Bacterial pseudokinase catalyzes protein polyglutamylation to inhibit the SidE-family ubiquitin ligases

Science. 2019 May 24;364(6442):787-792. doi: 10.1126/science.aaw7446.

Abstract

Enzymes with a protein kinase fold transfer phosphate from adenosine 5'-triphosphate (ATP) to substrates in a process known as phosphorylation. Here, we show that the Legionella meta-effector SidJ adopts a protein kinase fold, yet unexpectedly catalyzes protein polyglutamylation. SidJ is activated by host-cell calmodulin to polyglutamylate the SidE family of ubiquitin (Ub) ligases. Crystal structures of the SidJ-calmodulin complex reveal a protein kinase fold that catalyzes ATP-dependent isopeptide bond formation between the amino group of free glutamate and the γ-carboxyl group of an active-site glutamate in SidE. We show that SidJ polyglutamylation of SidE, and the consequent inactivation of Ub ligase activity, is required for successful Legionella replication in a viable eukaryotic host cell.

Publication types

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

MeSH terms

  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Biocatalysis
  • Calmodulin / chemistry
  • Calmodulin / metabolism
  • Catalytic Domain
  • Crystallography, X-Ray
  • HEK293 Cells
  • Humans
  • Legionella pneumophila / enzymology*
  • Legionella pneumophila / genetics
  • Legionella pneumophila / pathogenicity
  • Phosphorylation
  • Polyglutamic Acid / chemistry
  • Polyglutamic Acid / genetics
  • Polyglutamic Acid / metabolism*
  • Protein Domains / genetics
  • Protein Kinases / chemistry
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination*
  • Virulence Factors / chemistry
  • Virulence Factors / genetics
  • Virulence Factors / metabolism*

Substances

  • Bacterial Proteins
  • Calmodulin
  • SidJ protein, Legionella pneumophila
  • Virulence Factors
  • Polyglutamic Acid
  • Ubiquitin-Protein Ligases
  • Protein Kinases