Metabolism of the food-associated carcinogen 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine by human intestinal microbiota

Journal of Agricultural and Food Chemistry

Volumn 54, Issue 9, 2006, Pages 3454-3461

  Vanhaecke, Lynn ^a   Van Hoof, Nathalie ^a   Van Brabandt, Willem ^a   Soenen, Bram ^a   Heyerick, Arne ^a   De Kimpe, Norbert ^a   De Keukeleire, Denis ^a   De Verstraete, Willy ^a   Van De Wiele, Tom ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Cooking; Heterocyclic amine; HPLC; Intestinal bacteria; LC MS; Meat; NMR

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO(4,5 B)PYRIDINE; 2-AMINO-1-METHYL-6-PHENYLIMIDAZO(4,5-B)PYRIDINE; CARCINOGEN; IMIDAZOLE DERIVATIVE;

ADULT; ARTICLE; BACTERIUM; DIET; FECES; FEMALE; FOOD; HUMAN; INTESTINE; MALE; METABOLISM; MICROBIOLOGY;

ADULT; BACTERIA; CARCINOGENS; DIET; FECES; FEMALE; FOOD; HUMANS; IMIDAZOLES; INTESTINES; MALE;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 33744463436     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf053170+     Document Type: Article

References (48)

1. Nagao, M.; Honda, M.; Seino, Y.; Yahagi, T.; Sugimura, T. Mutagenicities of smoke condensates and charred surface of fish and meat. Cancer Lett. 1977, 2, 221-226.
2. Sinha, R.; Rothman, N.; Brown, E. D.; Salmon, C. P.; Knize, M. G.; Swanson, C. A.; Rossi, S. C.; Mark, S. D.; Levander, O. A.; Felton, J. S. High concentrations of the carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) occur in chicken but are dependent on the cooking method. Cancer Res. 1995, 55, 4516-4519.
3. Murray, S.; Lynch, A. M.; Knize, M. G.; Gooderham, N. J. Quantification of the carcinogens 2-amino-3,8-dimethyl-imidazo-[4,5-f]quinoxaline and 2-amino-3,4,8-trimethylimidazo[4,5-f]-quinoxaline and 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine in food using a combined assay based on gas chromatography-negative ion mass-spectrometry. J. Chromatogr. B 1993, 616, 211-219.
4. Zimmerli, B.; Rhyn, P.; Zoller, O.; Schlatter J. Occurrence of heterocyclic aromatic amines in the Swiss diet: Analytical method, exposure estimation and risk assessment. Food Addit. Contam. 2001, 18, 533-551.
5. Busquets, R.; Bordas, M.; Torbino, F.; Puignou, L.. Galceran, M. T. Occurrence of heterocyclic amines in several home-cooked meat dishes of the Spanish diet. J. Chromatogr. B. 2003, 802, 79-86.
6. Wong, K. Y.; Su, J.; Knize, M. G.; Koh, W. P.; Seow, A. Dietary exposure to heterocyclic amines in a Chinese population. Nutr. Cancer 2005, 52, 147-155.
7. Skog, K.; Augustsson, K.; Steineck, G.; Stenberg, M.; Jagerstad, M. Polar and non-polar heterocyclic amines in cooked fish and meat products and their corresponding pan residues. Food Chem. Toxicol. 1997, 35, 555-565.
8. Felton, J. S.; Knize, M. G.; Shen, N. H.; Lewis, P. R.; Andresen, B. D.; Happe, J.; Hatch, F. T. The isolation and identification of a new mutagen from fried ground-beef 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 1986, 7, 1081-1086.
9. Norrish, A. E.; Ferguson, L. R.; Knize, M. G.; Felton, J. S.; Sharpe, S. J.; Jackson, R. T. Heterocyclic amine content of cooked meat and risk of prostate cancer. J. Natl. Cancer Inst. 1999, 91, 2038-2044.
10. Ito, N.; Hasegawa, R.; Sano, M.; Tamano, S.; Esumi, H.; Takayama, S.; Sugimura, T. A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimidazo-[4,5-b]pyridine (PhIP). Carcinogenesis 1991, 12, 1503-1506.
11. Knize, M. G.; Felton, J. S. Formation and human risk of carcinogenic heterocyclic amines from natural precursors in meat. Nutr. Rev. 2005, 63, 158-165.
