Up-regulation of PYK2/PKCα-dependent haem oxygenase-1 by CO-releasing molecule-2 attenuates TNF-α-induced lung inflammation

Br J Pharmacol. 2018 Feb;175(3):456-468. doi: 10.1111/bph.14094. Epub 2017 Dec 22.

Abstract

Background and purpose: Haem oxygenase-1 (HO-1) could provide cytoprotection against various inflammatory diseases. However, the mechanisms underlying the protective effect of CO-releasing molecule-2 (CORM-2)-induced HO-1 expression against TNF-α-induced inflammatory responses in human pulmonary alveolar epithelial cells (HPAEpiCs) remain unknown.

Experimental approach: CORM-2-induced HO-1 protein and mRNA expression, and signalling pathways were determined by Western blot and real-time PCR, coupled with respective pharmacological inhibitors or transfection with siRNAs. The effect of CORM-2 on TNF-α-induced increase in leukocyte counts in BAL fluid and VCAM-1 expression in lung was determined by cell counting and Western blot analysis.

Key results: CORM-2 attenuated the TNF-α-induced pulmonary haematoma, VCAM-1 expression and increase in leukocytes through an up-regulation of HO-1 in mice; this effect of CORM-2 was reversed by the HO-1 inhibitor zinc protoporphyrin IX. Furthermore, CORM-2 increased HO-1 protein and mRNA expression as well as the phosphorylation of PYK2, PKCα and ERK1/2 (p44/p42 MAPK) in HPAEpiCs; these effects were attenuated by their respective pharmacological inhibitors or transfection with siRNAs. Inhibition of PKCα by Gö6976 or Gö6983 attenuated CORM-2-induced stimulation of PKCα and ERK1/2 phosphorylation but had no effect on PYK2 phosphorylation. Moreover, inhibition of PYK2 by PF431396 reduced the phosphorylation of all three protein kinases. Finally, PYK2/PKCα/ERK1/2-mediated stimulation of activator protein 1 was shown to play a key role in CORM-2-induced HO-1 expression via an up-regulation of c-Fos mRNA.

Conclusions and implications: CORM-2 activates a PYK2/PKCα/ERK1/2/AP-1 pathway leading to HO-1 expression in HPAEpiCs. This HO-1/CO system might have potential as a therapeutic target in pulmonary inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Focal Adhesion Kinase 2 / biosynthesis*
  • Heme Oxygenase-1 / biosynthesis*
  • Humans
  • Male
  • Mice
  • Mice, Inbred ICR
  • Organometallic Compounds / pharmacology*
  • Organometallic Compounds / therapeutic use
  • Pneumonia / chemically induced
  • Pneumonia / metabolism*
  • Pneumonia / prevention & control
  • Protein Kinase C-alpha / biosynthesis*
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / toxicity*
  • Up-Regulation / physiology

Substances

  • Organometallic Compounds
  • Tumor Necrosis Factor-alpha
  • tricarbonyldichlororuthenium (II) dimer
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • Focal Adhesion Kinase 2
  • PRKCA protein, human
  • Protein Kinase C-alpha