Effect of enterohaemorrhagic Escherichia coli O157:H7-specific enterohaemolysin on interleukin-1β production differs between human and mouse macrophages due to the different sensitivity of NLRP3 activation

Immunology. 2015 Jun;145(2):258-67. doi: 10.1111/imm.12442.

Abstract

Enterohaemorrhagic Escherichia coli (EHEC) O157:H7 infection in humans can cause acute haemorrhagic colitis and severe haemolytic uraemic syndrome. The role of enterohaemolysin (Ehx) in the pathogenesis of O157:H7-mediated disease in humans remains undefined. Recent studies have revealed the importance of the inflammatory response in O157:H7 pathogenesis in humans. We previously reported that Ehx markedly induced interleukin-1β (IL-1β) production in human macrophages. Here, we investigated the disparity in Ehx-induced IL-1β production between human and mouse macrophages and explored the underlying mechanism regarding the activation of NOD-like receptor family, pyrin domain containing 3 (NLRP3) inflammasomes. In contrast to the effects on human differentiated THP-1 cells and peripheral blood mononuclear cells, Ehx exerted no effect on IL-1β production in mouse macrophages and splenocytes because of a disparity in pro-IL-1β cleavage into mature IL-1β upon caspase-1 activation. Additionally, Ehx significantly contributed to O157:H7-induced ATP release from THP-1 cells, which was not detected in mouse macrophages. Confocal microscopy demonstrated that Ehx was a key inducer of cathepsin B release in THP-1 cells but not in mouse IC-21 cells upon O157:H7 challenge. Inhibitor experiments indicated that O157:H7-induced IL-1β production was largely dependent upon caspase-1 activation and partially dependent upon ATP signalling and cathepsin B release, which were both involved in NLRP3 activation. Moreover, inhibition of K(+) efflux drastically diminished O157:H7-induced IL-1β production and cytotoxicity. The findings in this study may shed light on whether and how the Ehx contributes to the development of haemolytic uraemic syndrome in human O157:H7 infection.

Keywords: enterohaemolysin; enterohaemorrhagic Escherichia coli; human; inflammasomes; interleukin-1β; mouse.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carrier Proteins / immunology*
  • Caspase 1 / immunology
  • Cathepsin B / immunology
  • Cell Line, Tumor
  • Escherichia coli O157*
  • Escherichia coli Proteins / toxicity*
  • Hemolysin Proteins / toxicity*
  • Hemolytic-Uremic Syndrome / immunology*
  • Hemolytic-Uremic Syndrome / pathology
  • Humans
  • Inflammasomes / immunology
  • Interleukin-1beta / immunology*
  • Macrophages / immunology*
  • Macrophages / pathology
  • Mice
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Species Specificity

Substances

  • Carrier Proteins
  • Escherichia coli Proteins
  • Hemolysin Proteins
  • IL1B protein, human
  • IL1B protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nlrp3 protein, mouse
  • enterohemolysin
  • CTSB protein, human
  • Cathepsin B
  • Ctsb protein, mouse
  • Caspase 1