Trefoil factor 1 expression suppresses Helicobacter pylori-induced inflammation in gastric carcinogenesis

Cancer. 2015 Dec 15;121(24):4348-58. doi: 10.1002/cncr.29644. Epub 2015 Sep 15.

Abstract

Background: Infection with Helicobacter pylori, a high-risk factor for gastric cancer, is frequently associated with chronic inflammation through activation of nuclear factor κB (NF-κB). Trefoil factor 1 (TFF1) is a constitutively expressed protein in the stomach that has tumor-suppressor functions and plays a critical role in maintaining mucosal integrity. This study investigated the role of TFF1 in regulating the proinflammatory response to H. pylori infections.

Methods: For in vitro studies, immunofluorescence, luciferase reporter assays, Western blots, and quantitative real-time polymerase chain reaction were performed to investigate the activation of NF-κB and its target genes in response to infections with H. pylori strains J166 and 7.13. In addition, Tff1-knockout (KO) and Tff1-wild-type mice were used for infections with the H. pylori strain called premouse Sydney strain 1.

Results: The reconstitution of TFF1 expression in gastric cancer cells significantly suppressed H. pylori-mediated increases in NF-κB-p65 nuclear staining, transcriptional activity, and expression of proinflammatory cytokine genes (tumor necrosis factor α, interleukin 1β, chemokine [C-X-C motif] ligand 5, and interleukin 4 receptor) that were associated with reductions in the expression and phosphorylation of NF-κB-p65 and IκB kinase α/β proteins. The in vivo studies using the Tff1-KO mouse model of gastric neoplasia confirmed the in vitro findings. Furthermore, they demonstrated increases in chronic inflammation scores and in the frequency of invasive gastric adenocarcinoma in the Tff1-KO mice infected with H. pylori versus the uninfected Tff1-KO mice.

Conclusions: These findings underscore an important protective role of TFF1 in abrogating H. pylori-mediated inflammation, a crucial hallmark of gastric tumorigenesis. Therefore, loss of TFF1 expression could be an important step in H. pylori-mediated gastric carcinogenesis.

Keywords: Helicobacter pylori; gastric cancer; inflammation; nuclear factor κB (NF-κB); trefoil factor 1 (TFF1).

Publication types

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

MeSH terms

  • Adenocarcinoma / genetics*
  • Adenocarcinoma / immunology
  • Adenocarcinoma / microbiology
  • Animals
  • Carcinogenesis / genetics*
  • Chemokine CXCL5 / immunology
  • Gastric Mucosa / immunology
  • Gastric Mucosa / metabolism*
  • Gastric Mucosa / microbiology
  • Helicobacter Infections / genetics*
  • Helicobacter Infections / immunology
  • Helicobacter pylori
  • Humans
  • I-kappa B Kinase / metabolism
  • In Vitro Techniques
  • Inflammation
  • Interleukin-1beta / immunology
  • Mice
  • Mice, Knockout
  • Peptides / genetics*
  • Phosphorylation
  • Real-Time Polymerase Chain Reaction
  • Receptors, Interleukin-4 / immunology
  • Stomach / immunology
  • Stomach / microbiology
  • Stomach Neoplasms / genetics*
  • Stomach Neoplasms / immunology
  • Stomach Neoplasms / microbiology
  • Transcription Factor RelA / metabolism
  • Trefoil Factor-1
  • Tumor Cells, Cultured
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Chemokine CXCL5
  • Interleukin-1beta
  • Peptides
  • Receptors, Interleukin-4
  • Tff1 protein, mouse
  • Transcription Factor RelA
  • Trefoil Factor-1
  • Tumor Necrosis Factor-alpha
  • I-kappa B Kinase