Affinity of S100A1 protein for calcium increases dramatically upon glutathionylation

FEBS J. 2005 May;272(10):2557-65. doi: 10.1111/j.1742-4658.2005.04680.x.

Abstract

S100A1 is a typical representative of a group of EF-hand calcium-binding proteins known as the S100 family. The protein is composed of two alpha subunits, each containing two calcium-binding loops (N and C). At physiological pH (7.2) and NaCl concentration (100 mm), we determined the microscopic binding constants of calcium to S100A1 by analysing the Ca(2+)-titration curves of Trp90 fluorescence for both the native protein and its Glu32 --> Gln mutant with an inactive N-loop. Using a chelator method, we also determined the calcium-binding constant for the S100A1 Glu73 --> Gln mutant with an inactive C-loop. The protein binds four calcium ions in a noncooperative way with binding constants of K(1) =4 +/- 2 x 10(3) m(-1) (C-loops) and K(2) approximately 10(2) m(-1) (N-loops). Only when both loops are saturated with calcium does the protein change its global conformation, exposing to the solvent hydrophobic patches, which can be detected by 2-p-toluidinylnaphthalene-6-sulfonic acid - a fluorescent probe of protein-surface hydrophobicity. S-Glutathionylation of the single cysteine residue (85) of the alpha subunits leads to a 10-fold increase in the affinity of the protein C-loops for calcium and an enormous - four orders of magnitude - increase in the calcium-binding constants of its N-loops, owing to a cooperativity effect corresponding to DeltaDeltaG = -6 +/- 1 kcal.mol(-1). A similar effect is observed upon formation of the mixed disulfide with cysteine and 2-mercaptoethanol. The glutathionylated protein binds TRTK-12 peptide in a calcium-dependent manner. S100A1 protein can act, therefore, as a linker between the calcium and redox signalling pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium-Binding Proteins / chemistry
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism*
  • CapZ Actin Capping Protein
  • Cattle
  • Egtazic Acid / analogs & derivatives*
  • Egtazic Acid / metabolism
  • Fluorescent Dyes / metabolism
  • Glutathione / metabolism*
  • Mutation
  • Naphthalenesulfonates / metabolism
  • Oligopeptides / metabolism
  • Oxidation-Reduction
  • Peptide Fragments
  • Protein Binding
  • Protein Conformation
  • S100 Proteins
  • Tryptophan / metabolism

Substances

  • 5-nitro-1,2-bis(2-aminophenoxy)ethane-N,N,N'N'-tetraacetic acid
  • Calcium-Binding Proteins
  • CapZ Actin Capping Protein
  • Fluorescent Dyes
  • Naphthalenesulfonates
  • Oligopeptides
  • Peptide Fragments
  • S100 Proteins
  • S100A1 protein
  • TRTK-12 peptide
  • Egtazic Acid
  • 2-(4-toluidino)-6-naphthalenesulfonic acid
  • Tryptophan
  • Glutathione
  • Calcium