Identification of a misfolded region in superoxide dismutase 1 that is exposed in amyotrophic lateral sclerosis

J Biol Chem. 2014 Oct 10;289(41):28527-38. doi: 10.1074/jbc.M114.581801. Epub 2014 Aug 27.

Abstract

Mutations and aberrant post-translational modifications within Cu,Zn-superoxide dismutase (SOD1) cause this otherwise protective enzyme to misfold, leading to amyotrophic lateral sclerosis (ALS). The C4F6 antibody selectively binds misfolded SOD1 in spinal cord tissues from postmortem human ALS cases, as well as from an ALS-SOD1 mouse model, suggesting that the C4F6 epitope reports on a pathogenic conformation that is common to misfolded SOD1 variants. To date, the residues and structural elements that comprise this epitope have not been elucidated. Using a chemical cross-linking and mass spectrometry approach, we identified the C4F6 epitope within several ALS-linked SOD1 variants, as well as an oxidized form of WT SOD1, supporting the notion that a similar misfolded conformation is shared among pathological SOD1 proteins. Exposure of the C4F6 epitope was modulated by the SOD1 electrostatic (loop VII) and zinc binding (loop IV) loops and correlated with SOD1-induced toxicity in a primary microglia activation assay. Site-directed mutagenesis revealed Asp(92) and Asp(96) as key residues within the C4F6 epitope required for the SOD1-C4F6 binding interaction. We propose that stabilizing the functional loops within SOD1 and/or obscuring the C4F6 epitope are viable therapeutic strategies for treating SOD1-mediated ALS.

Keywords: Amyotrophic Lateral Sclerosis (ALS) (Lou Gehrig Disease); Microglia; Neurodegenerative Disease; Protein Cross-linking; Protein Misfolding; Superoxide Dismutase (SOD).

Publication types

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

MeSH terms

  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / metabolism*
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Antibodies, Monoclonal / biosynthesis
  • Antibodies, Monoclonal / chemistry
  • Antibodies, Monoclonal / isolation & purification
  • Epitopes / chemistry*
  • Epitopes / genetics
  • Epitopes / metabolism
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Expression
  • Humans
  • Hybridomas / immunology
  • Isoenzymes / chemistry
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Isoenzymes / toxicity
  • Mice
  • Microglia / cytology
  • Microglia / drug effects
  • Microglia / metabolism
  • Mutagenesis, Site-Directed
  • Mutation
  • Oxidation-Reduction
  • Primary Cell Culture
  • Protein Binding
  • Protein Folding
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Recombinant Proteins / toxicity
  • Spinal Cord / chemistry
  • Spinal Cord / pathology
  • Superoxide Dismutase / chemistry*
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase / toxicity
  • Superoxide Dismutase-1

Substances

  • Antibodies, Monoclonal
  • Epitopes
  • Isoenzymes
  • Recombinant Proteins
  • SOD1 protein, human
  • Sod1 protein, mouse
  • Superoxide Dismutase
  • Superoxide Dismutase-1