Analysis of cytochrome P450 CYP119 ligand-dependent conformational dynamics by two-dimensional NMR and X-ray crystallography

J Biol Chem. 2015 Apr 17;290(16):10000-17. doi: 10.1074/jbc.M114.627935. Epub 2015 Feb 10.

Abstract

Defining the conformational states of cytochrome P450 active sites is critical for the design of agents that minimize drug-drug interactions, the development of isoform-specific P450 inhibitors, and the engineering of novel oxidative catalysts. We used two-dimensional (1)H,(15)N HSQC chemical shift perturbation mapping of (15)N-labeled Phe residues and x-ray crystallography to examine the ligand-dependent conformational dynamics of CYP119. Active site Phe residues were most affected by the binding of azole inhibitors and fatty acid substrates, in agreement with active site localization of the conformational changes. This was supported by crystallography, which revealed movement of the F-G loop with various azoles. Nevertheless, the NMR chemical shift perturbations caused by azoles and substrates were distinguishable. The absence of significant chemical shift perturbations with several azoles revealed binding of ligands to an open conformation similar to that of the ligand-free state. In contrast, 4-phenylimidazole caused pronounced NMR changes involving Phe-87, Phe-144, and Phe-153 that support the closed conformation found in the crystal structure. The same closed conformation is observed by NMR and crystallography with a para-fluoro substituent on the 4-phenylimidazole, but a para-chloro or bromo substituent engendered a second closed conformation. An open conformation is thus favored in solution with many azole ligands, but para-substituted phenylimidazoles give rise to two closed conformations that depend on the size of the para-substituent. The results suggest that ligands selectively stabilize discrete cytochrome P450 conformational states.

Keywords: Conformational Change; Cytochrome P450; Molecular Dynamics; Nuclear Magnetic Resonance (NMR); X-ray Crystallography.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • Archaeal Proteins / antagonists & inhibitors
  • Archaeal Proteins / chemistry*
  • Archaeal Proteins / genetics
  • Archaeal Proteins / metabolism
  • Catalytic Domain
  • Crystallography, X-Ray
  • Cytochrome P-450 Enzyme System / chemistry*
  • Cytochrome P-450 Enzyme System / genetics
  • Cytochrome P-450 Enzyme System / metabolism
  • Enzyme Inhibitors / chemistry
  • Fatty Acids / chemistry
  • Gene Expression
  • Imidazoles / chemistry
  • Ligands
  • Models, Molecular*
  • Molecular Sequence Data
  • Nuclear Magnetic Resonance, Biomolecular
  • Peptide Mapping
  • Protein Stability
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sulfolobus acidocaldarius / chemistry*
  • Sulfolobus acidocaldarius / enzymology

Substances

  • Archaeal Proteins
  • Enzyme Inhibitors
  • Fatty Acids
  • Imidazoles
  • Ligands
  • Recombinant Proteins
  • Cytochrome P-450 Enzyme System
  • CYP119 protein, Sulfolobus solfataricus

Associated data

  • PDB/4TT5
  • PDB/4TUV
  • PDB/4WPD
  • PDB/4WQJ