A single dipeptide sequence modulates the redox properties of a whole enzyme family

Fold Des. 1998;3(3):161-71. doi: 10.1016/S1359-0278(98)00024-8.

Abstract

Background: Disulfide exchange reactions are catalyzed by thiol/disulfide oxidoreductases. These enzymes possess a thioredoxin fold and contain a catalytic disulfide with the sequence Cys-X-X-Cys at the N terminus of an alpha helix. Despite these similarities, the various members differ strongly in their redox potentials (-122 mV to -270 mV). Using the strong oxidant DsbA from Escherichia coli as a model system, we investigated whether the redox properties of these enzymes can be modulated rationally by exchange of the X-X dipeptide.

Results: The X-X dipeptide of DsbA (Cys30-Pro31-His32-Cys33) was exchanged by the dipeptides of eukaryotic protein disulfide isomerase (PDI; Gly-His), glutaredoxin (Pro-Tyr), and thioredoxin (Gly-Pro) from E. coli. All variants were less oxidizing than wild-type DsbA and their redox potentials were in the order of the related natural enzymes (DsbA > PDI > glutaredoxin > thioredoxin). The equilibrium constant between glutathione and the thioredoxin-like variant increased 1200-fold compared with wild-type DsbA. The variants also showed a strong increase in the pKa of the nucleophilic cysteine (Cys30). As for glutaredoxin and thioredoxin, the catalytic disulfide stabilized the corresponding variants while destabilizing wild-type DsbA and the PDI-like variant.

Conclusions: The X-X dipeptide in the active site of thiol/disulfide oxidoreductases appears to be the main determinant of the redox properties of these enzymes. This empirical finding should be very useful for the design of new thiol/disulfide oxidoreductases with altered redox potentials and for studying the function of these enzymes in vivo.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Dipeptides*
  • Enzyme Stability
  • Glutaredoxins
  • Mutagenesis, Site-Directed
  • Oxidation-Reduction
  • Oxidoreductases*
  • Protein Disulfide-Isomerases / genetics
  • Protein Disulfide-Isomerases / metabolism*
  • Proteins / metabolism
  • Substrate Specificity
  • Sulfur-Sulfur Bond Isomerases / genetics
  • Sulfur-Sulfur Bond Isomerases / metabolism*
  • Thioredoxins / metabolism

Substances

  • Dipeptides
  • Glutaredoxins
  • Proteins
  • Thioredoxins
  • Oxidoreductases
  • Sulfur-Sulfur Bond Isomerases
  • Protein Disulfide-Isomerases