Activation mechanisms of transcriptional regulator CooA revealed by small-angle X-ray scattering

J Mol Biol. 2004 Aug 13;341(3):651-68. doi: 10.1016/j.jmb.2004.06.040.

Abstract

CooA, a heme-containing transcriptional activator, binds CO to the heme moiety and then undergoes a structural change that promotes the specific binding to the target DNA. To elucidate the activation mechanism coupled to CO binding, we investigated the CO-dependent structural transition of CooA with small-angle X-ray scattering (SAXS). In the absence of CO, the radius of gyration Rg and the second virial coefficient (A2) were 25.3(+/-0.5)A and -0.39(+/-0.25) x 10(-4)ml mol g(-2), respectively. CO binding caused a slight increase in Rg (by 0.5A) and a marked decrease in A2 (by 5.09 x 10(-4)ml mol g(-2)). The observed decrease in A2 points to higher attractive interactions between CO-bound CooA molecules in solution compared with CO-free CooA. Although the minor alternation of Rg rules out changes in the overall structure, the marked change in the surface properties points to a CO-induced conformational transition. The experimental Rg and SAXS curves of the two states did not agree with the crystal structure of CO-free CooA. We thus simulated the solution structures of CooA based on the experimental data using rigid-body refinements as well as low-resolution model reconstructions. Both results demonstrate that the hinge region connecting the N-terminal heme domain and C-terminal DNA-binding domain is kinked in CO-free CooA, so that the two domains are positioned close to each other. The CO-dependent structural change observed by SAXS corresponds to a slight swing of the DNA-binding domains away from the heme domains coupled with their rotation by about 8 degrees around the axis of 2-fold symmetry.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / chemistry
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism*
  • Carbon Monoxide / chemistry
  • Crystallography, X-Ray
  • Cyclic AMP / chemistry
  • DNA / chemistry
  • Gene Expression Regulation, Bacterial*
  • Heme / chemistry
  • Hemeproteins / chemistry*
  • Hemeproteins / metabolism*
  • Kinetics
  • Light
  • Models, Molecular
  • Protein Binding
  • Protein Conformation
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Scattering, Radiation
  • Spectrophotometry
  • Trans-Activators / chemistry*
  • Trans-Activators / metabolism*
  • Transcriptional Activation
  • Ultraviolet Rays
  • X-Rays

Substances

  • Amino Acids
  • Bacterial Proteins
  • CooA protein, Rhodospirillum rubrum
  • Hemeproteins
  • Trans-Activators
  • Heme
  • Carbon Monoxide
  • DNA
  • Cyclic AMP