Substrate selectivity of human cytochrome P450 2C9: importance of residues 476, 365, and 114 in recognition of diclofenac and sulfaphenazole and in mechanism-based inactivation by tienilic acid

Arch Biochem Biophys. 2003 Jan 1;409(1):80-91. doi: 10.1016/s0003-9861(02)00548-9.

Abstract

A series of six site-directed mutants of CYP 2C9 were constructed with the aim to better define the amino acid residues that play a critical role in substrate selectivity of CYP 2C9, particularly in three distinctive properties of this enzyme: (i) its selective mechanism-based inactivation by tienilic acid (TA), (ii) its high affinity and hydroxylation regioselectivity toward diclofenac, and (iii) its high affinity for the competitive inhibitor sulfaphenazole (SPA). The S365A mutant exhibited kinetic characteristics for the 5-hydroxylation of TA very similar to those of CYP 2C9; however, this mutant did not undergo any detectable mechanism-based inactivation by TA, which indicates that the OH group of Ser 365 could be the nucleophile forming a covalent bond with an electrophilic metabolite of TA in TA-dependent inactivation of CYP 2C9. The F114I mutant was inactive toward the hydroxylation of diclofenac; moreover, detailed analyses of its interaction with a series of SPA derivatives by difference visible spectroscopy showed that the high affinity of SPA to CYP 2C9 (K(s)=0.4 microM) was completely lost when the phenyl substituent of Phe 114 was replaced with the alkyl group of Ile (K(s)=190+/-20 microM), or when the phenyl substituent of SPA was replaced with a cyclohexyl group (K(s)=120+/-30 microM). However, this cyclohexyl derivative of SPA interacted well with the F114I mutant (K(s)=1.6+/-0.5 microM). At the opposite end, the F94L and F110I mutants showed properties very similar to those of CYP 2C9 toward TA and diclofenac. Finally, the F476I mutant exhibited at least three main differences compared to CYP 2C9: (i) big changes in the k(cat) and K(m) values for TA and diclofenac hydroxylation, (ii) a 37-fold increase of the K(i) value found for the inhibition of CYP 2C9 by SPA, and (iii) a great change in the regioselectivity of diclofenac hydroxylation, the 5-hydroxylation of this substrate by CYP 2C9 F476I exhibiting a k(cat) of 28min(-1). These data indicate that Phe 114 plays an important role in recognition of aromatic substrates of CYP 2C9, presumably via Pi-stacking interactions. They also provide the first experimental evidence showing that Phe 476 plays a crucial role in substrate recognition and hydroxylation by CYP 2C9.

MeSH terms

  • Amino Acids / chemistry
  • Anti-Infective Agents / pharmacology
  • Aryl Hydrocarbon Hydroxylases / chemistry*
  • Binding Sites
  • Crystallography, X-Ray
  • Cyclooxygenase Inhibitors / pharmacology
  • Cytochrome P-450 CYP2C9
  • Diclofenac / pharmacology*
  • Humans
  • Kinetics
  • Microsomes / metabolism
  • Models, Chemical
  • Models, Molecular
  • Mutagenesis, Site-Directed
  • Mutation
  • Phenylalanine / chemistry
  • Protein Binding
  • Protein Structure, Tertiary
  • Software
  • Spectrophotometry
  • Substrate Specificity
  • Sulfaphenazole / pharmacology*
  • Ticrynafen / pharmacology*
  • Time Factors
  • Ultraviolet Rays
  • Yeasts

Substances

  • Amino Acids
  • Anti-Infective Agents
  • Cyclooxygenase Inhibitors
  • Sulfaphenazole
  • Diclofenac
  • Phenylalanine
  • CYP2C9 protein, human
  • Cytochrome P-450 CYP2C9
  • Aryl Hydrocarbon Hydroxylases
  • Ticrynafen