Insights into the mode of inhibition of human mitochondrial monoamine oxidase B from high-resolution crystal structures

Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9750-5. doi: 10.1073/pnas.1633804100. Epub 2003 Aug 11.

Abstract

Monoamine oxidase B (MAO-B) is an outer mitochondrial membrane-bound enzyme that catalyzes the oxidative deamination of arylalkylamine neurotransmitters and has been a target for a number of clinically used drug inhibitors. The 1.7-A structure of the reversible isatin-MAO-B complex has been determined; it forms a basis for the interpretation of the enzyme's structure when bound to either reversible or irreversible inhibitors. 1,4-Diphenyl-2-butene is found to be a reversible MAO-B inhibitor, which occupies both the entrance and substrate cavity space in the enzyme. Comparison of these two structures identifies Ile-199 as a "gate" between the two cavities. Rotation of the side chain allows for either separation or fusion of the two cavities. Inhibition of the enzyme with N-(2-aminoethyl)-p-chlorobenzamide results in the formation of a covalent N(5) flavin adduct with the phenyl ring of the inhibitor occupying a position in the catalytic site overlapping that of isatin. Inhibition of MAO-B with the clinically used trans-2-phenylcyclopropylamine results in the formation of a covalent C(4a) flavin adduct with an opened cyclopropyl ring and the phenyl ring in a parallel orientation to the flavin. The peptide bond between the flavin-substituted Cys-397 and Tyr-398 is in a cis conformation, which allows the proper orientation of the phenolic ring of Tyr-398 in the active site. The flavin ring exists in a twisted nonplanar conformation, which is observed in the oxidized form as well as in both the N(5) and the C(4a) adducts. An immobile water molecule is H-bonded to Lys-296 and to the N(5) of the flavin as observed in other flavin-dependent amine oxidases. The active site cavities are highly apolar; however, hydrophilic areas exist near the flavin and direct the amine moiety of the substrate for binding and catalysis. Small conformational changes are observed on comparison of the different inhibitor-enzyme complexes. Future MAO-B drug design will need to consider "induced fit" contributions as an element in ligand-enzyme interactions.

Publication types

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

MeSH terms

  • Catalytic Domain
  • Coenzymes / chemistry
  • Crystallography, X-Ray
  • Flavins / chemistry
  • Humans
  • In Vitro Techniques
  • Isatin / chemistry
  • Isatin / pharmacology
  • Mitochondria / enzymology
  • Models, Molecular
  • Monoamine Oxidase / chemistry*
  • Monoamine Oxidase Inhibitors / chemistry
  • Monoamine Oxidase Inhibitors / pharmacology*
  • Protein Conformation
  • Static Electricity

Substances

  • Coenzymes
  • Flavins
  • Monoamine Oxidase Inhibitors
  • Isatin
  • Monoamine Oxidase

Associated data

  • PDB/1OJ9
  • PDB/1OJA
  • PDB/1OJB
  • PDB/1OJC
  • PDB/1OJD