Structural and mechanistic basis for protein glutamylation by the kinase fold

Mol Cell. 2021 Nov 4;81(21):4527-4539.e8. doi: 10.1016/j.molcel.2021.08.007. Epub 2021 Aug 17.

Abstract

The kinase domain transfers phosphate from ATP to substrates. However, the Legionella effector SidJ adopts a kinase fold, yet catalyzes calmodulin (CaM)-dependent glutamylation to inactivate the SidE ubiquitin ligases. The structural and mechanistic basis in which the kinase domain catalyzes protein glutamylation is unknown. Here we present cryo-EM reconstructions of SidJ:CaM:SidE reaction intermediate complexes. We show that the kinase-like active site of SidJ adenylates an active-site Glu in SidE, resulting in the formation of a stable reaction intermediate complex. An insertion in the catalytic loop of the kinase domain positions the donor Glu near the acyl-adenylate for peptide bond formation. Our structural analysis led us to discover that the SidJ paralog SdjA is a glutamylase that differentially regulates the SidE ligases during Legionella infection. Our results uncover the structural and mechanistic basis in which the kinase fold catalyzes non-ribosomal amino acid ligations and reveal an unappreciated level of SidE-family regulation.

Keywords: Legionella; SdeA; SdeB; SdeC; SdjA; SidE; SidJ; effectors; glutamylation; pseudokinase.

Publication types

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

MeSH terms

  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism
  • Calmodulin / chemistry
  • Catalysis
  • Catalytic Domain
  • Cryoelectron Microscopy
  • Legionella / enzymology
  • Mutagenesis
  • Peptides / chemistry
  • Protein Binding
  • Protein Conformation
  • Protein Domains
  • Protein Folding*
  • Proteins / chemistry*
  • Spectrometry, Fluorescence
  • Ubiquitin-Protein Ligases / chemistry
  • Virulence Factors / chemistry*
  • Virulence Factors / metabolism

Substances

  • Bacterial Proteins
  • Calmodulin
  • Peptides
  • Proteins
  • SidJ protein, Legionella pneumophila
  • Virulence Factors
  • Ubiquitin-Protein Ligases