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Polycyclic aromatic hydrocarbons (PAHs) are metabolized to trans-dihydrodiol proximate carcinogens by human epoxide hydrolase (EH) and CYP1A1. Human dihydrodiol dehydrogenase isoforms (AKR1C1−AKR1C4), members of the aldo−keto reductase (AKR) superfamily, activate trans-dihydrodiols by converting them to reactive and redox-active o-quinones.

We now show that the constitutively and widely expressed human AKR, aldehyde reductase (AKR1A1), will oxidize potent proximate carcinogen trans-dihydrodiols to their corresponding o-quinones. CDNA encoding AKR1A1 was isolated from HepG2 cells, overexpressed in Escherichia coli, purified to homogeneity, and characterized. AKR1A1 oxidized the potent proximate carcinogen (±)- trans-7,8-dihydroxy-7,8-dihydrobenzo[ a]pyrene with a higher utilization ratio ( V max/ K m) than any other human AKR.

AKR1A1 also displayed a high V max/ K m for the oxidation of 5-methylchrysene-7,8-diol, benz[ a]anthracene-3,4-diol, 7-methylbenz[ a]anthracene-3,4-diol, and 7,12-dimethylbenz[ a]anthracene-3,4-diol. AKR1A1 displayed rigid regioselectivity by preferentially oxidizing non-K-region trans-dihydrodiols.

The enzyme was stereoselective and oxidized 50% of each racemic PAH trans-dihydrodiol tested. The absolute stereochemistries of the reactions were assigned by circular dichroism spectrometry. AKR1A1 preferentially oxidized the metabolically relevant (−)-benzo[ a]pyrene-7( R),8( R) -dihydrodiol. AKR1A1 also preferred (−)-benz[ a]anthracene-3( R),4( R)-dihydrodiol, (+)-7-methylbenz[ a]anthracene-3( S),4( S)-dihydrodiol, and (−)-7,12-dimethylbenz[ a]anthracene-3( R),4( R)-dihydrodiol.

The product of the AKR1A1-catalyzed oxidation of (±)- trans-7,8-dihydroxy-7,8-dihydrobenzo[ a]pyrene was trapped with 2-mercaptoethanol and characterized as a thioether conjugate of benzo[ a]pyrene-7,8-dione by LC/MS. Multiple human tissue expression array analysis showed coexpression of AKR1A1, CYP1A1, and EH, indicating that trans-dihydrodiol substrates are formed in the same tissues in which AKR1A1 is expressed. The ability of this general metabolic enzyme to divert trans-dihydrodiols to o-quinones suggests that this pathway of PAH activation may be widespread in human tissues.

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