Escherichia coli α-hemolysin counteracts the anti-virulence innate immune response triggered by the Rho GTPase activating toxin CNF1 during bacteremia

PLoS Pathog. 2015 Mar 17;11(3):e1004732. doi: 10.1371/journal.ppat.1004732. eCollection 2015 Mar.

Abstract

The detection of the activities of pathogen-encoded virulence factors by the innate immune system has emerged as a new paradigm of pathogen recognition. Much remains to be determined with regard to the molecular and cellular components contributing to this defense mechanism in mammals and importance during infection. Here, we reveal the central role of the IL-1β signaling axis and Gr1+ cells in controlling the Escherichia coli burden in the blood in response to the sensing of the Rho GTPase-activating toxin CNF1. Consistently, this innate immune response is abrogated in caspase-1/11-impaired mice or following the treatment of infected mice with an IL-1β antagonist. In vitro experiments further revealed the synergistic effects of CNF1 and LPS in promoting the maturation/secretion of IL-1β and establishing the roles of Rac, ASC and caspase-1 in this pathway. Furthermore, we found that the α-hemolysin toxin inhibits IL-1β secretion without affecting the recruitment of Gr1+ cells. Here, we report the first example of anti-virulence-triggered immunity counteracted by a pore-forming toxin during bacteremia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacteremia / immunology
  • Bacterial Toxins / immunology*
  • Disease Models, Animal
  • Escherichia coli / immunology
  • Escherichia coli / pathogenicity
  • Escherichia coli Infections / immunology*
  • Escherichia coli Proteins / immunology*
  • Female
  • Hemolysin Proteins / immunology*
  • Host-Pathogen Interactions / immunology
  • Immunity, Innate / immunology*
  • Interleukin-1beta / biosynthesis
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Signal Transduction / immunology*
  • Virulence
  • Virulence Factors / immunology

Substances

  • Bacterial Toxins
  • Escherichia coli Proteins
  • Hemolysin Proteins
  • Hlya protein, E coli
  • Interleukin-1beta
  • Virulence Factors
  • cytotoxic necrotizing factor type 1

Grants and funding

Our laboratory is supported by INSERM, Ligue Nationale contre le Cancer, the French Government (National Research Agency, ANR) through the "Investments for the Future" LABEX SIGNALIFE ANR-11-LABX-0028-01 and ANR A05135AS, Association pour la Recherche sur le Cancer (ARC 3800, RAC13006AAA), and fellowship to M.D. from Infectiopôle Sud. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.