Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration

Biochim Biophys Acta. 2013 Nov;1830(11):4981-9. doi: 10.1016/j.bbagen.2013.07.002. Epub 2013 Jul 13.

Abstract

Background: Protein tyrosine nitration is a post-translational modification (PTM) mediated by nitric oxide-derived molecules. Peroxisomes are oxidative organelles in which the presence of nitric oxide (NO) has been reported.

Methods: We studied peroxisomal nitroproteome of pea leaves by high-performance liquid chromatography with tandem mass spectrometry (LC-MS/MS) and proteomic approaches.

Results: Proteomic analysis of peroxisomes from pea leaves detected a total of four nitro-tyrosine immunopositive proteins by using an antibody against nitrotyrosine. One of these proteins was found to be the NADH-dependent hydroxypyruvate reductase (HPR). The in vitro nitration of peroxisomal samples caused a 65% inhibition of HPR activity. Analysis of recombinant peroxisomal NADH-dependent HPR1 activity from Arabidopsis in the presence of H2O2, NO, GSH and peroxynitrite showed that the ONOO(-) molecule caused the highest inhibition of activity (51% at 5mM SIN-1), with 5mM H2O2 having no inhibitory effect. Mass spectrometric analysis of the nitrated recombinant HPR1 enabled us to determine that, among the eleven tyrosine present in this enzyme, only Tyr-97, Tyr-108 and Tyr-198 were exclusively nitrated to 3-nitrotyrosine by peroxynitrite. Site-directed mutagenesis confirmed Tyr198 as the primary site of nitration responsible for the inhibition on the enzymatic activity by peroxynitrite.

Conclusion: These findings suggest that peroxisomal HPR is a target of peroxynitrite which provokes a loss of function.

General significance: This is the first report demonstrating the peroxisomal NADH-dependent HPR activity involved in the photorespiration pathway is regulated by tyrosine nitration, indicating that peroxisomal NO metabolism may contribute to the regulation of physiological processes under no-stress conditions.

Keywords: 3-morpholinosydnonimine; GSH; GSNO; HPR; Hydroxypyruvate reductase; NO; Nitration; Nitric oxide; Nitro-proteome; ONOO(−); PTM; Peroxisome; Peroxynitrite; RNS; S-nitrosoglutathione; SIN-1; hydroxypyruvate reductase; nitric oxide; peroxynitrite; post-translational modification; reactive nitrogen species; reduced glutathione.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Arabidopsis / drug effects
  • Arabidopsis / enzymology
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Evolution, Molecular
  • Glutathione / pharmacology
  • Hydrogen Peroxide / pharmacology
  • Hydroxypyruvate Reductase / antagonists & inhibitors*
  • Hydroxypyruvate Reductase / genetics
  • Hydroxypyruvate Reductase / metabolism
  • Models, Molecular
  • Molecular Sequence Data
  • Nitrates / metabolism
  • Oxidation-Reduction / drug effects
  • Peroxisomes / drug effects
  • Peroxisomes / genetics
  • Peroxisomes / metabolism*
  • Peroxynitrous Acid / genetics
  • Peroxynitrous Acid / metabolism
  • Pisum sativum / enzymology
  • Pisum sativum / genetics
  • Pisum sativum / metabolism
  • Plant Leaves / genetics
  • Plant Leaves / metabolism
  • Proteome / drug effects
  • Proteome / genetics
  • Proteome / metabolism
  • Tyrosine / analogs & derivatives
  • Tyrosine / genetics
  • Tyrosine / metabolism*

Substances

  • Nitrates
  • Proteome
  • Peroxynitrous Acid
  • 3-nitrotyrosine
  • Tyrosine
  • Hydrogen Peroxide
  • Hydroxypyruvate Reductase
  • Glutathione