Effect of metal loading and subcellular pH on net charge of superoxide dismutase-1

J Mol Biol. 2013 Nov 15;425(22):4388-404. doi: 10.1016/j.jmb.2013.07.018. Epub 2013 Jul 17.

Abstract

The net charge of a folded protein is hypothesized to influence myriad biochemical processes (e.g., protein misfolding, electron transfer, molecular recognition); however, few tools exist for measuring net charge and this elusive property remains undetermined--at any pH--for nearly all proteins. This study used lysine-acetyl "protein charge ladders" and capillary electrophoresis to measure the net charge of superoxide dismutase-1 (SOD1)--whose aggregation causes amyotrophic lateral sclerosis (ALS)--as a function of coordinated metal ions and pH. The net negative charge of apo-SOD1 was similar to predicted values; however, the binding of a single Zn(2+) or Cu(2+) ion reduced the net negative charge by a greater magnitude than predicted (i.e., ~4 units, instead of 2), whereas the SOD1 protein underwent charge regulation upon binding 2-4 metal ions. From pH5 to pH8 (i.e., a range consistent with the multiple subcellular loci of SOD1), the holo-SOD1 protein underwent smaller fluctuations in net negative charge than predicted (i.e., ~3 units, instead of ~14) and did not undergo charge inversion at its isoelectric point (pI=5.3) but remained anionic. The regulation of SOD1 net charge along its pathways of metal binding, and across solvent pH, provides insight into its metal-induced maturation and enzymatic activity (which remains diffusion-limited across pH5-8). The anionic nature of holo-SOD1 across subcellular pH suggests that ~45 different ALS-linked mutations to SOD1 will reduce its net negative charge regardless of subcellular localization.

Keywords: ALS; CE; ICP-MS; SOD1; TCEP; WT; amyloid; amyotrophic lateral sclerosis; capillary electrophoresis; copper; inductively coupled plasma-mass spectrometry; metal ions; protein misfolding; superoxide dismutase-1; tris(2-carboxyethyl)phosphine; wild-type; zinc.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acetylation
  • Buffers
  • Catalytic Domain
  • Copper / chemistry
  • Copper / metabolism
  • Humans
  • Hydrogen-Ion Concentration
  • Metals / chemistry*
  • Protein Folding
  • Static Electricity*
  • Superoxide Dismutase / chemistry*
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase-1
  • Zinc / chemistry
  • Zinc / metabolism

Substances

  • Buffers
  • Metals
  • SOD1 protein, human
  • Copper
  • Superoxide Dismutase
  • Superoxide Dismutase-1
  • Zinc