Effects of the Escherichia coli toxin cytolysin A on mucosal immunostimulation via epithelial Ca2+ signalling and Toll-like receptor 4

Cell Microbiol. 2005 Jun;7(6):779-88. doi: 10.1111/j.1462-5822.2005.00510.x.

Abstract

Epithelial cells are vital to sense the presence of bacteria, thereby initiating a proper innate immune response. This occurs via different mechanisms, e.g. recognition by pattern recognition receptors (TLR), or alteration of the cellular Ca2+ homeostasis. The Escherichia coli toxin cytolysin A (ClyA) is naturally delivered to target cells as active pore assemblies within outer membrane vesicles (OMVs), and we here investigate a possible role of ClyA-containing OMVs (ClyA+ (OMV)) for induction of proinflammatory responses via the above-mentioned mechanisms. We report that low, sublytic concentrations of ClyA+ (OMV) affect the Ca2+ homeostasis in epithelial cells by induction of slow, intracellular Ca2+ oscillations, while increased concentrations act cytolytically. Thus, ClyA belongs to the novel group of pore-forming toxins shown to elicit such biphasic responses. Ca2+ waves in the minute range have been shown to regulate gene transcription of, e.g. interleukin (IL)-6 and -8. While the periodicity of ClyA+ (OMV)-induced Ca2+ waves (22.9 +/- 0.9 min) fail to induce an IL-8 response, our data fit to the general concept of frequency-specific gene expression. Molecular investigations of the signal transduction pathway reveals that ClyA+ (OMV) utilize a different one as compared with those previously reported for other toxins causing Ca2+ waves. The ClyA protein per se and ClyA pore assemblies are non-immunogenic, while lipopolysaccharide present on the OMVs induces a TLR4-dependent proinflammatory response as expected. Additional membrane components of the OMV, e.g. OmpW, was also found to elicit proinflammatory responses that was independent of TLR4 and Ca2+ signalling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Outer Membrane Proteins / immunology
  • Calcium / metabolism
  • Calcium Signaling*
  • Cells, Cultured
  • Epithelial Cells / immunology*
  • Epithelial Cells / microbiology
  • Escherichia coli / immunology
  • Escherichia coli Proteins / immunology
  • Escherichia coli Proteins / metabolism*
  • Female
  • Hemolysin Proteins / metabolism*
  • Humans
  • Immunity, Innate
  • Immunity, Mucosal
  • Interleukin-6 / metabolism
  • Interleukin-8 / metabolism
  • Lipopolysaccharides / toxicity
  • Membrane Glycoproteins / physiology*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Cell Surface / physiology*
  • Second Messenger Systems
  • Signal Transduction
  • Toll-Like Receptor 4
  • Toll-Like Receptors

Substances

  • Bacterial Outer Membrane Proteins
  • Escherichia coli Proteins
  • Hemolysin Proteins
  • Interleukin-6
  • Interleukin-8
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Receptors, Cell Surface
  • TLR4 protein, human
  • Tlr4 protein, rat
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • hlyE protein, E coli
  • ompW protein, E coli
  • Calcium