Haem oxygenase-1 up-regulation by rosiglitazone via ROS-dependent Nrf2-antioxidant response elements axis or PPARγ attenuates LPS-mediated lung inflammation

Br J Pharmacol. 2018 Oct;175(20):3928-3946. doi: 10.1111/bph.14465. Epub 2018 Sep 6.

Abstract

Background and purpose: Haem oxygenase-1 (HO-1) is induced by thiazolidinediones including rosiglitazone and exerts anti-inflammatory effects in various models. However, the molecular mechanisms underlying rosiglitazone-induced HO-1 expression remain largely unknown in human pulmonary alveolar epithelial cells (HPAEpiCs).

Experimental approach: HO-1 expression was determined by real time-PCR, Western blotting and promoter reporter analyses. Signalling pathways were investigated using pharmacological inhibitors or specific siRNAs. Interactions between nuclear factor erythroid-2-related factor (Nrf2) and antioxidant response elements (ARE) binding site of the HO-1 promoter were investigated with chromatin immunoprecipitation assays.

Key results: Up-regulation of HO-1 in HPAEpiCs or in mice by rosiglitazone blunted ICAM-1 expression and monocyte adhesion to HPAEpiCs challenged with LPS. Rosiglitazone-induced HO-1 expression was significantly attenuated by NADPH oxidase (NOX) inhibitors (apocynin and diphenyleneiodonium) or ROS scavenger (N-acetyl cysteine). The involvement of NOX activity and ROS generation in rosiglitazone-induced HO-1 expression was confirmed by transfection with p47phox or NOX2 siRNA. Moreover, pretreatment with the inhibitors of c-Src (c-Srci II), proline-rich tyrosine kinase 2 (Pyk2) (PF431396), Akt (Akti VIII) or PPARγ (GW9662) and transfection with siRNA of c-Src, Pyk2, Akt or PPARγ abolished the rosiglitazone-induced HO-1 expression in HPAEpiCs. Subsequently, Nrf2 was activated by phosphorylation of c-Src, Pyk2 and Akt, which turned on transcription of HO-1 gene by binding to AREs binding site and enhancing ARE promoter activity.

Conclusions and implications: Rosiglitazone induces HO-1 expression via either NOX/ROS/c-Src/Pyk2/Akt-dependent Nrf2 activation or PPARγ in HPAEpiCs and suppresses LPS-mediated inflammatory responses, suggesting that PPARγ agonists may be useful for protection against pulmonary inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Cell Line
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Heme Oxygenase-1 / metabolism*
  • Humans
  • Hypoglycemic Agents / pharmacology*
  • Lipopolysaccharides / pharmacology
  • Lung / cytology
  • Lung Diseases / metabolism*
  • Male
  • Mice, Inbred ICR
  • NF-E2-Related Factor 2 / metabolism
  • PPAR gamma / agonists
  • PPAR gamma / metabolism*
  • Reactive Oxygen Species / metabolism
  • Rosiglitazone / pharmacology*
  • Up-Regulation

Substances

  • Anti-Inflammatory Agents
  • Hypoglycemic Agents
  • Lipopolysaccharides
  • NF-E2-Related Factor 2
  • PPAR gamma
  • Reactive Oxygen Species
  • Rosiglitazone
  • Heme Oxygenase-1