Active-site maturation and activity of the copper-radical oxidase GlxA are governed by a tryptophan residue

Biochem J. 2017 Feb 20;474(5):809-825. doi: 10.1042/BCJ20160968.

Abstract

GlxA from Streptomyces lividans is a mononuclear copper-radical oxidase and a member of the auxiliary activity family 5 (AA5). Its domain organisation and low sequence homology make it a distinct member of the AA5 family in which the fungal galactose 6-oxidase (Gox) is the best characterised. GlxA is a key cuproenzyme in the copper-dependent morphological development of S. lividans with a function that is linked to the processing of an extracytoplasmic glycan. The catalytic sites in GlxA and Gox contain two distinct one-electron acceptors comprising the copper ion and a 3'-(S-cysteinyl) tyrosine. The latter is formed post-translationally through a covalent bond between a cysteine and a copper-co-ordinating tyrosine ligand and houses a radical. In GlxA and Gox, a second co-ordination sphere tryptophan residue (Trp288 in GlxA) is present, but the orientation of the indole ring differs between the two enzymes, creating a marked difference in the π-π stacking interaction of the benzyl ring with the 3'-(S-cysteinyl) tyrosine. Differences in the spectroscopic and enzymatic activity have been reported between GlxA and Gox with the indole orientation suggested as a reason. Here, we report a series of in vivo and in vitro studies using the W288F and W288A variants of GlxA to assess the role of Trp288 on the morphology, maturation, spectroscopic and enzymatic properties. Our findings point towards a salient role for Trp288 in the kinetics of copper loading and maturation of GlxA, with its presence essential for stabilising the metalloradical site required for coupling catalytic activity and morphological development.

Keywords: EPR spectroscopy; free radicals; post-translational modification; radical-copper oxidase.

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Substitution
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Binding Sites
  • Catalytic Domain
  • Cations, Divalent
  • Cloning, Molecular
  • Copper / chemistry*
  • Copper / metabolism
  • Crystallography, X-Ray
  • Cysteine / chemistry
  • Cysteine / metabolism
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Fusarium / chemistry
  • Fusarium / enzymology
  • Fusarium / growth & development
  • Galactose Oxidase / chemistry*
  • Galactose Oxidase / genetics
  • Galactose Oxidase / metabolism
  • Gene Expression
  • Kinetics
  • Ligands
  • Mutation
  • Oxidoreductases / chemistry*
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Protein Binding
  • Protein Domains
  • Protein Structure, Secondary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Streptomyces lividans / chemistry*
  • Streptomyces lividans / enzymology
  • Streptomyces lividans / growth & development
  • Structural Homology, Protein
  • Substrate Specificity
  • Tryptophan / chemistry*
  • Tryptophan / metabolism
  • Tyrosine / chemistry
  • Tyrosine / metabolism

Substances

  • Bacterial Proteins
  • Cations, Divalent
  • Ligands
  • Recombinant Proteins
  • Tyrosine
  • Copper
  • Tryptophan
  • Oxidoreductases
  • Galactose Oxidase
  • copper oxidase
  • Cysteine