Structural basis for allosteric control of the transcription regulator CcpA by the phosphoprotein HPr-Ser46-P

Cell. 2004 Sep 17;118(6):731-41. doi: 10.1016/j.cell.2004.08.027.

Abstract

Carbon catabolite repression (CCR) is one of the most fundamental environmental-sensing mechanisms in bacteria and imparts competitive advantage by establishing priorities in carbon metabolism. In gram-positive bacteria, the master transcription regulator of CCR is CcpA. CcpA is a LacI-GalR family member that employs, as an allosteric corepressor, the phosphoprotein HPr-Ser46-P, which is formed in glucose-replete conditions. Here we report structures of the Bacillus megaterium apoCcpA and a CcpA-(HPr-Ser46-P)-DNA complex. These structures reveal that HPr-Ser46-P mediates a novel two-component allosteric DNA binding activation mechanism that involves both rotation of the CcpA subdomains and relocation of pivot-point residue Thr61, which leads to juxtaposition of the DNA binding regions permitting "hinge" helix formation in the presence of cognate DNA. The structure of the CcpA-(HPr-Ser46-P)-cre complex also reveals the elegant mechanism by which CcpA family-specific interactions with HPr-Ser46-P residues Ser46-P and His15 partition the high-energy CCR and low-energy PTS pathways, the latter requiring HPr-His15-P.

Publication types

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

MeSH terms

  • Allosteric Regulation / genetics
  • Amino Acid Motifs
  • Amino Acid Sequence / physiology
  • Bacillus megaterium / genetics
  • Bacillus megaterium / metabolism*
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • DNA / chemistry
  • DNA / genetics
  • DNA / metabolism*
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Histidine / metabolism
  • Models, Molecular
  • Molecular Sequence Data
  • Molecular Structure
  • Phosphoprotein Phosphatases / chemistry
  • Phosphoprotein Phosphatases / genetics
  • Phosphoprotein Phosphatases / metabolism*
  • Protein Binding / physiology
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Protein Structure, Tertiary / physiology
  • Repressor Proteins / chemistry
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Serine / metabolism
  • Threonine / metabolism
  • Transcription Factors / chemistry
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Bacterial Proteins
  • DNA-Binding Proteins
  • Repressor Proteins
  • Transcription Factors
  • catabolite control proteins, bacteria
  • Threonine
  • Serine
  • Histidine
  • DNA
  • HPr kinase
  • Protein Serine-Threonine Kinases
  • Phosphoprotein Phosphatases

Associated data

  • PDB/1RZR
  • PDB/1SXG
  • PDB/1SXH
  • PDB/1SXI