An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1

Proc Natl Acad Sci U S A. 2012 Mar 27;109(13):5074-9. doi: 10.1073/pnas.1115402109. Epub 2012 Mar 13.

Abstract

Recent studies suggest that Cu/Zn superoxide dismutase (SOD1) could be pathogenic in both familial and sporadic amyotrophic lateral sclerosis (ALS) through either inheritable or nonheritable modifications. The presence of a misfolded WT SOD1 in patients with sporadic ALS, along with the recently reported evidence that reducing SOD1 levels in astrocytes derived from sporadic patients inhibits astrocyte-mediated toxicity on motor neurons, suggest that WT SOD1 may acquire toxic properties similar to familial ALS-linked mutant SOD1, perhaps through posttranslational modifications. Using patients' lymphoblasts, we show here that indeed WT SOD1 is modified posttranslationally in sporadic ALS and is iper-oxidized (i.e., above baseline oxidation levels) in a subset of patients with bulbar onset. Derivatization analysis of oxidized carbonyl compounds performed on immunoprecipitated SOD1 identified an iper-oxidized SOD1 that recapitulates mutant SOD1-like properties and damages mitochondria by forming a toxic complex with mitochondrial Bcl-2. This study conclusively demonstrates the existence of an iper-oxidized SOD1 with toxic properties in patient-derived cells and identifies a common SOD1-dependent toxicity between mutant SOD1-linked familial ALS and a subset of sporadic ALS, providing an opportunity to develop biomarkers to subclassify ALS and devise SOD1-based therapies that go beyond the small group of patients with mutant SOD1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis / enzymology*
  • Amyotrophic Lateral Sclerosis / pathology
  • Brain Stem / pathology*
  • Female
  • Humans
  • Lymphocytes / drug effects
  • Lymphocytes / enzymology
  • Male
  • Middle Aged
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitochondria / ultrastructure
  • Mutant Proteins / chemistry
  • Mutant Proteins / metabolism
  • Mutant Proteins / toxicity*
  • Oxidation-Reduction / drug effects
  • Protein Binding / drug effects
  • Protein Structure, Quaternary
  • Protein Transport / drug effects
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Superoxide Dismutase / adverse effects*
  • Superoxide Dismutase / chemistry
  • Superoxide Dismutase / metabolism*
  • Superoxide Dismutase / toxicity

Substances

  • Mutant Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Superoxide Dismutase