Phosphoinositide 3 kinase mediates Toll-like receptor 4-induced activation of NF-kappa B in endothelial cells

Infect Immun. 2003 Aug;71(8):4414-20. doi: 10.1128/IAI.71.8.4414-4420.2003.

Abstract

Many of the proinflammatory effects of gram-negative bacteria are elicited by the interaction of bacterial lipopolysaccharide (LPS) with Toll-like receptor 4 (TLR4) expressed on host cells. TLR4 signaling leads to activation of NF-kappa B and transcription of many genes involved in the inflammatory response. In this study, we examined the signaling pathways involved in NF-kappa B activation by TLR4 signaling in human microvascular endothelial cells. Akt is a major downstream target of phosphoinositide 3 kinase (PI3-kinase), and PI3-kinase activation is necessary and sufficient for Akt phosphorylation. Consequently, Akt kinase activation was used as a measure of PI3-kinase activity. In a stable transfection system, dominant-negative mutants of myeloid differentiation factor 88 (MyD88) and interleukin-1 (IL-1) receptor-associated kinase 1 (IRAK-1) (MyD88-TIR and IRAK-DD, respectively) blocked Akt kinase activity in response to LPS and IL-1 beta. A dominant-negative mutant (Mal-P/H) of MyD88 adapter-like protein (Mal), a protein with homology to MyD88, failed to inhibit LPS- or IL-1 beta-induced Akt activity. Moreover, a dominant-negative mutant of p85 (p85-DN) inhibited the NF-kappa B luciferase activity, IL-6 production, and I kappa B alpha degradation elicited by LPS and IL-1 beta but not that stimulated by tumor necrosis factor alpha. The dominant-negative mutant of Akt partially inhibited the NF-kappa B luciferase activity evoked by LPS and IL-1 beta. However, expression of a constitutively activated Akt failed to induce NF-kappa B luciferase activity. These findings indicate that TLR4- and IL-1R-induced PI3-kinase activity is mediated by the adapter proteins MyD88 and IRAK-1 but not Mal. Further, these studies suggest that PI3-kinase is an important mediator of LPS and IL-1 beta signaling leading to NF-kappa B activation in endothelial cells and that Akt is necessary but not sufficient for NF-kappa B activation by TLR4.

Publication types

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

MeSH terms

  • Cells, Cultured
  • Endothelium, Vascular / metabolism*
  • Enzyme Activation / drug effects
  • Gram-Negative Bacteria / pathogenicity
  • Humans
  • Interleukin-1 / pharmacology
  • Interleukin-1 Receptor-Associated Kinases
  • Interleukin-6 / biosynthesis
  • Lipopolysaccharides / toxicity
  • Membrane Glycoproteins / metabolism*
  • NF-kappa B / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Protein Kinases / genetics
  • Protein Kinases / metabolism
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Receptors, Cell Surface / metabolism*
  • Signal Transduction
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Interleukin-1
  • Interleukin-6
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • NF-kappa B
  • Proto-Oncogene Proteins
  • Receptors, Cell Surface
  • TLR4 protein, human
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • Tumor Necrosis Factor-alpha
  • Protein Kinases
  • AKT1 protein, human
  • Interleukin-1 Receptor-Associated Kinases
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt