Importance of a hypervariable active-site residue in human Mu class glutathione transferases catalyzing the bioactivation of chemotherapeutic thiopurine prodrugs

Biochim Biophys Acta. 2007 Aug;1770(8):1098-103. doi: 10.1016/j.bbagen.2007.04.001. Epub 2007 Apr 10.

Abstract

Glutathione transferases (GSTs) catalyze the bioactivation of the thiopurine prodrugs azathioprine, cis-6-(2-acetylvinylthio)purine (cAVTP) and trans-6-(2-acetylvinylthio)guanine (tAVTG), thereby releasing the antimetabolites 6-mercaptopurine and 6-thioguanine. In the GST Mu class, GST M1-1 has the highest catalytic efficiency, whereas GST M2-2 and other enzymes are less active. In the evolution of Mu class GSTs, residue 210 appears hypervariable and has particular functional significance. We demonstrate that the catalytic activity of GST M1-1 with cAVTP or tAVTG is successively diminished when wild-type Ser-210 is mutated into Ala followed by Thr. Conversely, mutating wild-type Thr-210 in GST M2-2 into Ala and Ser enhanced the corresponding activities. Comparisons were also made with GST M2-2 distinguished by Gly or Pro in position 210, as well as wild-type GSTs M4-4 and M5-5. The results suggest that the hydroxyl group of Ser in position 210 stabilizes the transition state of the GST-catalyzed reaction. The low activity of GSTs containing Thr in position 210 is probably due to steric hindrance caused by the beta-methyl group of the side chain. The ratios of the different catalytic efficiencies were translated into differences in the Gibbs free energies of transition state stabilization. The effects of the mutations were qualitatively parallel for the alternative substrates, but vary significantly in magnitude. From the evolutionary perspective the data show that a point mutation can alternatively enhance or attenuate the activity with a particular substrate and illustrate the functional plasticity of GSTs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Antimetabolites, Antineoplastic / metabolism
  • Binding Sites
  • Catalysis
  • Glutathione Transferase / genetics
  • Glutathione Transferase / metabolism*
  • Humans
  • Kinetics
  • Mercaptopurine / metabolism
  • Molecular Structure
  • Prodrugs / chemistry
  • Prodrugs / metabolism*
  • Serine / chemistry
  • Serine / metabolism
  • Spectrophotometry, Ultraviolet
  • Substrate Specificity

Substances

  • Antimetabolites, Antineoplastic
  • Prodrugs
  • Serine
  • Mercaptopurine
  • Glutathione Transferase