Helicobacter pylori induces MAPK phosphorylation and AP-1 activation via a NOD1-dependent mechanism

J Immunol. 2009 Dec 15;183(12):8099-109. doi: 10.4049/jimmunol.0900664.

Abstract

Helicobacter pylori rapidly activates MAPKs and transcription factors, NF-kappaB and AP-1, in gastric epithelial cells following host attachment. Activation of these signal transducers is largely dependent on the cag pathogenicity island (cagPAI)-encoded Type IV Secretion System. H. pylori was shown to translocate peptidoglycan through the Type IV Secretion System, which is recognized by the pathogen recognition molecule, NOD1, thus resulting in NF-kappaB activation. The mechanisms of H. pylori-induced MAPK and AP-1 activation, however, are less well defined and therefore, we assessed the contribution of NOD1 to their activation. For this, we used gastric epithelial cell lines, stably expressing siRNA to either NOD1 or a control gene. In siNOD1-expressing cells stimulated with cagPAI(+) H. pylori, we observed significant reductions in p38 and ERK phosphorylation (p < 0.05), whereas the levels of Jnk phosphorylation remained unchanged. Consistent with a previous report, however, we were able to demonstrate NOD1-dependent Jnk phosphorylation by the invasive pathogen Shigella flexneri, highlighting pathogen-specific host responses to infection. We also show that NOD1 was essential for H. pylori induction of not only NF-kappaB, but also AP-1 activation, implying that NOD1 induces robust proinflammatory responses, in an attempt to rapidly control infection. Pharmacological inhibition of p38 and ERK activity significantly reduced IL-8 production in response to H. pylori, further emphasizing the importance of MAPKs in innate immune responses to the pathogen. Thus, for the first time we have shown the important role for NOD1 in MAPK and AP-1 activation in response to cagPAI(+) H. pylori.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, Bacterial / physiology
  • Bacterial Outer Membrane Proteins / metabolism
  • Bacterial Outer Membrane Proteins / physiology
  • Bacterial Proteins / physiology
  • Cell Line
  • Cell Line, Tumor
  • Enzyme Activation / immunology
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Extracellular Signal-Regulated MAP Kinases / physiology
  • Gene Targeting
  • Helicobacter pylori / immunology*
  • Humans
  • Inflammation Mediators / metabolism
  • Inflammation Mediators / physiology
  • MAP Kinase Kinase 4 / metabolism
  • Nod1 Signaling Adaptor Protein / antagonists & inhibitors
  • Nod1 Signaling Adaptor Protein / genetics
  • Nod1 Signaling Adaptor Protein / physiology*
  • Phosphorylation / immunology
  • Secretory Vesicles / metabolism
  • Signal Transduction / immunology
  • Transcription Factor AP-1 / metabolism*

Substances

  • Antigens, Bacterial
  • Bacterial Outer Membrane Proteins
  • Bacterial Proteins
  • Inflammation Mediators
  • NOD1 protein, human
  • Nod1 Signaling Adaptor Protein
  • Transcription Factor AP-1
  • cagA protein, Helicobacter pylori
  • Extracellular Signal-Regulated MAP Kinases
  • MAP Kinase Kinase 4