A key hydrophobic patch identified in an AAA⁺ protein essential for its in trans inhibitory regulation

J Mol Biol. 2013 Aug 9;425(15):2656-69. doi: 10.1016/j.jmb.2013.04.024. Epub 2013 May 7.

Abstract

Bacterial enhancer binding proteins (bEBPs) are a subclass of the AAA(+) (ATPases Associated with various cellular Activities) protein family. They are responsible for σ(54)-dependent transcription activation during infection and function under many stressful growth conditions. The majority of bEBPs are regulated in their formation of ring-shaped hexameric self-assemblies via an amino-terminal domain through its phosphorylation or ligand binding. In contrast, the Escherichia coli phage shock protein F (PspF) is negatively regulated in trans by phage shock protein A (PspA). Up to six PspA subunits suppress PspF hexamer action. Here, we present biochemical evidence that PspA engages across the side of a PspF hexameric ring. We identify three key binding determinants located in a surface-exposed 'W56 loop' of PspF, which form a tightly packed hydrophobic cluster, the 'YLW' patch. We demonstrate the profound impact of the PspF W56 loop residues on ATP hydrolysis, the σ(54) binding loop 1, and the self-association interface. We infer from single-chain studies that for complete PspF inhibition to occur, more than three PspA subunits need to bind a PspF hexamer with at least two binding to adjacent PspF subunits. By structural modelling, we propose that PspA binds to PspF via its first two helical domains. After PspF binding-induced conformational changes, PspA may then share structural similarities with a bEBP regulatory domain.

Keywords: AAA(+); AAA(+) proteins; ATPases Associated with various cellular Activities; EDTA; PDB; Protein Data Bank; PspA; PspF; RNA polymerase; RNAP; WT; bEBP; bacterial enhancer binding protein; enhancer binding protein; ethylenediaminetetraacetic acid; phage shock protein A; phage shock protein F; wild type; σ54.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / metabolism*
  • Escherichia coli / chemistry
  • Escherichia coli / metabolism*
  • Escherichia coli Proteins / chemistry
  • Escherichia coli Proteins / metabolism*
  • Heat-Shock Proteins / chemistry
  • Heat-Shock Proteins / metabolism*
  • Hydrolysis
  • Models, Biological
  • Models, Molecular
  • Molecular Dynamics Simulation
  • Protein Binding
  • Protein Conformation
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • RNA Polymerase Sigma 54 / metabolism
  • Trans-Activators / chemistry
  • Trans-Activators / metabolism*

Substances

  • Bacterial Proteins
  • Escherichia coli Proteins
  • Heat-Shock Proteins
  • PspF protein, E coli
  • Trans-Activators
  • phage shock protein, Bacteria
  • Adenosine Triphosphate
  • RNA Polymerase Sigma 54