The interaction of the chemotherapeutic drug chlorambucil with human glutathione transferase A1-1: kinetic and structural analysis

PLoS One. 2013;8(2):e56337. doi: 10.1371/journal.pone.0056337. Epub 2013 Feb 27.

Abstract

Glutathione transferases (GSTs) are enzymes that contribute to cellular detoxification by catalysing the nucleophilic attack of glutathione (GSH) on the electrophilic centre of a number of xenobiotic compounds, including several chemotherapeutic drugs. In the present work we investigated the interaction of the chemotherapeutic drug chlorambucil (CBL) with human GSTA1-1 (hGSTA1-1) using kinetic analysis, protein crystallography and molecular dynamics. In the presence of GSH, CBL behaves as an efficient substrate for hGSTA1-1. The rate-limiting step of the catalytic reaction between CBL and GSH is viscosity-dependent and kinetic data suggest that product release is rate-limiting. The crystal structure of the hGSTA1-1/CBL-GSH complex was solved at 2.1 Å resolution by molecular replacement. CBL is bound at the H-site attached to the thiol group of GSH, is partially ordered and exposed to the solvent, making specific interactions with the enzyme. Molecular dynamics simulations based on the crystal structure indicated high mobility of the CBL moiety and stabilization of the C-terminal helix due to the presence of the adduct. In the absence of GSH, CBL is shown to be an alkylating irreversible inhibitor for hGSTA1-1. Inactivation of the enzyme by CBL followed a biphasic pseudo-first-order saturation kinetics with approximately 1 mol of CBL per mol of dimeric enzyme being incorporated. Structural analysis suggested that the modifying residue is Cys112 which is located at the entrance of the H-site. The results are indicative of a structural communication between the subunits on the basis of mutually exclusive modification of Cys112, indicating that the two enzyme active sites are presumably coordinated.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biocatalysis / drug effects
  • Chlorambucil / chemistry*
  • Chlorambucil / metabolism*
  • Crystallography, X-Ray
  • Glutathione / pharmacology
  • Glutathione Transferase / chemistry*
  • Glutathione Transferase / metabolism*
  • Humans
  • Hydrogen-Ion Concentration
  • Kinetics
  • Molecular Dynamics Simulation
  • Protein Binding / drug effects
  • Protein Subunits / chemistry
  • Protein Subunits / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Time Factors

Substances

  • Protein Subunits
  • Recombinant Proteins
  • Chlorambucil
  • GSTA1 protein, human
  • Glutathione Transferase
  • Glutathione

Grants and funding

This research has been co-financed by the European Union (European Social Fund – ESF) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) - Research Funding Program: Heracleitus II. The work was also supported by the action THALES: ‘Glutathione transferases: multifunctional molecular tools in red and green biotechnology’, falling under the Operational Programme “Education and Lifelong Learning” and is co-financed by the European Social Fund and National Resources. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.