Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages

J Immunol. 2001 Feb 1;166(3):1823-31. doi: 10.4049/jimmunol.166.3.1823.

Abstract

Exposure of macrophages to bacteria or LPS mediates activation of signaling pathways that induce expression of self defense-related genes. Pathogenic Yersinia species impair activation of transcription factor NF-kappaB and trigger apoptosis in macrophages. In this study, we dissected the mechanism of apoptosis induction by Yersinia. Selectively, Yersinia enterocolitica strains producing the effector protein Yersinia outer protein P (YopP) hampered NF-kappaB activation and subsequently conferred apoptosis to J774A.1 macrophages. Thereby, YopP bound and inhibited the macrophage NF-kappaB-activating kinase IKKbeta. YopP- and Yersinia-, but not Salmonella-induced apoptosis was specifically prevented by transient overexpression of NF-kappaB p65, giving evidence that YopP mediates cell death by disrupting the NF-kappaB signaling pathway. Transfection of J774A.1 macrophages with YopP induced a moderate, but significant degree of apoptosis (40-50% of transfected cells). This effect was strongly enhanced by additional initiation of LPS signaling (80-90%), indicating a synergism between LPS-induced signal transduction and inhibition of NF-kappaB by YopP. This reflects a strategy of a bacterial pathogen that takes advantage of LPS, serving as cofactor, to impair the macrophage.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Bacterial / immunology*
  • Adhesins, Bacterial / metabolism
  • Adhesins, Bacterial / physiology
  • Animals
  • Apoptosis / immunology*
  • Cell Line
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology
  • Enzyme Activation / immunology
  • I-kappa B Proteins*
  • Immunosuppressive Agents / immunology
  • Lipopolysaccharides / immunology*
  • Macrophages / cytology
  • Macrophages / immunology*
  • Macrophages / microbiology
  • Mice
  • NF-kappa B / antagonists & inhibitors*
  • NF-kappa B / metabolism
  • NF-kappa B / physiology*
  • Salmonella typhimurium / immunology
  • Signal Transduction / immunology*
  • Transcription Factor RelA
  • Yersinia enterocolitica / immunology*

Substances

  • Adhesins, Bacterial
  • DNA-Binding Proteins
  • I kappa B beta protein
  • I-kappa B Proteins
  • Immunosuppressive Agents
  • Lipopolysaccharides
  • NF-kappa B
  • Transcription Factor RelA
  • YadA protein, Yersinia