COX-2/EP2-EP4/β-catenin signaling regulates patulin-induced intestinal cell proliferation and inflammation

Toxicol Appl Pharmacol. 2018 Oct 1:356:224-234. doi: 10.1016/j.taap.2018.08.009. Epub 2018 Aug 20.

Abstract

Patulin (PAT), a mycotoxin, is a natural contaminant that is produced by certain species of Penicillium, Aspergillus and Byssochlamys. The major contamination of PAT is in apple and apple based products. PAT is known to cause glutathione depletion, oxidative DNA damage and cell proliferation. Recently, in vitro studies have indicated that PAT can also increase the intestinal epithelial permeability, modulate tight junctions and decrease transepithelial electrical resistance. Nonetheless, no previous study has evaluated the mechanisms responsible for PAT-induced intestinal toxicity or its relevance to the in vivo situation. Here, Wistar rats were orally treated with 100 μg/kg body weight (b.wt.) of PAT, either alone or along with 100 mg/kg b. wt. of celecoxib for 3 days. We found that PAT exposure led to significantly higher levels of PGE2 in serum and intestinal tissue and high expression of COX-2 and Ki-67 compared to controls. Interestingly, our results showed that celecoxib treatment could decrease the PAT-induced PGE2 and reduce the PAT-induced intestinal damage. To study the mechanistic aspect, normal rat intestinal epithelial cells (IEC-6) were treated with non-toxic concentrations (100 nM, 250 nM and 500 nM) of PAT for 6 h. It was observed that PAT exposure caused enhanced proliferation, higher expression of COX-2, and EP2 and EP4 receptors, along with increased PGE2 secretion. Additionally, PAT exposure caused enhanced Akt expression, which in turn inhibits GSK-3β and stabilizes β-catenin. Overall, our study suggests that the COX-2/EP2-EP4/β-catenin signaling cascades are involved in the regulation of PAT-induced intestinal cell proliferation and inflammation.

Keywords: Cell proliferation; Inflammation; Intestinal toxicity; Mycotoxin; Patulin; Prostaglandin E2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Celecoxib / pharmacology
  • Cell Proliferation / drug effects*
  • Cyclooxygenase 2 / drug effects*
  • Cyclooxygenase 2 Inhibitors / pharmacology
  • Dinoprostone / blood
  • Enteritis / drug therapy*
  • Enteritis / physiopathology
  • Epithelial Cells / drug effects
  • Glycoproteins
  • Intestines / cytology*
  • Intestines / drug effects*
  • Male
  • Oncogene Protein v-akt / biosynthesis
  • Patulin / pharmacology*
  • Plant Proteins
  • Rats
  • Rats, Wistar
  • Receptors, Prostaglandin E, EP2 Subtype / drug effects*
  • Receptors, Prostaglandin E, EP4 Subtype / drug effects
  • Signal Transduction / genetics*
  • Signal Transduction / physiology
  • beta Catenin / drug effects*

Substances

  • Ctnnb1 protein, rat
  • Cyclooxygenase 2 Inhibitors
  • EP4 glycoprotein, Daucus carota
  • Glycoproteins
  • Plant Proteins
  • Ptger2 protein, rat
  • Ptger4 protein, rat
  • Receptors, Prostaglandin E, EP2 Subtype
  • Receptors, Prostaglandin E, EP4 Subtype
  • beta Catenin
  • Patulin
  • Cyclooxygenase 2
  • Ptgs2 protein, rat
  • Oncogene Protein v-akt
  • Celecoxib
  • Dinoprostone