Reactive oxygen species-mediated DJ-1 monomerization modulates intracellular trafficking involving karyopherin β2

Mol Cell Biol. 2014 Aug;34(16):3024-40. doi: 10.1128/MCB.00286-14. Epub 2014 Jun 9.

Abstract

Mutations in DJ-1 are a cause of recessive, early-onset Parkinson's disease (PD). Although oxidative stress and mitochondrial integrity have been implicated in PD, it is largely unknown why neurons degenerate. DJ-1 is involved in oxidative stress-mediated responses and in mitochondrial maintenance; however, its specific function remains vague. Here we show that DJ-1 exhibits neuronal dynamic intracellular trafficking, with dimeric/monomeric cycling modulated by the oxidative environment. We demonstrate that oxidative stress enhances monomerization of wild-type cytosolic DJ-1, leading to nuclear recruitment. The pathogenic DJ-1/E163K variant is unable to homodimerize but is retained in the cytosol upon wild-type DJ-1 heterodimerization. We found that this wild-type/pathogenic heterodimer is disrupted by oxidative stress, leading to DJ-1/E163K mitochondrial translocation. We further demonstrated that endogenously expressed wild-type DJ-1 is imported into neuronal nuclei as a monomer and that nucleo-cytoplasmic transport is oxidative stress mediated. We identified a novel proline-tyrosine nuclear localization signal (PY-NLS) in DJ-1, and we found that nuclear monomeric DJ-1 import is mediated by an oxidative stress-dependent interaction with karyopherin β2. Our study provides evidence that oxidative stress-mediated intracellular trafficking of DJ-1, mediated by dynamic DJ-1 dimeric/monomeric cycling, is implicated in PD pathogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism*
  • Cytosol / metabolism
  • Female
  • Humans
  • Mice
  • Mitochondria
  • Neurons / metabolism
  • Oncogene Proteins / genetics
  • Oncogene Proteins / metabolism*
  • Oxidative Stress*
  • Parkinson Disease / genetics
  • Parkinson Disease / metabolism*
  • Peroxiredoxins
  • Protein Deglycase DJ-1
  • Protein Transport / genetics
  • RNA-Binding Proteins / genetics
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction / genetics
  • beta Karyopherins / metabolism*

Substances

  • Oncogene Proteins
  • RNA-Binding Proteins
  • Reactive Oxygen Species
  • TNPO1 protein, human
  • beta Karyopherins
  • Peroxiredoxins
  • PARK7 protein, mouse
  • Protein Deglycase DJ-1