Structure of microsomal cytochrome P450 2B4 complexed with the antifungal drug bifonazole: insight into P450 conformational plasticity and membrane interaction

J Biol Chem. 2006 Mar 3;281(9):5973-81. doi: 10.1074/jbc.M511464200. Epub 2005 Dec 21.

Abstract

To better understand ligand-induced structural transitions in cytochrome P450 2B4, protein-ligand interactions were investigated using a bulky inhibitor. Bifonazole, a broad spectrum antifungal agent, inhibits monooxygenase activity and induces a type II binding spectrum in 2B4dH(H226Y), a modified enzyme previously crystallized in the presence of 4-(4-chlorophenyl)imidazole (CPI). Isothermal titration calorimetry and tryptophan fluorescence quenching indicate no significant burial of protein apolar surface nor altered accessibility of Trp-121 upon bifonazole binding, in contrast to recent results with CPI. A 2.3 A crystal structure of 2B4-bifonazole reveals a novel open conformation with ligand bound in the active site, which is significantly different from either the U-shaped cleft of ligand-free 2B4 or the small active site pocket of 2B4-CPI. The O-shaped active site cleft of 2B4-bifonazole is widely open in the middle but narrow at the top. A bifonazole molecule occupies the bottom of the active site cleft, where helix I is bent approximately 15 degrees to accommodate the bulky ligand. The structure also defines unanticipated interactions between helix C residues and bifonazole, suggesting an important role of helix C in azole recognition by mammalian P450s. Comparison of the ligand-free 2B4 structure, the 2B4-CPI structure, and the 2B4-bifonazole structure identifies structurally plastic regions that undergo correlated conformational changes in response to ligand binding. The most plastic regions are putative membrane-binding motifs involved in substrate access or substrate binding. The results allow us to model the membrane-associated state of P450 and provide insight into how lipophilic substrates access the buried active site.

Publication types

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

MeSH terms

  • Antifungal Agents / chemistry
  • Antifungal Agents / metabolism*
  • Aryl Hydrocarbon Hydroxylases / chemistry*
  • Aryl Hydrocarbon Hydroxylases / metabolism
  • Binding Sites
  • Cell Membrane / metabolism*
  • Crystallography, X-Ray
  • Cytochrome P450 Family 2
  • Imidazoles / chemistry
  • Imidazoles / metabolism*
  • Microsomes / enzymology*
  • Models, Molecular
  • Molecular Structure
  • Protein Binding
  • Protein Structure, Tertiary*

Substances

  • Antifungal Agents
  • Imidazoles
  • Aryl Hydrocarbon Hydroxylases
  • Cytochrome P450 Family 2
  • cytochrome P-450 CYP2B4 (rabbit)
  • bifonazole

Associated data

  • PDB/2BDM