The stimulated innate resistance event in Bordetella pertussis infection is dependent on reactive oxygen species production

Infect Immun. 2013 Jul;81(7):2371-8. doi: 10.1128/IAI.00336-13. Epub 2013 Apr 29.

Abstract

The exacerbated induction of innate immune responses in airways can abrogate diverse lung infections by a phenomenon known as stimulated innate resistance (StIR). We recently demonstrated that the enhancement of innate response activation can efficiently impair Bordetella pertussis colonization in a Toll-like receptor 4 (TLR4)-dependent manner. The aim of this work was to further characterize the effect of lipopolysaccharide (LPS) on StIR and to identify the mechanisms that mediate this process. Our results showed that bacterial infection was completely abrogated in treated mice when the LPS of B. pertussis (1 μg) was added before (48 h or 24 h), after (24 h), or simultaneously with the B. pertussis challenge (10(7) CFU). Moreover, we detected that LPS completely cleared bacterial infection as soon as 2 h posttreatment. This timing suggests that the observed StIR phenomenon should be mediated by fast-acting antimicrobial mechanisms. Although neutrophil recruitment was already evident at this time point, depletion assays using an anti-GR1 antibody showed that B. pertussis clearance was achieved even in the absence of neutrophils. To evaluate the possible role of free radicals in StIR, we performed animal assays using the antioxidant N-acetyl cysteine (NAC), which is known to inactivate oxidant species. NAC administration blocked the B. pertussis clearance induced by LPS. Nitrite concentrations were also increased in the LPS-treated mice; however, the inhibition of nitric oxide synthetases did not suppress the LPS-induced bacterial clearance. Taken together, our results show that reactive oxygen species (ROS) play an essential role in the TLR4-dependent innate clearance of B. pertussis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcysteine / administration & dosage
  • Acetylcysteine / pharmacology
  • Animals
  • Bacterial Load
  • Bordetella Infections / immunology*
  • Bordetella Infections / microbiology
  • Bordetella pertussis / drug effects
  • Bordetella pertussis / immunology
  • Bordetella pertussis / pathogenicity*
  • Guanidines / pharmacology
  • Immunity, Innate*
  • Lipopolysaccharides / immunology
  • Lipopolysaccharides / pharmacology
  • Lung / immunology
  • Lung / microbiology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism
  • Nitrites / metabolism
  • Reactive Oxygen Species / immunology*
  • Time Factors
  • Toll-Like Receptor 4 / immunology

Substances

  • Guanidines
  • Lipopolysaccharides
  • Nitrites
  • Reactive Oxygen Species
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Nitric Oxide Synthase
  • pimagedine
  • Acetylcysteine