Staphylococcal PknB as the first prokaryotic representative of the proline-directed kinases

PLoS One. 2010 Feb 4;5(2):e9057. doi: 10.1371/journal.pone.0009057.

Abstract

In eukaryotic cell types, virtually all cellular processes are under control of proline-directed kinases and especially MAP kinases. Serine/threonine kinases in general were originally considered as a eukaryote-specific enzyme family. However, recent studies have revealed that orthologues of eukaryotic serine/threonine kinases exist in bacteria. Moreover, various pathogenic species, such as Yersinia and Mycobacterium, require serine/threonine kinases for successful invasion of human host cells. The substrates targeted by bacterial serine/threonine kinases have remained largely unknown. Here we report that the serine/threonine kinase PknB from the important pathogen Staphylococcus aureus is released into the external milieu, which opens up the possibility that PknB does not only phosphorylate bacterial proteins but also proteins of the human host. To identify possible human targets of purified PknB, we studied in vitro phosphorylation of peptide microarrays and detected 68 possible human targets for phosphorylation. These results show that PknB is a proline-directed kinase with MAP kinase-like enzymatic activity. As the potential cellular targets for PknB are involved in apoptosis, immune responses, transport, and metabolism, PknB secretion may help the bacterium to evade intracellular killing and facilitate its growth. In apparent agreement with this notion, phosphorylation of the host-cell response coordinating transcription factor ATF-2 by PknB was confirmed by mass spectrometry. Taken together, our results identify PknB as the first prokaryotic representative of the proline-directed kinase/MAP kinase family of enzymes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activating Transcription Factor 2 / metabolism
  • Amino Acid Sequence
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Binding Sites
  • Blotting, Western
  • Humans
  • MAP Kinase Kinase 4 / metabolism
  • Mass Spectrometry
  • Mutation
  • Peptides / metabolism
  • Phosphorylation
  • Proline / metabolism*
  • Protein Array Analysis
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Staphylococcus aureus / enzymology*
  • Staphylococcus aureus / genetics
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • ATF2 protein, human
  • Activating Transcription Factor 2
  • Bacterial Proteins
  • Peptides
  • Proline
  • Protein Serine-Threonine Kinases
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 4