Mass Spectrometric Characterization of Human Serum Albumin Adducts Formed with N-Oxidized Metabolites of 2-Amino-1-methylphenylimidazo[4,5-b]pyridine in Human Plasma and Hepatocytes

Chem Res Toxicol. 2015 May 18;28(5):1045-59. doi: 10.1021/acs.chemrestox.5b00075. Epub 2015 Apr 10.

Abstract

2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), a carcinogenic heterocyclic aromatic amine formed in cooked meats, is metabolically activated to electrophilic intermediates that form covalent adducts with DNA and protein. We previously identified an adduct of PhIP formed at the Cys(34) residue of human serum albumin following reaction of albumin with the genotoxic metabolite 2-hydroxyamino-1-methyl-6-phenylimidazo[4,5-b]pyridine (HONH-PhIP). The major adducted peptide recovered from a tryptic/chymotryptic digest was identified as the missed-cleavage peptide LQQC*([SO2PhIP])PFEDHVK, a [cysteine-S-yl-PhIP]-S-dioxide linked adduct. In this investigation, we have characterized the albumin adduction products of N-sulfooxy-2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (N-sulfooxy-PhIP), which is thought to be a major genotoxic metabolite of PhIP formed in vivo. Targeted and data-dependent scanning methods showed that N-sulfooxy-PhIP adducted to the Cys(34) of albumin in human plasma to form LQQC*([SO2PhIP])PFEDHVK at levels that were 8-10-fold greater than the adduct levels formed with N-(acetyloxy)-2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (N-acetoxy-PhIP) or HONH-PhIP. We also discovered that N-sulfooxy-PhIP forms an adduct at the sole tryptophan (Trp(214)) residue of albumin in the sequence AW*([PhIP])AVAR. However, stable adducts of PhIP with albumin were not detected in human hepatocytes. Instead, PhIP and 2-amino-1-methyl-6-(5-hydroxy)phenylimidazo[4,5-b]pyridine (5-HO-PhIP), a solvolysis product of the proposed nitrenium ion of PhIP, were recovered during the proteolysis, suggesting a labile sulfenamide linkage had formed between an N-oxidized intermediate of PhIP and Cys(34) of albumin. A stable adduct was formed at the Tyr(411) residue of albumin in hepatocytes and identified as a deaminated product of PhIP, Y(*[desaminoPhIP])TK, where the 4-HO-tyrosine group bound to the C-2 imidazole atom of PhIP.

Publication types

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

MeSH terms

  • Carcinogens / analysis
  • Carcinogens / metabolism*
  • Chromatography, High Pressure Liquid
  • Cooking
  • DNA Adducts / chemistry
  • DNA Adducts / metabolism*
  • Hepatocytes / chemistry
  • Hepatocytes / drug effects*
  • Hepatocytes / metabolism
  • Humans
  • Imidazoles / analysis
  • Imidazoles / metabolism*
  • Models, Molecular
  • Oxidation-Reduction
  • Serum Albumin / chemistry
  • Serum Albumin / metabolism*
  • Spectrometry, Mass, Electrospray Ionization

Substances

  • Carcinogens
  • DNA Adducts
  • Imidazoles
  • Serum Albumin
  • 2-amino-1-methyl-6-phenylimidazo(4,5-b)pyridine