Reduction of inflammatory bowel disease-induced tumor development in IL-10 knockout mice with soluble epoxide hydrolase gene deficiency

Mol Carcinog. 2013 Sep;52(9):726-38. doi: 10.1002/mc.21918. Epub 2012 Apr 19.

Abstract

Soluble epoxide hydrolase (sEH) quickly inactivates anti-inflammatory epoxyeicosatrienoic acids (EETs) by converting them to dihydroxyeicosatrienoic acids (DHETs). Inhibition of sEH has shown effects against inflammation, but little is studied about the role of sEH in inflammatory bowel disease (IBD) and its induced carcinogenesis. In the present study, the effect of sEH gene deficiency on the development of IBD-induced tumor development was determined in IL-10 knockout mice combined with sEH gene deficiency. Tumor development in the bowel was examined at the age of 25 wk for male mice and 35 wk for female mice. Compared to IL-10(-/-) mice, sEH (-/-)/IL-10(-/-) mice exhibited a significant decrease of tumor multiplicity (2 ± 0.9 tumors/mouse vs. 1 ± 0.3 tumors/mouse) and tumor size (344.55 ± 71.73 mm³ vs. 126.94 ± 23.18 mm³), as well as a marked decrease of precancerous dysplasia. The significantly lower inflammatory scores were further observed in the bowel in sEH(-/-)/IL-10(-/-) mice as compared to IL-10(-/-) mice, including parameters of inflammation-involved area (0.70 ± 0.16 vs. 1.4 ± 0.18), inflammation cell infiltration (1.55 ± 0.35 vs. 2.15 ± 0.18), and epithelial hyperplasia (0.95 ± 0.21 vs. 1.45 ± 0.18), as well as larger ulcer formation. qPCR and Western blotting assays demonstrated a significant downregulation of cytokines/chemokines (TNF-α, MCP-1, and IL-12, 17, and 23) and NF-κB signals. Eicosanoid acid metabolic profiling revealed a significant increase of ratios of EETs to DHETs and EpOMEs to DiOMEs. These results indicate that sEH plays an important role in IBD and its-induced carcinogenesis and could serve as a highly potential target of chemoprevention and treatment for IBD.

Keywords: IL-10; carcinogenesis; eicosanoid acid metabolic profiling; inflammatory bowel disease; soluble epoxide hydrolase.

Publication types

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

MeSH terms

  • Animals
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / pathology*
  • Chemokine CCL2 / genetics
  • Down-Regulation
  • Eicosanoids / genetics
  • Epoxide Hydrolases / deficiency*
  • Epoxide Hydrolases / genetics
  • Female
  • Hyperplasia
  • Inflammation / genetics
  • Inflammation / pathology
  • Inflammatory Bowel Diseases / enzymology
  • Inflammatory Bowel Diseases / genetics
  • Inflammatory Bowel Diseases / pathology*
  • Interleukin-10 / deficiency*
  • Interleukin-10 / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-kappa B / genetics
  • Precancerous Conditions / genetics
  • Precancerous Conditions / pathology
  • Tumor Necrosis Factor-alpha / genetics

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Eicosanoids
  • NF-kappa B
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Epoxide Hydrolases