Doc toxin is a kinase that inactivates elongation factor Tu

J Biol Chem. 2014 Mar 14;289(11):7788-98. doi: 10.1074/jbc.M113.544429. Epub 2014 Jan 21.

Abstract

The Doc toxin from bacteriophage P1 (of the phd-doc toxin-antitoxin system) has served as a model for the family of Doc toxins, many of which are harbored in the genomes of pathogens. We have shown previously that the mode of action of this toxin is distinct from the majority derived from toxin-antitoxin systems: it does not cleave RNA; in fact P1 Doc expression leads to mRNA stabilization. However, the molecular triggers that lead to translation arrest are not understood. The presence of a Fic domain, albeit slightly altered in length and at the catalytic site, provided a clue to the mechanism of P1 Doc action, as most proteins with this conserved domain inactivate GTPases through addition of an adenylyl group (also referred to as AMPylation). We demonstrated that P1 Doc added a single phosphate group to the essential translation elongation factor and GTPase, elongation factor (EF)-Tu. The phosphorylation site was at a highly conserved threonine, Thr-382, which was blocked when EF-Tu was treated with the antibiotic kirromycin. Therefore, we have established that Fic domain proteins can function as kinases. This distinct enzymatic activity exhibited by P1 Doc also solves the mystery of the degenerate Fic motif unique to the Doc family of toxins. Moreover, we have established that all characterized Fic domain proteins, even those that phosphorylate, target pivotal GTPases for inactivation through a post-translational modification at a single functionally critical acceptor site.

Keywords: Adenylylation; Antitoxin; Fic; GTPase; Phosphorylation; Post-translational Modification; Protein Synthesis; Translation; Translation Elongation Factors.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • Anti-Bacterial Agents / chemistry
  • Bacteriophage P1 / metabolism*
  • Binding Sites
  • Cell Proliferation
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / metabolism*
  • Gene Expression Regulation, Bacterial
  • Mass Spectrometry
  • Molecular Docking Simulation
  • Peptide Chain Elongation, Translational*
  • Peptide Elongation Factor Tu / metabolism*
  • Phosphorylation
  • Protein Binding
  • Protein Processing, Post-Translational
  • Protein Structure, Tertiary
  • Pyridones / chemistry
  • RNA, Messenger / metabolism
  • Recombinant Proteins / chemistry
  • Threonine / chemistry
  • Viral Proteins / metabolism*

Substances

  • Anti-Bacterial Agents
  • Doc protein, Enterobacteria phage P1
  • Escherichia coli Proteins
  • Pyridones
  • RNA, Messenger
  • Recombinant Proteins
  • Viral Proteins
  • Threonine
  • Peptide Elongation Factor Tu
  • tufB protein, E coli
  • mocimycin