Gemigliptin, a DPP4 inhibitor, ameliorates nonalcoholic steatohepatitis through AMP-activated protein kinase-independent and ULK1-mediated autophagy

Mol Metab. 2023 Dec:78:101806. doi: 10.1016/j.molmet.2023.101806. Epub 2023 Sep 20.

Abstract

Objective: Abnormal autophagic function and activated inflammasomes are typical features in the liver of patients with non-alcoholic steatohepatitis (NASH). Here, we explored whether gemigliptin, a dipeptidyl peptidase 4 (DPP4) inhibitor for treatment of type 2 diabetes, can induce autophagy and regulate inflammasome activation as a potential NASH treatment independent of its anti-diabetic effect.

Methods: Expression analysis was performed using human liver samples obtained from 18 subjects who underwent hepatectomy. We explored the function and mechanism of gemigliptin using a methionine- and choline-deficient diet (MCD)-induced NASH mouse model and HepG2 cells cultured in MCD-mimicking medium.

Results: Autophagy was suppressed by marked decreases in the expression of ULK1 and LC3II/LC3I ratio in human NAFLD/NASH patients, a NASH mouse model, and HepG2 cells cultured with MCD-mimicking media. Surprisingly, we found that the expression of p-AMPK decreased in liver tissues from patients with steatosis but was restored in NASH patients. The expression of p-AMPK in the NASH mouse model was similar to that of the control group. Hence, these results indicate that autophagy was reduced in NASH via an AMPK-independent pathway. However, gemigliptin treatment attenuated lipid accumulation, inflammation, and fibrosis in the liver of MCD diet-fed mice with restoration of ULK1 expression and autophagy induction. In vitro, gemigliptin alleviated inflammasome activation through induction of ULK1-dependent autophagy. Furthermore, gemigliptin treatment upregulated ULK1 expression and activated AMPK even after siRNA-mediated knockdown of AMPKα1/2 and ULK1, respectively.

Conclusions: Collectively, these results suggest that gemigliptin ameliorated NASH via AMPK-independent, ULK1-mediated effects on autophagy.

Keywords: Autophagy; DPP-4 inhibitor; Gemigliptin; Inflammasome; NASH; ULK-1.

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Animals
  • Autophagy
  • Autophagy-Related Protein-1 Homolog
  • Choline
  • Diabetes Mellitus, Type 2*
  • Dipeptidyl-Peptidase IV Inhibitors* / pharmacology
  • Dipeptidyl-Peptidase IV Inhibitors* / therapeutic use
  • Disease Models, Animal
  • Humans
  • Inflammasomes
  • Intracellular Signaling Peptides and Proteins
  • Methionine
  • Mice
  • Non-alcoholic Fatty Liver Disease* / drug therapy
  • Non-alcoholic Fatty Liver Disease* / metabolism

Substances

  • Dipeptidyl-Peptidase IV Inhibitors
  • AMP-Activated Protein Kinases
  • LC15-0444
  • Inflammasomes
  • Choline
  • Methionine
  • ULK1 protein, human
  • Autophagy-Related Protein-1 Homolog
  • Intracellular Signaling Peptides and Proteins