Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B

J Immunol. 2004 Feb 15;172(4):2522-9. doi: 10.4049/jimmunol.172.4.2522.

Abstract

Although oxidative stress has been thought to play a general role in the activation of NF-kappaB, the involvement of reactive oxygen species (ROS) in facilitating nuclear translocation of NF-kappaB in neutrophils has not been described. In addition, the mechanisms by which ROS modulate the transcriptional activity of NF-kappaB in response to Toll-like receptor 4 (TLR4)-dependent signaling are not well characterized. To examine these issues, oxidant-dependent signaling events downstream of TLR4 were investigated in neutrophils stimulated with LPS. Pretreatment of neutrophils with the antioxidants N-acetylcysteine or alpha-tocopherol prevented LPS-induced nuclear translocation of NF-kappaB. Antioxidant treatment of LPS-stimulated neutrophils also inhibited the production of proinflammatory cytokines (TNF-alpha, macrophage inflammatory protein-2, and IL-1beta), as well as activation of the kinases IkappaB kinase alpha, IkappaB kinase beta, p38, Akt, and extracellular receptor-activated kinases 1 and 2. The decrease in cytoplasmic levels of IkappaBalpha produced by exposure of neutrophils to LPS was prevented by N-acetylcysteine or alpha-tocopherol. Activation of IL-1R-associated kinase-1 (IRAK-1) and IRAK-4 in response to LPS stimulation was inhibited by antioxidants. These results demonstrate that proximal events in TLR4 signaling, at or antecedent to IRAK-1 and IRAK-4 activation, are oxidant dependent and indicate that ROS can modulate NF-kappaB-dependent transcription through their involvement in early TLR4-mediated cellular responses.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Acetylcysteine / pharmacology
  • Active Transport, Cell Nucleus / immunology
  • Animals
  • Antioxidants / pharmacology
  • Cell Nucleus / immunology
  • Cell Nucleus / metabolism
  • Cells, Cultured
  • Cytokines / metabolism
  • Enzyme Activation / drug effects
  • Enzyme Activation / immunology
  • Enzyme Inhibitors / pharmacology
  • Enzyme Stability / drug effects
  • Enzyme Stability / immunology
  • I-kappa B Kinase
  • I-kappa B Proteins / metabolism
  • Inflammation Mediators / metabolism
  • Interleukin-1 Receptor-Associated Kinases
  • Lipopolysaccharides / pharmacology
  • Male
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred BALB C
  • Mitogen-Activated Protein Kinases / metabolism
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / metabolism*
  • Neutrophils / enzymology
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Oxidants / physiology
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Protein Kinases / metabolism
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Reactive Oxygen Species / metabolism*
  • Receptors, Cell Surface / physiology*
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • Up-Regulation / immunology
  • alpha-Tocopherol / pharmacology
  • p38 Mitogen-Activated Protein Kinases

Substances

  • Antioxidants
  • Cytokines
  • Enzyme Inhibitors
  • I-kappa B Proteins
  • Inflammation Mediators
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • NF-kappa B
  • Nfkbia protein, mouse
  • Oxidants
  • Proto-Oncogene Proteins
  • Reactive Oxygen Species
  • Receptors, Cell Surface
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • NF-KappaB Inhibitor alpha
  • Protein Kinases
  • Phosphotransferases (Alcohol Group Acceptor)
  • Interleukin-1 Receptor-Associated Kinases
  • Irak4 protein, mouse
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Chuk protein, mouse
  • I-kappa B Kinase
  • Ikbkb protein, mouse
  • Ikbke protein, mouse
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • alpha-Tocopherol
  • Acetylcysteine