Inhibition of NF-κB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE

J Immunol. 2010 Oct 1;185(7):4118-27. doi: 10.4049/jimmunol.1000500. Epub 2010 Sep 10.

Abstract

Intestinal dendritic cells (DCs) send processes between epithelial cells into the gut lumen to sample pathogens. Noninvasive enteropathogenic Escherichia coli (EPEC) colonize the gut using a type three secretion system (T3SS) to inject effector proteins into epithelial cells. We hypothesized that EPEC might also inject proteins into DC processes to dampen immune recognition. Using a T3SS-linked fluorescence resonance energy transfer-based system we show that EPEC injects effectors into in vitro grown human myeloid DCs. Injected cells emit a blue signal due to cleavage of the green fluorescence resonance energy transfer-based substrate CCF2/AM by β-lactamase. When cultured with a mutant EPEC unable to translocate effector proteins, myeloid DCs show rapid activation of NF-κB, secrete large amounts of proinflammatory cytokines and increase expression of CD80, CD83, and CD86, whereas wild-type EPEC barely elicits cytokine production and shuts off nuclear translocation of NF-κB p65. By deleting effector protein genes, we identified NleE as being critical for this effect. Expression of NleE in HeLa cells completely prevented nuclear p65 accumulation in response to IL1-β, and luciferase production in an NF-κB reporter cell line. DCs cocultured with wild-type EPEC or NleE-complemented strains were less potent at inducing MLR. EPEC was also able to inject effectors into DCs sending processes through model gut epithelium in a transwell system and into Peyer's patch myeloid DCs. Thus, EPEC translocate effectors into human DCs to dampen the inflammatory response elicited by its own pathogen-associated molecular patterns.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blotting, Western
  • Cell Separation
  • Coculture Techniques
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Dendritic Cells / microbiology*
  • Enteropathogenic Escherichia coli / immunology
  • Enteropathogenic Escherichia coli / metabolism
  • Enteropathogenic Escherichia coli / pathogenicity*
  • Enzyme-Linked Immunosorbent Assay
  • Escherichia coli Infections / immunology
  • Escherichia coli Infections / metabolism*
  • Escherichia coli Proteins / immunology
  • Escherichia coli Proteins / metabolism*
  • Flow Cytometry
  • Fluorescent Antibody Technique
  • HeLa Cells
  • Humans
  • Lymphocyte Culture Test, Mixed
  • Microscopy, Confocal
  • NF-kappa B / immunology
  • NF-kappa B / metabolism*
  • Signal Transduction / immunology*
  • Virulence Factors / immunology
  • Virulence Factors / metabolism*

Substances

  • Escherichia coli Proteins
  • NF-kappa B
  • NleE protein, E coli
  • Virulence Factors