Active-site topologies of human CYP2D6 and its aspartate-301 --> glutamate, asparagine, and glycine mutants

Arch Biochem Biophys. 1996 Jul 1;331(1):134-40. doi: 10.1006/abbi.1996.0291.

Abstract

Cytochrome P450 2D6 (CYP2D6) catalyzes the oxidation of substrates with a positively charged nitrogen atom 5-7 angstroms from the site of the oxidation. The active-site topology of CYP2D6 is examined here with phenyl-, 2-naphthyl-, and p-biphenyldiazene, which react with P450 enzymes to form sigma-bonded aryl-iron (Fe-Ar) complexes. Ferricyanide-mediated migration of the aryl group from the iron to the porphyrin nitrogens produces the N-arylprotoporphyrin IX regioisomers (NB:NA:NC:ND, in which the aryl group is bound to the nitrogen of pyrrole rings B, A, C, and D, respectively) in the following ratios (zero means <5%): phenyl, 10:90:00:00; 2-naphthyl, 09:91:00:00; and p-biphenyl, 16:84:00:00. These results suggest that the CYP2D6 active site is open above pyrrole ring A and to a small extent above pyrrole ring B but is closed above pyrrole rings C and D. This geometry differs from those determined by the same method for P450s for which crystal structures are available. Replacement of Asp-301 by a Glu, which preserves the carboxylate side chain, causes no detectable change in the N-aryl porphyrin regioisomer patterns and only minor changes in the catalytic activity. Replacement of Asp-301 by an Asn or Gly, which eliminates the negatively charged side chain, suppresses migration of the aryl groups to pyrrole ring B without impairing migration to pyrrole ring A and virtually abolishes catalytic activity. These results provide a refined model of the active site of CYP2D6. They confirm, furthermore, that the loss of activity observed when Asp-301 is replaced by a neutral residue is due to loss of the charge-pairing interaction with the substrate positive charge and/or subtle structural effects in the vicinity of pyrrole ring B, but not to major structural reorganization of the active site.

Publication types

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

MeSH terms

  • Asparagine
  • Aspartic Acid
  • Binding Sites
  • Cytochrome P-450 CYP2D6
  • Cytochrome P-450 Enzyme System / chemistry*
  • Cytochrome P-450 Enzyme System / genetics*
  • Electrochemistry
  • Glutamic Acid
  • Glycine
  • Humans
  • Hydrazines / chemistry
  • Imines / chemistry
  • Mixed Function Oxygenases / chemistry*
  • Mixed Function Oxygenases / genetics*
  • Models, Molecular
  • Molecular Structure
  • Mutation*
  • Protoporphyrins / chemistry
  • Saccharomyces cerevisiae / enzymology
  • Saccharomyces cerevisiae / genetics
  • Structure-Activity Relationship

Substances

  • Hydrazines
  • Imines
  • Protoporphyrins
  • Aspartic Acid
  • Glutamic Acid
  • Asparagine
  • Cytochrome P-450 Enzyme System
  • phenyldiazene
  • protoporphyrin IX
  • Mixed Function Oxygenases
  • Cytochrome P-450 CYP2D6
  • Glycine