The crystal structure of the adenylation enzyme VinN reveals a unique β-amino acid recognition mechanism

J Biol Chem. 2014 Nov 7;289(45):31448-57. doi: 10.1074/jbc.M114.602326. Epub 2014 Sep 22.

Abstract

Adenylation enzymes play important roles in the biosynthesis and degradation of primary and secondary metabolites. Mechanistic insights into the recognition of α-amino acid substrates have been obtained for α-amino acid adenylation enzymes. The Asp residue is invariant and is essential for the stabilization of the α-amino group of the substrate. In contrast, the β-amino acid recognition mechanism of adenylation enzymes is still unclear despite the importance of β-amino acid activation for the biosynthesis of various natural products. Herein, we report the crystal structure of the stand-alone adenylation enzyme VinN, which specifically activates (2S,3S)-3-methylaspartate (3-MeAsp) in vicenistatin biosynthesis. VinN has an overall structure similar to that of other adenylation enzymes. The structure of the complex with 3-MeAsp revealed that a conserved Asp(230) residue is used in the recognition of the β-amino group of 3-MeAsp similar to α-amino acid adenylation enzymes. A mutational analysis and structural comparison with α-amino acid adenylation enzymes showed that the substrate-binding pocket of VinN has a unique architecture to accommodate 3-MeAsp as a β-amino acid substrate. Thus, the VinN structure allows the first visualization of the interaction of an adenylation enzyme with a β-amino acid and provides new mechanistic insights into the selective recognition of β-amino acids in this family of enzymes.

Keywords: Adenylation Enzyme; Antibiotics; Biosynthesis; Polyketide; Structural Biology; X-ray Crystallography; β-Amino Acid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Aminoglycosides / chemistry*
  • Bacterial Proteins / chemistry*
  • Crystallography, X-Ray
  • DNA Mutational Analysis
  • Escherichia coli / metabolism
  • Hydrogen Bonding
  • Lactams / chemistry*
  • Macrolides / chemistry*
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • N-Methylaspartate / chemistry
  • Nucleotidyltransferases / chemistry*
  • Phylogeny
  • Protein Binding
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Recombinant Proteins / chemistry
  • Sequence Homology, Amino Acid
  • Streptomyces / enzymology*
  • Substrate Specificity

Substances

  • Aminoglycosides
  • Bacterial Proteins
  • Lactams
  • Macrolides
  • Recombinant Proteins
  • vicenistatin
  • N-Methylaspartate
  • Nucleotidyltransferases

Associated data

  • PDB/3WV4
  • PDB/3WV5
  • PDB/3WVN