Posttranslational modification and regulation of glutamate-cysteine ligase by the α,β-unsaturated aldehyde 4-hydroxy-2-nonenal

Free Radic Biol Med. 2011 Jan 1;50(1):14-26. doi: 10.1016/j.freeradbiomed.2010.10.694. Epub 2010 Oct 21.

Abstract

4-Hydroxy-2-nonenal (4-HNE) is a lipid peroxidation product formed during oxidative stress that can alter protein function via adduction of nucleophilic amino acid residues. 4-HNE detoxification occurs mainly via glutathione (GSH) conjugation and transporter-mediated efflux. This results in a net loss of cellular GSH, and restoration of GSH homeostasis requires de novo GSH biosynthesis. The rate-limiting step in GSH biosynthesis is catalyzed by glutamate-cysteine ligase (GCL), a heterodimeric holoenzyme composed of a catalytic (GCLC) and a modulatory (GCLM) subunit. The relative levels of the GCL subunits are a major determinant of cellular GSH biosynthetic capacity and 4-HNE induces the expression of both GCL subunits. In this study, we demonstrate that 4-HNE can alter GCL holoenzyme formation and activity via direct posttranslational modification of the GCL subunits in vitro. 4-HNE directly modified Cys553 of GCLC and Cys35 of GCLM in vitro, which significantly increased monomeric GCLC enzymatic activity, but reduced GCL holoenzyme activity and formation of the GCL holoenzyme complex. In silico molecular modeling studies also indicate these residues are likely to be functionally relevant. Within a cellular context, this novel posttranslational regulation of GCL activity could significantly affect cellular GSH homeostasis and GSH-dependent detoxification during periods of oxidative stress.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aldehydes / chemistry
  • Aldehydes / metabolism
  • Aldehydes / pharmacology*
  • Animals
  • Cysteine / metabolism
  • Cysteine Proteinase Inhibitors / pharmacology
  • Glutamate-Cysteine Ligase / chemistry
  • Glutamate-Cysteine Ligase / metabolism*
  • Humans
  • Lipid Peroxidation / drug effects
  • Lipid Peroxidation / physiology
  • Lysine / metabolism
  • Mass Spectrometry
  • Metabolic Detoxication, Phase I / physiology
  • Mice
  • Oxidative Stress / drug effects
  • Oxidative Stress / physiology
  • Protein Processing, Post-Translational / drug effects*
  • Protein Subunits / analysis
  • Protein Subunits / chemistry
  • Protein Subunits / metabolism
  • Stereoisomerism
  • Tumor Cells, Cultured

Substances

  • Aldehydes
  • Cysteine Proteinase Inhibitors
  • Protein Subunits
  • GCLM protein, human
  • Glutamate-Cysteine Ligase
  • 4-hydroxy-2-nonenal
  • Lysine
  • Cysteine