Structural basis for recognizing phosphoarginine and evolving residue-specific protein phosphatases in gram-positive bacteria

Cell Rep. 2013 Jun 27;3(6):1832-9. doi: 10.1016/j.celrep.2013.05.023. Epub 2013 Jun 13.

Abstract

Many cellular pathways are regulated by the competing activity of protein kinases and phosphatases. The recent identification of arginine phosphorylation as a protein modification in bacteria prompted us to analyze the molecular basis of targeting phospho-arginine. In this work, we characterize an annotated tyrosine phosphatase, YwlE, that counteracts the protein arginine kinase McsB. Strikingly, structural studies of YwlE reaction intermediates provide a direct view on a captured arginine residue. Together with biochemical data, the crystal structures depict the evolution of a highly specific phospho-arginine phosphatase, with the use of a size-and-polarity filter for distinguishing phosphorylated arginine from other phosphorylated side chains. To confirm the proposed mechanism, we performed bioinformatic searches for phosphatases, employing a similar selectivity filter, and identified a protein in Drosophila melanogaster exhibiting robust arginine phosphatase activity. In sum, our findings uncover the molecular framework for specific targeting of phospho-arginine and suggest that protein arginine (de)phosphorylation may be relevant in eukaryotes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Arginine / analogs & derivatives*
  • Arginine / chemistry
  • Arginine / genetics
  • Arginine / metabolism
  • Gram-Positive Bacteria / enzymology
  • Gram-Positive Bacteria / metabolism*
  • Humans
  • Molecular Sequence Data
  • Organophosphorus Compounds / chemistry
  • Organophosphorus Compounds / metabolism
  • Phosphoprotein Phosphatases / chemistry*
  • Phosphoprotein Phosphatases / genetics
  • Phosphoprotein Phosphatases / metabolism
  • Phosphorylation
  • Protein Processing, Post-Translational
  • Structure-Activity Relationship
  • Substrate Specificity

Substances

  • Organophosphorus Compounds
  • phospho-L-arginine
  • Arginine
  • Phosphoprotein Phosphatases

Associated data

  • PDB/4KK3
  • PDB/4KK4