Carbon monoxide released from its pharmacological donor, tricarbonyldichlororuthenium (II) dimer, accelerates the healing of pre-existing gastric ulcers

Br J Pharmacol. 2017 Oct;174(20):3654-3668. doi: 10.1111/bph.13968. Epub 2017 Aug 30.

Abstract

Background and purpose: Carbon monoxide (CO), a gaseous mediator produced by haem oxygenases (HOs), has been shown to prevent stress-, ethanol-, aspirin- and alendronate-induced gastric damage; however, its role in gastric ulcer healing has not been fully elucidated. We investigated whether CO released from tricarbonyldichlororuthenium (II) dimer (CORM-2) can affect gastric ulcer healing and determined the mechanisms involved in this healing action.

Experimental approach: Gastric ulcers were induced in Wistar rats by serosal application of acetic acid. Animals received 9 days of treatment with RuCl3 [2.5 mg·kg-1 intragastrically (i.g.)], haemin (5 mg·kg-1 i.g.), CORM-2 (0.1-10 mg·kg-1 i.g.) administered alone or with zinc protoporphyrin IX (ZnPP, 10 mg·kg-1 i.g.), 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ, 5 mg·kg-1 i.g.), NG -nitro-l-arginine (l-NNA, 15 mg·kg-1 i.g.), indomethacin (5 mg·kg-1 i.g.) or glibenclamide (10 mg·kg-1 i.g.). Gastric ulcer area and gastric blood flow (GBF) were assessed planimetrically, microscopically and by laser flowmeter respectively. Gastric mRNA/protein expressions of EGF, EGF receptors, VEGFA, HOs, nuclear factor (erythroid-derived 2)-like 2 (Nrf2), COX-2, hypoxia-inducible factor (HIF)-1α and pro-inflammatory iNOS, IL-1β and TNF-α were determined by real-time PCR or Western blots.

Key results: CORM-2 and haemin but not RuCl3 or ZnPP decreased ulcer size while increasing GBF. These effects were reduced by ODQ, indomethacin, l-NNA and glibenclamide. CORM-2 significantly decreased the expression of pro-inflammatory markers, Nrf2/HO1 and HIF-1α, and up-regulated EGF.

Conclusions and implications: CO released from CORM-2 or endogenously produced by the HO1/Nrf2 pathway accelerates gastric ulcer healing via an increase in GBF, an up-regulation in EGF expression and down-regulation of the inflammatory response.

MeSH terms

  • Acetic Acid
  • Animals
  • Carbon Monoxide / metabolism*
  • Cyclooxygenase 2 / genetics
  • Cyclooxygenase 2 / metabolism
  • Epidermal Growth Factor / genetics
  • ErbB Receptors / metabolism
  • Gastric Mucosa / metabolism
  • Heme Oxygenase (Decyclizing) / genetics
  • Heme Oxygenase (Decyclizing) / metabolism
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Interleukin-1beta / genetics
  • Male
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / metabolism
  • Organometallic Compounds / pharmacology
  • Organometallic Compounds / therapeutic use*
  • Rats, Wistar
  • Regional Blood Flow / drug effects
  • Stomach / blood supply
  • Stomach / drug effects
  • Stomach / pathology
  • Stomach Ulcer / chemically induced
  • Stomach Ulcer / drug therapy*
  • Stomach Ulcer / metabolism
  • Stomach Ulcer / pathology
  • Tumor Necrosis Factor-alpha / genetics
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Hif1a protein, rat
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • IL1B protein, rat
  • Interleukin-1beta
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, rat
  • Organometallic Compounds
  • Tumor Necrosis Factor-alpha
  • Vascular Endothelial Growth Factor A
  • tricarbonyldichlororuthenium (II) dimer
  • vascular endothelial growth factor A, rat
  • Epidermal Growth Factor
  • Carbon Monoxide
  • Nitric Oxide Synthase Type II
  • Nos2 protein, rat
  • Heme Oxygenase (Decyclizing)
  • Hmox1 protein, rat
  • heme oxygenase-2
  • Cyclooxygenase 2
  • Ptgs2 protein, rat
  • Egfr protein, rat
  • ErbB Receptors
  • Acetic Acid