Cholesterol glucosylation by Helicobacter pylori delays internalization and arrests phagosome maturation in macrophages

J Microbiol Immunol Infect. 2016 Oct;49(5):636-645. doi: 10.1016/j.jmii.2014.05.011. Epub 2014 Jul 26.

Abstract

Background/purpose: Helicobacter pylori colonizes the human stomach and contributes to chronic inflammation of the gastric mucosa. H. pylori persistence occurs because of insufficient eradication by phagocytic cells. A key factor of H. pylori, cholesterol-α-glucosyltransferase encoded by capJ that extracts host cholesterol and converts it to cholesteryl glucosides, is important to evade host immunity. Here, we examined whether phagocytic trafficking in macrophages was perturbed by capJ-carrying H. pylori.

Methods: J774A.1 cells were infected with H. pylori at a multiplicity of infection of 50. Live-cell imaging and confocal microscopic analysis were applied to monitor the phagocytic trafficking events. The viability of H. pylori inside macrophages was determined by using gentamicin colony-forming unit assay. The phagocytic routes were characterized by using trafficking-intervention compounds.

Results: Wild type (WT) H. pylori exhibited more delayed entry into macrophages and also arrested phagosome maturation more than did capJ knockout mutant. Pretreatment of genistein and LY294002 prior to H. pylori infection reduced the internalization of WT but not capJ-knockout H. pylori in macrophages.

Conclusion: Cholesterol glucosylation by H. pylori interferes with phagosome trafficking via a lipid-raft and PI3K-dependent manner, which retards engulfment of bacteria for prolonged intracellular survival of H. pylori.

Keywords: Helicobacter pylori; cholesteryl glucosides; lipid raft; phagocytosis; phagosome maturation; phagosome trafficking.

MeSH terms

  • Animals
  • Cell Line
  • Cholesterol / analogs & derivatives*
  • Cholesterol / metabolism*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism*
  • Helicobacter Infections / immunology
  • Helicobacter Infections / microbiology
  • Helicobacter pylori / genetics
  • Helicobacter pylori / immunology*
  • Helicobacter pylori / metabolism
  • Immune Evasion / immunology*
  • Macrophages / immunology*
  • Membrane Microdomains / metabolism
  • Mice
  • Microscopy, Confocal
  • Phagocytosis / immunology
  • Phagosomes / immunology*
  • Phagosomes / microbiology
  • Phosphatidylinositol 3-Kinases / metabolism

Substances

  • cholesteryl glucoside
  • Cholesterol
  • Glucosyltransferases
  • Hp0421 protein, Helicobacter pylori