A Legionella effector ADP-ribosyltransferase inactivates glutamate dehydrogenase

J Biol Chem. 2021 Jan-Jun:296:100301. doi: 10.1016/j.jbc.2021.100301. Epub 2021 Jan 18.

Abstract

ADP-ribosyltransferases (ARTs) are a widespread superfamily of enzymes frequently employed in pathogenic strategies of bacteria. Legionella pneumophila, the causative agent of a severe form of pneumonia known as Legionnaire's disease, has acquired over 330 translocated effectors that showcase remarkable biochemical and structural diversity. However, the ART effectors that influence L. pneumophila have not been well defined. Here, we took a bioinformatic approach to search the Legionella effector repertoire for additional divergent members of the ART superfamily and identified an ART domain in Legionella pneumophila gene0181, which we hereafter refer to as Legionella ADP-Ribosyltransferase 1 (Lart1) (Legionella ART 1). We show that L. pneumophila Lart1 targets a specific class of 120-kDa NAD+-dependent glutamate dehydrogenase (GDH) enzymes found in fungi and protists, including many natural hosts of Legionella. Lart1 targets a conserved arginine residue in the NAD+-binding pocket of GDH, thereby blocking oxidative deamination of glutamate. Therefore, Lart1 could be the first example of a Legionella effector which directly targets a host metabolic enzyme during infection.

Keywords: ADP-ribosylation; bacterial pathogenesis; bioinformatics; cell metabolism; enzyme kinetics; glutamate; glutamate dehydrogenase; infectious disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP Ribose Transferases / chemistry*
  • ADP Ribose Transferases / genetics
  • ADP Ribose Transferases / metabolism
  • ADP-Ribosylation
  • Amino Acid Sequence
  • Amoeba / microbiology
  • Animals
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Binding Sites
  • Cloning, Molecular
  • Deamination
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Fungi
  • Gene Expression
  • Genetic Vectors / chemistry
  • Genetic Vectors / metabolism
  • Glutamate Dehydrogenase / chemistry*
  • Glutamate Dehydrogenase / genetics
  • Glutamate Dehydrogenase / metabolism
  • Host-Pathogen Interactions
  • Kinetics
  • Legionella pneumophila / enzymology
  • Legionella pneumophila / genetics*
  • Legionella pneumophila / pathogenicity
  • Models, Molecular
  • Oxidation-Reduction
  • Protein Binding
  • Protein Conformation, alpha-Helical
  • Protein Conformation, beta-Strand
  • Protein Interaction Domains and Motifs
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Substrate Specificity

Substances

  • Bacterial Proteins
  • Recombinant Proteins
  • Glutamate Dehydrogenase
  • ADP Ribose Transferases