Epigenetic downregulation of MUC17 by H. pylori infection facilitates NF-κB-mediated expression of CEACAM1-3S in human gastric cancer

Gastric Cancer. 2019 Sep;22(5):941-954. doi: 10.1007/s10120-019-00932-0. Epub 2019 Feb 18.

Abstract

Background and aims: Helicobacter pylori invades the mucosal barrier and infects the mucins of gastric epithelial cells. However, whether gastric carcinogenesis caused by H. pylori infection involves the membrane-bound mucins is unclear. This study explored the role of mucin 17 (MUC17) in gastric cancer (GC) associated with H. pylori infection.

Methods: The expression of MUC17 and carcinoembryonic antigen-related cell adhesion molecule 1 (CEACAM1) was examined in human GC cells and tissues with H. pylori infection. Gain- and loss-of-function assays were performed to assess the role of MUC17 in regulating CEACAM1 in H. pylori-infected GC cells.

Results: MUC17 was downregulated in H. pylori-infected GC cells and tissues in association with poor survival of GC patients. Downregulation of MUC17 was attributable to MUC17 promoter methylation mediated by DNA methyltransferase 1 (DNMT1) H. pylori-enhanced GC cell proliferation and colony formation associated with MUC17 downregulation. Gain- and loss-of-function assays showed that MUC17 inhibited the H. pylori-enhanced GC cell growth by preventing the translocation of H. pylori CagA into GC cells. Moreover, MUC17 downregulated the expression of CEACAM1 variant 3S (CEACAM1-3S) in GC cells and tissues with H. pylori infection. Additionally, MUC17 downregulated CEACAM1 promoter activity via attenuation of NF-κB activation in GC cells.

Conclusions: MUC17 was epigenetically downregulated in GC with H. pylori infection. MUC17 inhibited H. pylori CagA translocation via attenuation of NF-κB-mediated expression of CEACAM1-3S in GC cells. Thus, MUC17 may serve as a valuable prognostic biomarker for H. pylori-associated GC.

Keywords: CEACAM1; CagA; Gastric cancer; H. pylori; Mucin 17.

MeSH terms

  • Antigens, CD / genetics
  • Antigens, CD / metabolism*
  • Apoptosis
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Proliferation
  • Epigenesis, Genetic*
  • Female
  • Follow-Up Studies
  • Gene Expression Regulation, Neoplastic*
  • Helicobacter Infections / complications*
  • Helicobacter Infections / microbiology
  • Helicobacter pylori / isolation & purification
  • Humans
  • Male
  • Middle Aged
  • Mucins / genetics
  • Mucins / metabolism*
  • NF-kappa B / genetics
  • NF-kappa B / metabolism*
  • Prognosis
  • Promoter Regions, Genetic
  • Stomach Neoplasms / epidemiology
  • Stomach Neoplasms / metabolism
  • Stomach Neoplasms / microbiology
  • Stomach Neoplasms / pathology*
  • Survival Rate
  • Tumor Cells, Cultured

Substances

  • Antigens, CD
  • Biomarkers, Tumor
  • CD66 antigens
  • Cell Adhesion Molecules
  • MUC17 protein, human
  • Mucins
  • NF-kappa B