Overexpression of 5-lipoxygenase and cyclooxygenase 2 in hamster and human oral cancer and chemopreventive effects of zileuton and celecoxib

Clin Cancer Res. 2005 Mar 1;11(5):2089-96. doi: 10.1158/1078-0432.CCR-04-1684.

Abstract

Purpose: Previous studies have suggested an important role of aberrant arachidonic acid metabolism, especially the cyclooxygenase (Cox) pathway, in oral carcinogenesis. However, it is unknown whether the 5-lipoxygenase (5-Lox) pathway contributes to oral carcinogenesis, and whether combination of inhibitors of both pathways may have synergistic or additive effects of chemoprevention.

Experimental design: 5-Lox expression was examined in 7,12-dimethylbenz[a]anthracene (DMBA)-induced hamster and human oral cancer tissues by immunohistochemistry, and Cox2 expression was investigated in hamster oral tissues using in situ hybridization. Zileuton (a specific 5-Lox inhibitor) and celecoxib (a specific Cox2 inhibitor), either alone or in combination, were investigated for their chemopreventive effects on the DMBA-induced hamster model at the post-initiation stage through topical application.

Results: 5-Lox was overexpressed during oral carcinogenesis in hamsters and humans, as well as Cox2 in the hamster tissues. In a chemoprevention study using the post-initiation DMBA model, incidence of hamster oral squamous cell carcinoma was reduced from 76.9% (20 of 26) to 45.8% (11 of 24, P < 0.05) and 32.1% (9 of 28, P < 0.01) by 3% and 6% topical zileuton, respectively; and to 57.6% (15 of 26, P > 0.05) and 50% (12 of 24, P < 0.05) by 3% and 6% topical celecoxib, respectively. When used in combination, celecoxib and zileuton (3% of each) had an additive inhibitory effect on the incidence of squamous cell carcinoma (36%, 9 of 25, P < 0.01). Other pathologic variables and the levels of leukotriene B4 and prostaglandin E2 of the hamster tissues were reduced as well.

Conclusions: The results clearly showed that both 5-Lox and Cox2 played important roles in oral carcinogenesis. Zileuton and celecoxib prevented oral carcinogenesis at the post-initiation stage through their inhibitory effects on arachidonic acid metabolism.

Publication types

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

MeSH terms

  • 9,10-Dimethyl-1,2-benzanthracene / administration & dosage
  • Animals
  • Arachidonate 5-Lipoxygenase / biosynthesis*
  • Arachidonic Acid / metabolism
  • Carcinogens / administration & dosage
  • Carcinoma, Squamous Cell / genetics*
  • Carcinoma, Squamous Cell / physiopathology
  • Carcinoma, Squamous Cell / prevention & control*
  • Celecoxib
  • Cell Transformation, Neoplastic*
  • Chemoprevention
  • Cricetinae
  • Cyclooxygenase 2
  • Cyclooxygenase 2 Inhibitors
  • Cyclooxygenase Inhibitors / pharmacology*
  • Disease Models, Animal
  • Humans
  • Hydroxyurea / analogs & derivatives*
  • Hydroxyurea / pharmacology*
  • Immunohistochemistry
  • In Situ Hybridization
  • Lipoxygenase Inhibitors / pharmacology*
  • Male
  • Membrane Proteins
  • Mesocricetus
  • Mouth Neoplasms / genetics*
  • Mouth Neoplasms / physiopathology
  • Mouth Neoplasms / prevention & control*
  • Neoplasms, Experimental
  • Prostaglandin-Endoperoxide Synthases / biosynthesis*
  • Pyrazoles / pharmacology*
  • Sulfonamides / pharmacology*
  • Up-Regulation

Substances

  • Carcinogens
  • Cyclooxygenase 2 Inhibitors
  • Cyclooxygenase Inhibitors
  • Lipoxygenase Inhibitors
  • Membrane Proteins
  • Pyrazoles
  • Sulfonamides
  • Arachidonic Acid
  • 9,10-Dimethyl-1,2-benzanthracene
  • Arachidonate 5-Lipoxygenase
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • Prostaglandin-Endoperoxide Synthases
  • Celecoxib
  • zileuton
  • Hydroxyurea