Quaternary structure of Dictyostelium discoideum nucleoside diphosphate kinase counteracts the tendency of monomers to form a molten globule

Biochemistry. 2003 Dec 16;42(49):14599-605. doi: 10.1021/bi035273w.

Abstract

Multimeric enzymes that lose their quaternary structure often cease to be catalytically competent. In these cases, conformational stability depends on contacts between subunits, and minor mutations affecting the surface of the monomers may affect overall stability. This effect may be sensitive to pH, temperature, or solvent composition. We investigated the role of oligomeric structure in protein stability by heat and chemical denaturation of hexameric nucleoside diphosphate kinase from Dictyostelium discoideum and its P105G mutant over a wide range of pH. The wild-type enzyme has been reported to unfold without prior dissociation into monomers, whereas monomer unfolding follows dissociation for the P105G mutant (Giartosio et al. (1996) J. Biol. Chem. 271, 17845-51). We show here that these features are also preserved at alkaline pH, with the wild-type enzyme always hexameric at room temperature whereas the mutant dissociates into monomers at pH >or=10. In acidic conditions (pH <or=6), even in the absence of denaturant, the predominant species for both proteins is an intermediate monomeric form with the characteristics of a molten globule: disordered tertiary native structure but preserved secondary structure. Monomers therefore seem to have a low intrinsic stability, which is overcome by the conformational organization in the oligomeric structure.

MeSH terms

  • Amino Acid Substitution / genetics
  • Anilino Naphthalenesulfonates / chemistry
  • Animals
  • Calorimetry, Differential Scanning
  • Chromatography, Gel
  • Circular Dichroism
  • Dictyostelium / enzymology*
  • Enzyme Activation
  • Enzyme Stability
  • Fluorescent Dyes / chemistry
  • Hydrogen-Ion Concentration
  • Nucleoside-Diphosphate Kinase / chemistry*
  • Nucleoside-Diphosphate Kinase / metabolism
  • Protein Binding
  • Protein Denaturation
  • Protein Folding
  • Protein Renaturation
  • Protein Structure, Quaternary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Spectrometry, Fluorescence
  • Thermodynamics
  • Urea / chemistry

Substances

  • Anilino Naphthalenesulfonates
  • Fluorescent Dyes
  • Recombinant Proteins
  • 5,5'-bis(8-(phenylamino)-1-naphthalenesulfonate)
  • Urea
  • Nucleoside-Diphosphate Kinase