Selective Targeting by a Mechanism-Based Inactivator against Pyridoxal 5'-Phosphate-Dependent Enzymes: Mechanisms of Inactivation and Alternative Turnover

Biochemistry. 2017 Sep 19;56(37):4951-4961. doi: 10.1021/acs.biochem.7b00499. Epub 2017 Sep 6.

Abstract

Potent mechanism-based inactivators can be rationally designed against pyridoxal 5'-phosphate (PLP)-dependent drug targets, such as ornithine aminotransferase (OAT) or γ-aminobutyric acid aminotransferase (GABA-AT). An important challenge, however, is the lack of selectivity toward other PLP-dependent, off-target enzymes, because of similarities in mechanisms of all PLP-dependent aminotransferase reactions. On the basis of complex crystal structures, we investigate the inactivation mechanism of OAT, a hepatocellular carcinoma target, by (1R,3S,4S)-3-amino-4-fluorocyclopentane-1-carboxylic acid (FCP), a known inactivator of GABA-AT. A crystal structure of OAT and FCP showed the formation of a ternary adduct. This adduct can be rationalized as occurring via an enamine mechanism of inactivation, similar to that reported for GABA-AT. However, the crystal structure of an off-target, PLP-dependent enzyme, aspartate aminotransferase (Asp-AT), in complex with FCP, along with the results of attempted inhibition assays, suggests that FCP is not an inactivator of Asp-AT, but rather an alternate substrate. Turnover of FCP by Asp-AT is also supported by high-resolution mass spectrometry. Amid existing difficulties in achieving selectivity of inactivation among a large number of PLP-dependent enzymes, the obtained results provide evidence that a desirable selectivity could be achieved, taking advantage of subtle structural and mechanistic differences between a drug-target enzyme and an off-target enzyme, despite their largely similar substrate binding sites and catalytic mechanisms.

Publication types

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

MeSH terms

  • 4-Aminobutyrate Transaminase / antagonists & inhibitors*
  • 4-Aminobutyrate Transaminase / chemistry
  • 4-Aminobutyrate Transaminase / metabolism
  • Aspartate Aminotransferases / antagonists & inhibitors*
  • Aspartate Aminotransferases / chemistry
  • Aspartate Aminotransferases / genetics
  • Aspartate Aminotransferases / metabolism
  • Binding Sites
  • Catalytic Domain
  • Crystallography, X-Ray
  • Cycloleucine / analogs & derivatives*
  • Cycloleucine / chemistry
  • Cycloleucine / metabolism
  • Cycloleucine / pharmacology
  • Databases, Chemical
  • Databases, Protein
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / metabolism
  • Enzyme Inhibitors / pharmacology*
  • Escherichia coli Proteins / antagonists & inhibitors
  • Escherichia coli Proteins / chemistry
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Humans
  • Ligands
  • Models, Molecular*
  • Molecular Conformation
  • Ornithine-Oxo-Acid Transaminase / antagonists & inhibitors*
  • Ornithine-Oxo-Acid Transaminase / chemistry
  • Ornithine-Oxo-Acid Transaminase / genetics
  • Ornithine-Oxo-Acid Transaminase / metabolism
  • Protein Conformation
  • Pyridoxal Phosphate / chemistry
  • Pyridoxal Phosphate / metabolism*
  • Pyridoxamine / chemistry
  • Pyridoxamine / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Structural Homology, Protein
  • Substrate Specificity

Substances

  • 3-amino-4-fluorocyclopentane-1-carboxylic acid
  • Enzyme Inhibitors
  • Escherichia coli Proteins
  • Ligands
  • Recombinant Proteins
  • Cycloleucine
  • Pyridoxal Phosphate
  • Pyridoxamine
  • Aspartate Aminotransferases
  • Ornithine-Oxo-Acid Transaminase
  • 4-Aminobutyrate Transaminase