Expression of a cyclo-oxygenase-2 transgene in murine liver causes hepatitis

Gut. 2007 Jul;56(7):991-9. doi: 10.1136/gut.2006.097923. Epub 2006 Dec 5.

Abstract

Background: It has been proved that cyclo-oxygenase-2 (COX-2) is rapidly induced by inflammatory mediators. However, it is not known whether overexpression of COX-2 in the liver is sufficient to promote activation or secretion of inflammatory factors leading to hepatitis.

Aim: To investigate the role forced expression of COX-2 in liver by using inducible COX-2 transgenic (TG) mice.

Methods: TG mice that overexpress the human COX-2 gene in the liver using the liver-specific transthyretin promoter and non-TG littermates were derived and fed the normal diet for up to 12 months. Hepatic prostaglandin E(2) (PGE(2)) content was determined using enzyme immunoassay, nuclear factor kappaB (NF-kappaB) activation by electrophoretic mobility shift assays, apoptosis by terminal deoxynucleotidyl transferase-mediated dUTP-digoxigenin nick end labelling and proliferation by Ki-67 immunohistochemistry.

Results: COX-2 TG mice exhibited strongly increased COX-2 and PGE(2), elevated serum alanine aminotransferase level and histological hepatitis. Hepatic COX-2 expression in the TG mice resulted in activation of NF-kappaB and inflammatory cytokine cascade, with a marked expression of the proinflammatory cytokines tumour necrosis factor (TNF)-alpha (9.4-fold), interleukin (IL)-6 (4.4-fold), IL-1beta (3.6-fold), and of the anti-inflammatory cytokine IL-10 (4.4-fold) and chemokine macrophage inflammatory protein-2 (3.2-fold). The inflammatory response of the COX-2 TG mice was associated with infiltration macrophages and lymphocytes, increased cell proliferation and high rates of cell apoptosis. Administration of the COX-2 inhibitor celecoxib in TG mice restored liver histology to normal.

Conclusion: Enhanced COX-2 expression in hepatocytes is sufficient to induce hepatitis by activating NF-kappaB, stimulating the secretion of proinflammatory cytokines, recruiting macrophage and altering cell kinetics. Inhibition of COX-2 represents a mechanism-based chemopreventive approach to hepatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Celecoxib
  • Cell Proliferation
  • Chemokines / metabolism
  • Chemotaxis
  • Cyclooxygenase 2 / genetics
  • Cyclooxygenase 2 / metabolism
  • Cyclooxygenase 2 / physiology*
  • Cyclooxygenase 2 Inhibitors / therapeutic use
  • Cytokines / metabolism
  • Dinoprostone / metabolism
  • Female
  • Gene Expression
  • Growth Substances / metabolism
  • Hepatitis, Animal / drug therapy
  • Hepatitis, Animal / enzymology*
  • Hepatitis, Animal / pathology
  • Hepatocytes / enzymology
  • Immunoenzyme Techniques
  • Liver / enzymology
  • Liver / pathology
  • Lymphocytes / physiology
  • Macrophages / physiology
  • Mice
  • Mice, Transgenic
  • NF-kappa B / metabolism
  • Pyrazoles / therapeutic use
  • Sulfonamides / therapeutic use

Substances

  • Chemokines
  • Cyclooxygenase 2 Inhibitors
  • Cytokines
  • Growth Substances
  • NF-kappa B
  • Pyrazoles
  • Sulfonamides
  • Cyclooxygenase 2
  • Celecoxib
  • Dinoprostone