Human UDP-glucuronosyltransferase 1A1 is the primary enzyme responsible for the N-glucuronidation of N-hydroxy-PhIP in vitro

Chem Res Toxicol. 2004 Aug;17(8):1137-44. doi: 10.1021/tx049898m.

Abstract

UDP-glucuronosyltransferase 1A proteins (UGT1A) catalyze the glucuronidation of many endogenous and xenobiotic compounds including heterocyclic amines and their hydroxylated metabolites. Studies have shown that in humans UGT1A-mediated glucuronidation is an important pathway in the detoxification of food-borne carcinogenic heterocyclic amines. The biotransformation of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), the most mass abundant heterocyclic amine found in cooked meats, is highly dependent on cytochrome P4501A2 hydroxylation followed by UGT-catalyzed glucuronidation of the N-hydroxy-PhIP reactive intermediate. To determine which UGT1A proteins are involved in the glucuronidation of N-hydroxy-PhIP, microsomal preparations from baculovirus-infected insect cells that express all of the known functional human UGT1A isozymes (UGT1A1, -1A3, -1A4, -1A6, -1A7, -1A8, -1A9, and -1A10) were exposed to N-hydroxy-PhIP and the reaction products were isolated by HPLC. All UGT1A proteins except UGT1A6 showed some degree of activity toward N-hydroxy-PhIP. The formation of both N-hydroxy-PhIP-N(2)-glucuronide and N-hydroxy-PhIP-N3-glucuronide was both time- and substrate concentration-dependent. UGT1A1 was the most efficient in converting N-hydroxy-PhIP to both conjugates producing five times more of the N(2)-conjugate than UGT1A4, the next most active UGT, and 286 times more than UGT1A7, the least active UGT. With an apparent K(m) of 52 microM and a K(cat) of 114 min(-)(1), UGT1A1 was also the most catalytically efficient in forming N-hydroxy-PhIP-N(2)-glucuronide. The catalytic efficiency for N-hydroxy-PhIP-N3-glucuronide formation was 8, 10, and 6 times lower for UGT1A1, -1A4, and -1A8, respectively, when compared to the K(cat) values for N-hydroxy-PhIP-N(2)-glucuronide formation. These results clearly show that UGT1A1 has the highest specificity for glucuronidating N-hydroxy-PhIP. Polymorphic expression resulting in decreased UGT1A1 activity in humans can cause reduced rates of glucuronidation, which can change the metabolic ratio between bioactivation and detoxification to favor bioactivation. This change will increase the susceptibility to the deleterious effects from PhIP exposure because the capacity to form nontoxic N-hydroxy-PhIP glucuronide conjugates will be diminished.

Publication types

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

MeSH terms

  • Biotransformation
  • Carcinogens / toxicity
  • Glucuronides / metabolism*
  • Glucuronosyltransferase / metabolism*
  • Humans
  • Hydrogen-Ion Concentration
  • Imidazoles / metabolism*
  • Imidazoles / toxicity
  • Kinetics
  • Microsomes / enzymology
  • Pyridines / metabolism*
  • Pyridines / toxicity
  • Time Factors

Substances

  • Carcinogens
  • Glucuronides
  • Imidazoles
  • Pyridines
  • 2-hydroxyamino-1-methyl-6-phenylimidazo(4,5-b)pyridine
  • UGT1A1 enzyme
  • Glucuronosyltransferase