Linagliptin ameliorates acetic acid-induced colitis via modulating AMPK/SIRT1/PGC-1α and JAK2/STAT3 signaling pathway in rats

Toxicol Appl Pharmacol. 2022 Mar 1:438:115906. doi: 10.1016/j.taap.2022.115906. Epub 2022 Feb 3.

Abstract

Ulcerative colitis is a chronic inflammatory disease, profoundly affecting the patient's quality of life and is associated with various complications. Linagliptin, a potent DPP- IV inhibitor, shows favorable anti-inflammatory effects in several animal model pathologies. To this end, the present study aimed to investigate the anti-inflammatory effect of linagliptin in a rat model of acetic acid-induced colitis. Moreover, the molecular mechanisms behind this effect were addressed. Accordingly, colitis was established by the administration of a 2 ml 6% acetic acid intrarectally and treatment with linagliptin (5 mg/kg) started 24 h after colitis induction and continued for 7 days. On one hand, the DPP-IV inhibitor alleviated the severity of colitis as evidenced by a decrease of disease activity index (DAI) scores, colon weight/length ratio, macroscopic damage, and histopathological deteriorations. Additionally, linagliptin diminished colon inflammation via attenuation of TNF-α, IL-6, and NF-κB p65 besides restoration of anti-inflammatory cytokine IL-10. On the other hand, linagliptin increased levels of p-AMPK, SIRT1, and PGC-1α while abolishing the increment in p-JAK2 and p-STAT3. In parallel linagliptin reduced mTOR levels and upregulated expression levels of SHP and MKP-1 which is postulated to mediate AMPK-driven JAK2/STAT3 inhibition. Based on these findings, linagliptin showed promising anti-inflammatory activity against acetic acid-induced colitis that is mainly attributed to the activation of the AMPK-SIRT1-PGC-1α pathway as well as suppression of the JAK2/STAT3 signaling pathway that might be partly mediated through AMPK activation.

Keywords: AMPK; Acetic acid; Linagliptin; STAT3; Ulcerative colitis.

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Acetic Acid / pharmacology*
  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Colitis / chemically induced*
  • Colitis / drug therapy*
  • Colitis / metabolism
  • Cytokines / metabolism
  • Disease Models, Animal
  • Inflammation / chemically induced
  • Inflammation / drug therapy
  • Inflammation / metabolism
  • Janus Kinase 2 / metabolism*
  • Linagliptin / pharmacology*
  • Male
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / metabolism
  • Rats
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / drug effects*
  • Sirtuin 1 / metabolism

Substances

  • Anti-Inflammatory Agents
  • Cytokines
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • STAT3 Transcription Factor
  • Stat3 protein, rat
  • Linagliptin
  • Jak2 protein, rat
  • Janus Kinase 2
  • AMP-Activated Protein Kinases
  • Sirtuin 1
  • Acetic Acid