IL-10 on Th17/Treg balance was assessed. The in vivo significance of Tregs on the H pylori-specific Th17 response and H pylori density was determined by using anti-CD25 neutralizing antibodies to deplete Tregs in mice.

Results: We showed that mucosal CD11c(+) DCs are located near the surface of normal gastric epithelium, and their number increased after H pylori infection. Study of the direct interaction of DCs with H pylori showed a Treg-skewed response. The Treg skewing was independent of H pylori VacA and CagA and dependent on TGF-beta and IL-10. In vivo Treg skewing by adoptive transfer of H pylori-pulsed DCs reduces the ratio of gastric IL-17/Foxp3 mRNA expressions. The depletion of CD25(+) Tregs results in early reduction of H pylori density, which is correlated with enhanced peripheral H pylori-specific Th17, but not Th1, response.

Conclusions: Overall, our study indicates that H pylori alters the DC-polarized Th17/Treg balance toward a Treg-biased response, which suppresses the effective induction of H pylori-specific Th17 immunity.

Publication types

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

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antigens, Bacterial / immunology
  • Bacterial Proteins / immunology
  • Cell Proliferation
  • Cells, Cultured
  • Dendritic Cells / immunology*
  • Dendritic Cells / microbiology
  • Disease Models, Animal
  • Female
  • Forkhead Transcription Factors / metabolism
  • Gastric Mucosa / immunology*
  • Gastric Mucosa / microbiology
  • Helicobacter Infections / immunology*
  • Helicobacter Infections / microbiology
  • Helicobacter pylori / growth & development
  • Helicobacter pylori / immunology*
  • Immune Evasion*
  • Interleukin-10 / metabolism
  • Interleukin-17 / immunology*
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Microscopy, Confocal
  • Microscopy, Fluorescence, Multiphoton
  • RNA, Messenger / metabolism
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / microbiology
  • T-Lymphocytes, Regulatory / immunology*
  • Time Factors
  • Transforming Growth Factor beta / metabolism

Substances

  • Antigens, Bacterial
  • Bacterial Proteins
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Il2ra protein, mouse
  • Interleukin-17
  • Interleukin-2 Receptor alpha Subunit
  • RNA, Messenger
  • Transforming Growth Factor beta
  • VacA protein, Helicobacter pylori
  • cagA protein, Helicobacter pylori
  • Interleukin-10