Role of FAN in tumor necrosis factor-alpha and lipopolysaccharide-induced interleukin-6 secretion and lethality in D-galactosamine-sensitized mice

J Biol Chem. 2004 Apr 30;279(18):18648-55. doi: 10.1074/jbc.M314294200. Epub 2004 Feb 25.

Abstract

Tumor necrosis factor (TNF) alpha-induced neutral sphingomyelinase-mediated generation of ceramide, a bioactive lipid molecule, is transduced by the adaptor protein FAN, which binds to the intracellular region of the CD120a TNFalpha receptor. FAN-deficient mice do not exhibit any gross abnormality. To further explore the functions of FAN in vivo and because CD120a-deficient mice are resistant to endotoxin-induced liver failure and lethality, we investigated the susceptibility of FAN-deficient animals to lipopolysaccharide (LPS). We show that after d-galactosamine sensitization, FAN-deficient mice were partially resistant to LPS- and TNFalpha-induced lethality. Although LPS challenge resulted in a hepatic ceramide content lower in mutant mice than in control animals, it triggered similar histological alterations, caspase activation, and DNA fragmentation in the liver. Interestingly, LPS-induced elevation of IL-6 (but not TNFalpha) serum concentrations was attenuated in FAN-deficient mice. A less pronounced secretion of IL-6 was also observed after LPS or TNFalpha treatment of cultured peritoneal macrophages and embryonic fibroblasts isolated from FAN-deficient mice, as well as in human fibroblasts expressing a mutated FAN. Finally, we show that d-galactosamine-sensitized IL-6-deficient mice were partially resistant to endotoxin-induced liver apoptosis and lethality. These findings highlight the role of FAN and IL-6 in the inflammatory response initiated by endotoxin, implicating TNFalpha.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Cells, Cultured
  • Ceramides / analysis
  • Drug Resistance
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Galactosamine / administration & dosage
  • Galactosamine / pharmacology*
  • Humans
  • Interleukin-6 / blood
  • Interleukin-6 / metabolism*
  • Intracellular Signaling Peptides and Proteins
  • Lipopolysaccharides / pharmacology*
  • Lipopolysaccharides / poisoning
  • Liver / chemistry
  • Liver / cytology
  • Macrophages, Peritoneal / drug effects
  • Macrophages, Peritoneal / metabolism
  • Mice
  • Mice, Knockout
  • Proteins / physiology*
  • Survival Rate
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Tumor Necrosis Factor-alpha / poisoning

Substances

  • Ceramides
  • Interleukin-6
  • Intracellular Signaling Peptides and Proteins
  • Lipopolysaccharides
  • NSMAF protein, human
  • Nsmaf protein, mouse
  • Proteins
  • Tumor Necrosis Factor-alpha
  • Galactosamine