Cyclooxygenase-2 expression and effect of celecoxib in gastric adenomas of trefoil factor 1-deficient mice

Cancer Res. 2003 Jun 15;63(12):3032-6.

Abstract

Expression of cyclooxygenase-2 (Cox-2) is elevated in gastric adenocarcinomas and precursor lesions leading to this disease. Mice deficient for trefoil factor 1 (TFF1) develop a pyloric adenoma with full penetrance. Because inhibition of Cox-2 suppresses tumor growth in several animal models, we studied expression of Cox-2 and effect of a selective Cox-2 inhibitor celecoxib in gastrointestinal tissues of the TFF1-deficient mice. Cox-2 mRNA and protein were strongly expressed in the pyloric adenomas of the TFF1(-/-) mice as detected by in situ hybridization and immunohistochemistry. Nonneoplastic gastrointestinal tissues of wild-type or TFF1(-/-) mice expressed low or nondetectable levels of Cox-2. Celecoxib (1600 ppm p.o. for 3 months) caused ulceration and inflammation of the adenoma in all treated TFF1(-/-) mice (n = 7). This effect of the drug was adenoma specific, because no histological alterations were observed in the non-neoplastic gastric or intestinal tissues in the TFF1(-/-) or wild-type mice receiving the drug treatment. All untreated TFF1(-/-) mice had an adenoma (n = 7), but none demonstrated the combination of ulceration and inflammation. Our data show that Cox-2 is expressed in gastric adenomas of the TFF1(-/-) mice and suggest that inhibition of Cox-2 disturbs the integrity of the adenoma by promoting ulceration and inflammation. These findings support the effort to initiate clinical studies to investigate the effect of Cox-2 inhibitors as a chemotherapeutic modality for dysplasias of the stomach.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoma / complications
  • Adenoma / drug therapy
  • Adenoma / enzymology*
  • Adenoma / genetics
  • Angiogenesis Inhibitors / blood
  • Angiogenesis Inhibitors / therapeutic use
  • Angiogenesis Inhibitors / toxicity
  • Animals
  • Celecoxib
  • Cyclooxygenase 2
  • Cyclooxygenase 2 Inhibitors
  • Cyclooxygenase Inhibitors / blood
  • Cyclooxygenase Inhibitors / therapeutic use
  • Cyclooxygenase Inhibitors / toxicity*
  • Enzyme Induction
  • Gastric Mucosa / drug effects
  • Gastric Mucosa / pathology
  • Gastritis / chemically induced*
  • Gastritis / etiology
  • Gene Expression Regulation, Neoplastic
  • Genetic Predisposition to Disease
  • Isoenzymes / antagonists & inhibitors
  • Isoenzymes / biosynthesis
  • Isoenzymes / physiology*
  • Mice
  • Mice, Knockout
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / physiology*
  • Peptides / deficiency*
  • Peptides / genetics
  • Prostaglandin-Endoperoxide Synthases / biosynthesis
  • Prostaglandin-Endoperoxide Synthases / physiology*
  • Pylorus* / drug effects
  • Pylorus* / pathology
  • Pyrazoles
  • RNA, Messenger / biosynthesis
  • RNA, Neoplasm / biosynthesis
  • Stomach Neoplasms / complications
  • Stomach Neoplasms / drug therapy
  • Stomach Neoplasms / enzymology*
  • Stomach Neoplasms / genetics
  • Stomach Ulcer / chemically induced*
  • Stomach Ulcer / etiology
  • Sulfonamides / blood
  • Sulfonamides / therapeutic use
  • Sulfonamides / toxicity*
  • Trefoil Factor-1

Substances

  • Angiogenesis Inhibitors
  • Cyclooxygenase 2 Inhibitors
  • Cyclooxygenase Inhibitors
  • Isoenzymes
  • Neoplasm Proteins
  • Peptides
  • Pyrazoles
  • RNA, Messenger
  • RNA, Neoplasm
  • Sulfonamides
  • Tff1 protein, mouse
  • Trefoil Factor-1
  • Cyclooxygenase 2
  • Prostaglandin-Endoperoxide Synthases
  • Celecoxib