HAMP Domain Rotation and Tilting Movements Associated with Signal Transduction in the PhoQ Sensor Kinase

mBio. 2015 May 26;6(3):e00616-15. doi: 10.1128/mBio.00616-15.

Abstract

HAMP domains are α-helical coiled coils that often transduce signals from extracytoplasmic sensing domains to cytoplasmic domains. Limited structural information has resulted in hypotheses that specific HAMP helix movement changes downstream enzymatic activity. These hypotheses were tested by mutagenesis and cysteine cross-linking analysis of the PhoQ histidine kinase, essential for resistance to antimicrobial peptides in a variety of enteric pathogens. These results support a mechanistic model in which periplasmic signals which induce an activation state generate a rotational movement accompanied by a tilt in α-helix 1 which activates kinase activity. Biochemical data and a high-confidence model of the PhoQ cytoplasmic domain indicate a possible physical interaction of the HAMP domain with the catalytic domain as necessary for kinase repression. These results support a model of PhoQ activation in which changes in the periplasmic domain lead to conformational movements in the HAMP domain helices which disrupt interaction between the HAMP and the catalytic domains, thus promoting increased kinase activity.

Importance: Most studies on the HAMP domain signaling states have been performed with chemoreceptors or the HAMP domain of Af1503. Full-length structures of the HAMP-containing histidine kinases VicK and CpxA or a hybrid between the HAMP domain of Af1503 and the EnvZ histidine kinase agree with the parallel four-helix bundle structure identified in Af1503 and provide snapshots of structural conformations experienced by HAMP domains. We took advantage of the fact that we can easily regulate the activation state of PhoQ histidine kinase to study its HAMP domain in the context of the full-length protein in living cells and provide biochemical evidence for different conformational states experienced by Salmonella enterica serovar Typhimurium PhoQ HAMP domain upon signaling.

Publication types

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

MeSH terms

  • Antimicrobial Cationic Peptides / metabolism
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Circular Dichroism
  • DNA Mutational Analysis
  • Histidine Kinase
  • Models, Molecular
  • Mutant Proteins / chemistry
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Protein Binding
  • Protein Conformation
  • Protein Kinases / chemistry*
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Protein Structure, Tertiary
  • Salmonella typhimurium / chemistry
  • Salmonella typhimurium / metabolism
  • Salmonella typhimurium / physiology*
  • Signal Transduction*

Substances

  • Antimicrobial Cationic Peptides
  • Bacterial Proteins
  • Mutant Proteins
  • PhoQ protein, Bacteria
  • Protein Kinases
  • Histidine Kinase