Bioactivation of fluorinated 2-aryl-benzothiazole antitumor molecules by human cytochrome P450s 1A1 and 2W1 and deactivation by cytochrome P450 2S1

Chem Res Toxicol. 2012 Aug 20;25(8):1740-51. doi: 10.1021/tx3001994. Epub 2012 Jul 10.

Abstract

Both 2-(4-amino-3-methylphenyl)-5-fluorobenzothiazole (5F 203) and 5-fluoro-2-(3,4-dimethoxyphenyl)-benzothiazole (GW 610) contain the benzothiazole pharmacophore and possess potent and selective in vitro antitumor properties. Prior studies suggested the involvement of cytochrome P450 (P450) 1A1 and 2W1-mediated bioactivation in the antitumor activities and P450 2S1-mediated deactivation of 5F 203 and GW 610. In the present study, the biotransformation pathways of 5F 203 and GW 610 by P450s 1A1, 2W1, and 2S1 were investigated, and the catalytic parameters of P450 1A1- and 2W1-catalyzed oxidation were determined in steady-state kinetic studies. The oxidations of 5F 203 catalyzed by P450s 1A1 and 2W1 yielded different products, and the formation of a hydroxylamine was observed for the first time in the latter process. Liquid chromatography-mass spectrometry (LC-MS) analysis with the synthetic hydroxylamine and also a P450 2W1/5F 203 incubation mixture indicated the formation of dGuo adduct via a putative nitrenium intermediate. P450 2W1-catalyzed oxidation of GW 610 was 5-fold more efficient than the P450 1A1-catalyzed reaction. GW 610 underwent a two-step oxidation process catalyzed by P450 1A1 or 2W1: a regiospecific O-demethylation and a further hydroxylation. Glutathione (GSH) conjugates of 5F 203 and GW 610, presumably through a quninoneimine and a 1,2-quinone intermediate, respectively, were detected. These results demonstrate that human P450s 1A1 and 2W1 mediate 5F 203 and GW 610 bioactivation to reactive intermediates and lead to GSH conjugates and a dGuo adduct, which may account for the antitumor activities of 5F 203 and GW 610 and also be involved in cell toxicity. P450 2S1 can catalyze the reduction of the hydroxylamine to the amine 5F 203 under anaerobic conditions and, to a lesser extent, under aerobic conditions, thus attenuating the anticancer activity.

Publication types

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

MeSH terms

  • Antineoplastic Agents / chemical synthesis
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / metabolism*
  • Benzothiazoles / chemical synthesis
  • Benzothiazoles / chemistry
  • Benzothiazoles / metabolism*
  • Biocatalysis
  • Chromatography, High Pressure Liquid
  • Cytochrome P-450 CYP1A1 / metabolism*
  • Cytochrome P-450 Enzyme System / metabolism*
  • Cytochrome P450 Family 2
  • DNA Adducts / chemistry
  • Humans
  • Kinetics
  • Microsomes, Liver / metabolism
  • Oxidation-Reduction
  • Spectrometry, Mass, Electrospray Ionization
  • Thiazoles / chemical synthesis
  • Thiazoles / chemistry
  • Thiazoles / metabolism*

Substances

  • 2-(3,4-dimethoxyphenyl)-5-fluorobenzothiazole
  • 2-(4-amino-3-methylphenyl)-5-fluorobenzothiazole
  • Antineoplastic Agents
  • Benzothiazoles
  • DNA Adducts
  • Thiazoles
  • Cytochrome P-450 Enzyme System
  • CYP2S1 protein, human
  • CYP2W1 protein, human
  • Cytochrome P-450 CYP1A1
  • Cytochrome P450 Family 2