HMGB1 Binds to Lipoteichoic Acid and Enhances TNF-α and IL-6 Production through HMGB1-Mediated Transfer of Lipoteichoic Acid to CD14 and TLR2

J Innate Immun. 2015;7(4):405-16. doi: 10.1159/000369972. Epub 2015 Feb 5.

Abstract

Lipoteichoic acid (LTA) is a component of the cell wall of Gram-positive bacteria and induces a toll-like receptor 2 (TLR2)-mediated inflammatory response upon initial binding to lipopolysaccharide-binding protein (LBP) and subsequent transfer to CD14. In this study, we identified a novel role for the nuclear protein high-mobility group box 1 (HMGB1) in LTA-mediated inflammation. Results of ELISA, surface plasmon resonance and native PAGE electrophoretic mobility shift analyses indicated that HMGB1 binds to LTA in a concentration-dependent manner and that this binding is inhibited by LBP. Native PAGE, fluorescence-based transfer and confocal imaging analyses indicated that HMGB1 catalytically disaggregates LTA and transfers LTA to CD14. NF-κB p65 nuclear transmigration, degradation of IκBα and reporter assay results demonstrated that NF-κB activity in HEK293-hTLR2/6 cells is significantly upregulated by a mixture of LTA and soluble CD14 in the presence of HMGB1. Furthermore, the production of TNF-α and IL-6 in J774A.1 and RAW264.7 cells increased significantly following treatment with a mixture of LTA and HMGB1 compared with treatment with LTA or HMGB1 alone. Thus, we propose that HMGB1 plays an important role in LTA-mediated inflammation by binding to and transferring LTA to CD14, which is subsequently transferred to TLR2 to induce an inflammatory response.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • HEK293 Cells
  • HMGB1 Protein / genetics
  • HMGB1 Protein / immunology*
  • HMGB1 Protein / metabolism
  • Humans
  • Interleukin-6 / genetics
  • Interleukin-6 / immunology*
  • Interleukin-6 / metabolism
  • Lipopolysaccharide Receptors / genetics
  • Lipopolysaccharide Receptors / immunology*
  • Lipopolysaccharides / genetics
  • Lipopolysaccharides / immunology*
  • Lipopolysaccharides / metabolism
  • Protein Binding / genetics
  • Protein Binding / immunology
  • Teichoic Acids / genetics
  • Teichoic Acids / immunology*
  • Teichoic Acids / metabolism
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / immunology*
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • HMGB1 Protein
  • HMGB1 protein, human
  • IL6 protein, human
  • Interleukin-6
  • Lipopolysaccharide Receptors
  • Lipopolysaccharides
  • TLR2 protein, human
  • Teichoic Acids
  • Toll-Like Receptor 2
  • Tumor Necrosis Factor-alpha
  • lipoteichoic acid