Protein polyglutamylation catalyzed by the bacterial calmodulin-dependent pseudokinase SidJ

Elife. 2019 Nov 4:8:e51162. doi: 10.7554/eLife.51162.

Abstract

Pseudokinases are considered to be the inactive counterparts of conventional protein kinases and comprise approximately 10% of the human and mouse kinomes. Here, we report the crystal structure of the Legionella pneumophila effector protein, SidJ, in complex with the eukaryotic Ca2+-binding regulator, calmodulin (CaM). The structure reveals that SidJ contains a protein kinase-like fold domain, which retains a majority of the characteristic kinase catalytic motifs. However, SidJ fails to demonstrate kinase activity. Instead, mass spectrometry and in vitro biochemical analyses demonstrate that SidJ modifies another Legionella effector SdeA, an unconventional phosphoribosyl ubiquitin ligase, by adding glutamate molecules to a specific residue of SdeA in a CaM-dependent manner. Furthermore, we show that SidJ-mediated polyglutamylation suppresses the ADP-ribosylation activity. Our work further implies that some pseudokinases may possess ATP-dependent activities other than conventional phosphorylation.

Keywords: Legionella pneumophila; SdeA; SidJ; biochemistry; chemical biology; glutamylation; molecular biophysics; phosphoribosyl ubiquitination; structural biology; ubiquitin.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Bacterial Proteins / chemistry
  • Bacterial Proteins / metabolism*
  • Calmodulin / chemistry
  • Calmodulin / metabolism*
  • Crystallography, X-Ray
  • Glutamates / metabolism*
  • Humans
  • Legionella pneumophila / metabolism*
  • Mass Spectrometry
  • Membrane Proteins / metabolism*
  • Protein Conformation
  • Protein Processing, Post-Translational*
  • Virulence Factors / chemistry
  • Virulence Factors / metabolism*

Substances

  • Bacterial Proteins
  • Calmodulin
  • Glutamates
  • Membrane Proteins
  • SdeA protein, Legionella pneumophila
  • SidJ protein, Legionella pneumophila
  • Virulence Factors

Associated data

  • PDB/6PLM
  • PDB/5YIJ