TLR4-MD-2 complex is negatively regulated by an endogenous ligand, globotetraosylceramide

Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):4714-9. doi: 10.1073/pnas.1218508110. Epub 2013 Mar 5.

Abstract

Although endogenous ligands for Toll-like receptor (TLR)4-myeloid differentiation factor 2 (MD2) have not been well-understood, we here report that a globo-series glycosphingolipid, globotetraosylceramide (Gb4), attenuates the toxicity of lipopolysaccharides (LPSs) by binding to TLR4-MD-2. Because α1,4-galactosyltransferase (A4galt)-deficient mice lacking globo-series glycosphingolipids showed higher sensitivity to LPS than wild-type mice, we examined mechanisms by which globo-series glycosphingolipids attenuate LPS toxicity. Cultured endothelial cells lacking A4galt showed higher expression of LPS-inducible genes upon LPS treatment. In turn, introduction of A4galt cDNA resulted in the neo expression of Gb4, leading to the reduced expression of LPS-inducible genes. Exogenous Gb4 induced similar effects. As a mechanism for the suppressive effects of Gb4 on LPS signals, specific binding of Gb4 to the LPS receptor TLR4-MD-2 was demonstrated by coprecipitation of Gb4 with recombinant MD-2 and by native PAGE. A docking model also supported these data. Taken together with colocalization of TLR4-MD-2 with Gb4 in lipid rafts after LPS stimulation, it was suggested that Gb4 competes with LPS for binding to TLR4-MD-2. Finally, administration of Gb4 significantly protected mice from LPS-elicited mortality. These results suggest that Gb4 is an endogenous ligand for TLR4-MD-2 and is capable of attenuating LPS toxicity, indicating the possibility for its therapeutic application in endotoxin shock.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Galactosyltransferases / genetics
  • Galactosyltransferases / immunology
  • Galactosyltransferases / metabolism
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Gene Expression Regulation / immunology
  • Globosides / genetics
  • Globosides / immunology*
  • Globosides / metabolism
  • Lipopolysaccharides / toxicity
  • Lymphocyte Antigen 96 / genetics
  • Lymphocyte Antigen 96 / immunology*
  • Lymphocyte Antigen 96 / metabolism
  • Membrane Microdomains / genetics
  • Membrane Microdomains / immunology
  • Membrane Microdomains / metabolism
  • Mice
  • Mice, Mutant Strains
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / immunology*
  • Multiprotein Complexes / metabolism
  • Protein Binding
  • Shock, Septic / chemically induced
  • Shock, Septic / genetics
  • Shock, Septic / immunology
  • Shock, Septic / metabolism
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology*
  • Toll-Like Receptor 4 / metabolism

Substances

  • Globosides
  • Lipopolysaccharides
  • Ly96 protein, mouse
  • Lymphocyte Antigen 96
  • Multiprotein Complexes
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • globotetraosylceramide
  • Galactosyltransferases