Tetraacylated lipid A and paclitaxel-selective activation of TLR4/MD-2 conferred through hydrophobic interactions

J Immunol. 2014 Feb 15;192(4):1887-95. doi: 10.4049/jimmunol.1302119. Epub 2014 Jan 13.

Abstract

LPS exerts potent immunostimulatory effects through activation of the TLR4/MD-2 receptor complex. The hexaacylated lipid A is an agonist of mouse (mTLR4) and human TLR4/MD-2, whereas the tetraacylated lipid IVa and paclitaxel activate only mTLR4/MD-2 and antagonize activation of the human receptor complex. Hydrophobic mutants of TLR4 or MD-2 were used to investigate activation of human embryonic kidney 293 cells by different TLR4 agonists. We show that each of the hydrophobic residues F438 and F461, which are located on the convex face of leucine-rich repeats 16 and 17 of the mTLR4 ectodomain, are essential for activation of with lipid IVa and paclitaxel, which, although not a structural analog of LPS, activates cells expressing mTLR4/MD-2. Both TLR4 mutants were inactive when stimulated with lipid IVa or paclitaxel, but retained significant activation when stimulated with LPS or hexaacylated lipid A. We show that the phenylalanine residue at position 126 of mouse MD-2 is indispensable only for activation with paclitaxel. Its replacement with leucine or valine completely abolished activation with paclitaxel while preserving the responsiveness to lipid IVa and lipid A. This suggests specific interaction of paclitaxel with F126 because its replacement with leucine even augmented activation by lipid A. These results provide an insight into the molecular mechanism of TLR4 activation by two structurally very different agonists.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acylation
  • Animals
  • Binding Sites
  • Cell Line
  • Enzyme Activation
  • Glycolipids / chemistry
  • Glycolipids / immunology*
  • Glycolipids / pharmacology
  • HEK293 Cells
  • Humans
  • Hydrophobic and Hydrophilic Interactions
  • Lipid A / analogs & derivatives*
  • Lipid A / chemistry
  • Lipid A / immunology
  • Lipid A / pharmacology
  • Lymphocyte Antigen 96 / chemistry
  • Lymphocyte Antigen 96 / immunology*
  • Mice
  • Paclitaxel / chemistry
  • Paclitaxel / pharmacology*
  • Phenylalanine / chemistry
  • Protein Binding
  • Protein Structure, Tertiary
  • Toll-Like Receptor 4 / chemistry
  • Toll-Like Receptor 4 / immunology*
  • Tubulin Modulators / pharmacology*

Substances

  • Glycolipids
  • Lipid A
  • Lymphocyte Antigen 96
  • Toll-Like Receptor 4
  • Tubulin Modulators
  • lipid A precursors, bacterial
  • Phenylalanine
  • Paclitaxel