Tumor necrosis factor-alpha-induced reduction of glomerular filtration rate in rats with fulminant hepatic failure

Lab Invest. 2014 Jul;94(7):740-51. doi: 10.1038/labinvest.2014.71. Epub 2014 Jun 2.

Abstract

The mechanism of renal failure during fulminant hepatic failure (FHF) or end-stage of liver disease is not fully understood. The present study aims to delineate the mechanisms of decreased glomerular filtration rate (GFR) in acute hepatic failure. A rat model of renal insufficiency in severe liver injury was established by lipopolysaccharide (LPS) plus D-galactosamine (GalN) exposure. GFR was evaluated by continuous infusion of fluorescein isothiocyanate-inulin with implanted micro-osmotic pumps. GalN/LPS intoxication resulted in severe hepatocyte toxicity as evidenced by liver histology and biochemical tests, whereas renal morphology remained normal. GFR was reduced by 33% of the controls 12 h after GalN/LPS exposure, accompanied with a decreased serum sodium levels, a marked increase in serum TNF-α and ET-1 levels as well as significantly upregulated renal type 1 inositol 1,4,5-trisphosphate receptor (IP3R1) expression. The upregulated IP3R1 expression was abrogated by the treatment of anti-TNF-α antibodies, but not by 2-aminoethoxydiphenylborate (2-APB), which blocks the inositol 1,4,5-trisphosphate signaling pathway. Treatments with either TNF-α antibodies or 2-APB also significantly improved the compromised GFR, elevated serum urea nitrogen and creatinine levels, and reversed the decrease in glomerular inulin space and the increase in glomerular calcium content in GalN/LPS-exposed rats. The extent of acute liver injury as reflected by serum ALT levels was much more attenuated by anti-TNF-α antibodies than by 2-APB. Liver histology further confirmed that anti-TNF-α antibodies conferred better protection than 2-APB in GalN/LPS-exposed rats. LPS-elicited TNF-α over-production is responsible for decreased GFR through IP3R1 overexpression, and the compromised GFR resulted in the development of acute renal failure in rats with FHF.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies / immunology
  • Antibodies / pharmacology
  • Blotting, Western
  • Boron Compounds / pharmacology
  • Calcium / metabolism
  • Galactosamine
  • Gene Expression / drug effects
  • Glomerular Filtration Rate / drug effects
  • Glomerular Filtration Rate / physiology*
  • Inositol 1,4,5-Trisphosphate / metabolism
  • Inositol 1,4,5-Trisphosphate Receptors / genetics
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism
  • Kidney Glomerulus / metabolism
  • Kidney Glomerulus / physiopathology
  • Kidney Glomerulus / ultrastructure
  • Lipopolysaccharides
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Liver Failure, Acute / chemically induced
  • Liver Failure, Acute / metabolism*
  • Liver Failure, Acute / physiopathology*
  • Male
  • Microscopy, Electron
  • Rats
  • Rats, Sprague-Dawley
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor-alpha / blood
  • Tumor Necrosis Factor-alpha / immunology
  • Tumor Necrosis Factor-alpha / metabolism*
  • Up-Regulation / drug effects

Substances

  • Antibodies
  • Boron Compounds
  • Inositol 1,4,5-Trisphosphate Receptors
  • Itpr1 protein, rat
  • Lipopolysaccharides
  • Tumor Necrosis Factor-alpha
  • Galactosamine
  • Inositol 1,4,5-Trisphosphate
  • 2-aminoethoxydiphenyl borate
  • Calcium