Endothelin-1 stimulates catalase activity through the PKCδ-mediated phosphorylation of serine 167

Free Radic Biol Med. 2014 Feb:67:255-64. doi: 10.1016/j.freeradbiomed.2013.10.814. Epub 2013 Nov 6.

Abstract

Our previous studies have shown that endothelin-1 (ET-1) stimulates catalase activity in endothelial cells and in lambs with acute increases in pulmonary blood flow (PBF), without altering gene expression. The purpose of this study was to investigate the molecular mechanism by which this occurs. Exposing pulmonary arterial endothelial cells to ET-1 increased catalase activity and decreased cellular hydrogen peroxide (H2O2) levels. These changes correlated with an increase in serine-phosphorylated catalase. Using the inhibitory peptide δV1.1, this phosphorylation was shown to be protein kinase Cδ (PKCδ) dependent. Mass spectrometry identified serine 167 as the phosphorylation site. Site-directed mutagenesis was used to generate a phospho-mimic (S167D) catalase. Activity assays using recombinant protein purified from Escherichia coli or transiently transfected COS-7 cells demonstrated that S167D catalase had an increased ability to degrade H2O2 compared to the wild-type enzyme. Using a phospho-specific antibody, we were able to verify that pS167 catalase levels are modulated in lambs with acute increases in PBF in the presence and absence of the ET receptor antagonist tezosentan. S167 is located on the dimeric interface, suggesting it could be involved in regulating the formation of catalase tetramers. To evaluate this possibility we utilized analytical gel filtration to examine the multimeric structure of recombinant wild-type and S167D catalase. We found that recombinant wild-type catalase was present as a mixture of monomers and dimers, whereas S167D catalase was primarily tetrameric. Further, the incubation of wild-type catalase with PKCδ was sufficient to convert wild-type catalase into a tetrameric structure. In conclusion, this is the first report indicating that the phosphorylation of catalase regulates its multimeric structure and activity.

Keywords: Catalase; Free radicals; Phosphorylation; Posttranslational regulation.

MeSH terms

  • Animals
  • COS Cells
  • Catalase / chemistry*
  • Catalase / genetics
  • Catalase / metabolism
  • Chlorocebus aethiops
  • Endothelial Cells / cytology
  • Endothelial Cells / drug effects*
  • Endothelial Cells / enzymology
  • Endothelin-1 / pharmacology*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Expression
  • Hydrogen Peroxide / antagonists & inhibitors
  • Hydrogen Peroxide / metabolism
  • Mutagenesis, Site-Directed
  • Oxidation-Reduction
  • Phosphorylation / drug effects
  • Primary Cell Culture
  • Protein Kinase C-delta / genetics*
  • Protein Kinase C-delta / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Protein Multimerization / drug effects
  • Pulmonary Artery / cytology
  • Pulmonary Artery / drug effects
  • Pulmonary Artery / enzymology
  • Pyridines / pharmacology
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Serine / metabolism
  • Sheep
  • Tetrazoles / pharmacology
  • Vasodilator Agents / pharmacology

Substances

  • Endothelin-1
  • Protein Kinase Inhibitors
  • Pyridines
  • Recombinant Proteins
  • Tetrazoles
  • Vasodilator Agents
  • Serine
  • tezosentan
  • Hydrogen Peroxide
  • Catalase
  • Protein Kinase C-delta