The proteasome as a lipopolysaccharide-binding protein in macrophages: differential effects of proteasome inhibition on lipopolysaccharide-induced signaling events

J Immunol. 2003 Aug 1;171(3):1515-25. doi: 10.4049/jimmunol.171.3.1515.

Abstract

We have developed a novel LPS probe using a highly purified and homogenous preparation of [(3)H] Escherichia coli LPS from the deep rough mutant, which contains a covalently linked, photoactivable 4-p-(azidosalicylamido)-butylamine group. This cross-linker was used to identify the LPS-binding proteins in membranes of the murine-macrophage-like cell line RAW 264.7. The alpha-subunit (PSMA1 C2, 29.5 kDa) and the beta-subunit (PSMB4 N3, 24.36 kDa) of the 20S proteasome complex were identified as LPS-binding proteins. This is the first report demonstrating LPS binding to enzymes such as the proteasome subunits. Functionally, LPS enhanced the chymotrypsin-like activity of the proteasome to degrade synthetic peptides in vitro and, conversely, the proteasome inhibitor lactacystin completely blocked the LPS-induced proteasome's chymotrypsin activity as well as macrophage TNF-alpha secretion and the expression of multiple inflammatory mediator genes. Lactacystin also completely blocked the LPS-induced expression of Toll-like receptor 2 mRNA. In addition, lactacystin dysregulated mitogen-activated protein kinase phosphorylation in LPS-stimulated macrophages, but failed to inhibit IL-1 receptor-associated kinase-1 activity. Importantly, lactacystin also prevented LPS-induced shock in mice. These data strongly suggest that the proteasome complex regulates the LPS-induced signal transduction and that it may be an important therapeutic target in Gram-negative sepsis.

Publication types

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

MeSH terms

  • Acetylcysteine / analogs & derivatives*
  • Acetylcysteine / pharmacology
  • Acute-Phase Proteins*
  • Animals
  • Carrier Proteins / metabolism*
  • Cell Line
  • Chymotrypsin / metabolism
  • Cross-Linking Reagents / chemical synthesis
  • Cysteine Endopeptidases / metabolism*
  • Cysteine Proteinase Inhibitors / pharmacology
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Down-Regulation / immunology
  • Enzyme Activation / immunology
  • Escherichia coli / chemistry
  • Escherichia coli / genetics
  • Glutamate Synthase / metabolism
  • Leupeptins / pharmacology
  • Lipopolysaccharides / administration & dosage
  • Lipopolysaccharides / antagonists & inhibitors
  • Lipopolysaccharides / chemical synthesis
  • Lipopolysaccharides / metabolism*
  • Lipopolysaccharides / pharmacology*
  • Macrophages / drug effects
  • Macrophages / enzymology*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages, Peritoneal / drug effects
  • Macrophages, Peritoneal / enzymology
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / metabolism
  • Membrane Glycoproteins*
  • Membrane Proteins / metabolism
  • Methanosarcina / enzymology
  • Mice
  • Mice, Inbred C3H
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / metabolism
  • Multienzyme Complexes / antagonists & inhibitors*
  • Multienzyme Complexes / metabolism*
  • Phosphorylation / drug effects
  • Proteasome Endopeptidase Complex
  • Shock, Septic / immunology
  • Shock, Septic / mortality
  • Shock, Septic / prevention & control
  • Signal Transduction / drug effects
  • Signal Transduction / immunology*
  • Tritium / metabolism

Substances

  • Acute-Phase Proteins
  • Carrier Proteins
  • Cross-Linking Reagents
  • Cysteine Proteinase Inhibitors
  • Leupeptins
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Membrane Proteins
  • Multienzyme Complexes
  • Re lipopolysaccharide
  • lipopolysaccharide-binding protein
  • Tritium
  • lactacystin
  • Glutamate Synthase
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • Chymotrypsin
  • Cysteine Endopeptidases
  • Proteasome Endopeptidase Complex
  • benzyloxycarbonylleucyl-leucyl-leucine aldehyde
  • Acetylcysteine