Prominent Stereoselectivity of NNAL Glucuronidation in Upper Aerodigestive Tract Tissues

Chem Res Toxicol. 2019 Aug 19;32(8):1689-1698. doi: 10.1021/acs.chemrestox.9b00217. Epub 2019 Jul 30.

Abstract

Tobacco specific nitrosamines (TSNAs) are among the most potent carcinogens found in cigarettes and smokeless tobacco products. Decreases in TSNA detoxification, particularly 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK), have been associated with tobacco-related cancer incidence. NNK is metabolized by carbonyl reduction to its major carcinogenic metabolite, 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL), which is detoxified by glucuronidation at the nitrogen within the pyridine ring or at the chiral alcohol to form four glucuronide products: (R)-NNAL-O-Gluc, (S)-NNAL-O-Gluc, (R)-NNAL-N-Gluc, (S)-NNAL-N-Gluc. Stereoselective NNAL-Gluc formation and the relative expression of NNAL-glucuronidating UGTs (1A4, 1A9, 1A10, 2B7, 2B10, 2B17) were analyzed in 39 tissue specimens from the upper aerodigestive tract (esophagus (n = 13), floor of mouth (n = 4), larynx (n = 9), tongue (n = 7), and tonsil (n = 6)). All pooled tissue types preferentially formed (R)-NNAL-O-Gluc in the presence of racemic-NNAL; only esophagus exhibited any detectable formation of (S)-NNAL-O-Gluc. For every tissue type examined, UGT1A10 exhibited the highest relative expression levels among the NNAL-O-glucuronidating UGTs, ranging from 36% (tonsil) to 49% (esophagus), followed by UGT1A9 > UGT2B7 > UGT2B17. UGT1A10 also exhibited similar or higher levels of expression as compared to both NNAL-N-glucuronidating UGTs, 1A4 and 2B10. In a screening of cells expressing individual UGT enzymes, all NNAL glucuronidating UGTs exhibited some level of stereospecific preference for individual NNAL enantiomers, with UGTs 1A10 and 2B17 forming primarily (R)-NNAL-O-Gluc. These data suggest that UGTs 1A10 and 2B17 may be important enzymes in the detoxification of TSNAs like NNK in tissues of the upper aerodigestive tract.

Publication types

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

MeSH terms

  • Digestive System / chemistry
  • Digestive System / metabolism*
  • Glucuronides / chemistry
  • Glucuronides / metabolism*
  • Glucuronosyltransferase / metabolism
  • HEK293 Cells
  • Humans
  • Kinetics
  • Molecular Structure
  • Nitrosamines / chemistry
  • Nitrosamines / metabolism*
  • Stereoisomerism

Substances

  • Glucuronides
  • Nitrosamines
  • Glucuronosyltransferase
  • 4-(methylnitrosamino)-1-(3-pyridyl)-1-butan-1-ol