Activation of AMPK/mTOR-driven autophagy and inhibition of NLRP3 inflammasome by saxagliptin ameliorate ethanol-induced gastric mucosal damage

Life Sci. 2021 Sep 1:280:119743. doi: 10.1016/j.lfs.2021.119743. Epub 2021 Jun 21.

Abstract

Aims: Saxagliptin, a selective/potent dipeptidyl peptidase-4 inhibitor, has revealed remarkable anti-inflammatory features in murine models of nephrotoxicity, hepatic injury, and neuroinflammation. However, its potential effect on ethanol-induced gastric mucosal injury has not been examined. Hence, the present work investigated the prospect of saxagliptin to attenuate ethanol-evoked gastric injury, with emphasis on the AMPK/mTOR-driven autophagy and NLRP3/ASC/caspase-1 pathway.

Materials and methods: In ethanol-induced gastropathy, the gastric tissues were examined by immunohistochemistry, immunoblotting, histopathology, and ELISA.

Key findings: The results demonstrated that saxagliptin (10 mg/kg; by gavage) suppressed the gastric pathological signs (area of gastric ulcer and ulcer index scores), histopathologic aberrations/damage scores, without provoking hypoglycemia in rats. These protective features were attributed to the enhancement of gastric mucosal autophagy flux, as proven with increased expression of LC3-II and Beclin 1, decreased accumulation of p62 SQSTM1, and activation of the autophagy-linked AMPK/mTOR pathway by increasing the expression of p-AMPK/AMPK and decreasing the expression of the autophagy suppressor p-mTOR/mTOR signal. In tandem, saxagliptin counteracted the ethanol-induced pro-apoptotic events by downregulating Bax, upregulating Bcl2 protein, and lowering the Bax/Bcl2 ratio. Equally important, saxagliptin suppressed the NLRP3 inflammasome in the gastric tissue by lowering the expression of NLRP3, ASC, and nuclear NF-κBp65, decreasing the activity of caspase-1, and diminishing the IL-1β levels. In the same regard, saxagliptin suppressed the mucosal oxidative stress by lowering lipid peroxide levels, increasing GSH and GPx antioxidants, and activating Nrf2/HO-1 pathway.

Significance: Saxagliptin may be a promising intervention against ethanol-evoked gastropathy by activating AMPK/mTOR-driven autophagy and inhibiting NLRP3 inflammasome.

Keywords: Apoptosis; Autophagy; Ethanol; Inflammasome; Oxidative stress; Saxagliptin.

MeSH terms

  • AMP-Activated Protein Kinase Kinases
  • Adamantane / analogs & derivatives*
  • Adamantane / therapeutic use
  • Animals
  • Autophagy / drug effects*
  • Dipeptides / therapeutic use*
  • Dipeptidyl-Peptidase IV Inhibitors / therapeutic use*
  • Ethanol / adverse effects*
  • Inflammasomes / antagonists & inhibitors
  • Inflammasomes / metabolism
  • Male
  • NLR Family, Pyrin Domain-Containing 3 Protein / antagonists & inhibitors
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Protein Kinases / metabolism
  • Rats
  • Rats, Wistar
  • Signal Transduction / drug effects
  • Stomach Diseases / chemically induced*
  • Stomach Diseases / drug therapy*
  • Stomach Diseases / pathology
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Dipeptides
  • Dipeptidyl-Peptidase IV Inhibitors
  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, rat
  • Ethanol
  • saxagliptin
  • Protein Kinases
  • mTOR protein, rat
  • TOR Serine-Threonine Kinases
  • AMP-Activated Protein Kinase Kinases
  • Adamantane