12. Shirai, T.; Sano, M.; Tamano, S.; Takahashi, S.; Hirose, M.; Futakuchi, M.; Hasegawa, R.; Imaida, K.; Matsumoto, K.; Wakabayashi, K.; Sugimura, T.; Ito, N. The prostate: A target for carcinogenicity of 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine (PhIP) derived from cooked foods. Cancer Res. 1997, 57, 195-198.
13. Snyderwine, E. G. Mammary gland carcinogenesis by food-derived heterocyclic amines: Metabolism and additional factors influencing carcinogenesis by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Environ. Mol. Mutagen. 2002, 39, 165-170.
14. Ito, N.; Hasegawa, R.; Imaida, K.; Tamano, S.; Hagiwara, A.; Hirose, M.; Shirai, T. Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in the rat. Mutat. Res.-Fundam. Mol. Mech. Mutagen. 1997, 376, 107-114.
15. Aeschbacher, H. U.; Turesky, R. J. Mammalian-cell mutagenicity and metabolism of heterocyclic aromatic amines. Mutat. Res. 1991, 259, 235-250.
16. Knasmuller, S.; Steinkellner, H.; Hirschl, A. M.; Rabot, S.; Nobis, E. C.; Kassie, F. Impact of bacteria in dairy products and of the intestinal microflora on the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Mutat. Res.-Fundam. Mol. Mech. Mutagen. 2001, 480, 129-138.
17. Kulp, K. S.; Knize, M. G.; Fowler, N. D.; Salmon, C. P.; Felton, J. S. PhIP metabolites in human urine after consumption of well-cooked chicken. J. Chromatogr. B 2004, 802, 143-153.
18. Malfatti, M. A.; Kulp, K. S.; Knize, M. G.; Davis, C.; Massengill, J. P.; Williams, S.; Nowell, S.; MacLeod, S.; Dingley, K. H.; Turteltaub, K. W.; Lang, N. P.; Felton, J. S. The identification of 2-C-14 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine metabolites in humans. Carcinogenesis 1999, 20, 705-713.
19. Bolognani, F.; Rumney, C. J.; Pool-Zobel, B. L.; Rowland, I. R. Effect of lactobacilli, bifidobacteria and inulin on the formation of aberrant crypt foci in rats. Eur. J. Nutr. 2001, 40, 293-300.
20. Turbic, A.; Ahokas, J. T.; Haskard, C. A. Selective in vitro binding of dietary mutagens, individually or in combination, by lactic acid bacteria. Food Addit. Contam. 2002, 19, 144-152.
21. Hirayama, K.; Baranczewski, P.; Akerlund, J. E.; Midtvedt, T.; Moller, L.; Rafter, J. Effects of human intestinal flora on mutagenicity of and DNA adduct formation from food and environmental mutagens. Carcinogenesis 2000, 21, 2105-2111.
22. Kassie, F.; Rabot, S.; Kundi, M.; Chabicovsky, M.; Qin, H. M.; Knasmuller, S. Intestinal microflora play a crucial role in the genotoxicity of the cooked food mutagen 2-amino-3-methylimidazo[4,5-f]quinoline (IQ). Carcinogenesis 2001, 22, 1721-1725.
23. Rumney, C. J.; Rowland, I. R. In vivo and in vitro models of the human colonic flora. Crit. Rev. Food Sci. 1992, 31, 299-331.
24. Bashir, M.; Kingston, D. G. I.; Carman, R. J.; Vantassell, R. L.; Wilkins, T. D. Anaerobic metabolism of 2-amino-3-methyl-3H-imidazo[4,5-f] quinoline (IQ) by human faecal flora. Mutat. Res. 1987, 190, 187-190.
25. Carman, R. J.; Vantassell, R. L.; Kingston, D. G. I.; Bashir, M.; Wilkins, T. D. Conversion of IQ, a dietary pyrolysis carcinogen to a direct-acting mutagen by normal intestinal bacteria of humans. Mutat. Res. 1988, 206, 335-342.
26. Bashir, M.; Kingston, D. G. I.; Vantassell, R. L.; Wilkins, T. D. Synthesis and biological evaluation of methylated derivatives of the cooked food mutagen metabolite 2-amino-3,6-dihydro-3-methyl-7H-imidazo[4,5-f]quinolin-7-one (7-OH-IQ). Heterocycles 1989, 29, 1915-1922.
27. Humblot, C.; Combourieu, B.; Vaisanen, M. L.; Furet, J. P.; Delort, A. M.; Rabot, S. 1H- nuclear magnetic resonance spectroscopy-based studies of the metabolism of food-borne carcinogen 2-amino-3-methyl-imidazo[4,5-f]quinoline (IQ) by human intestinal microbiota. Appl. Environ. Microbiol. 2005, 71, 5116-5123.
28. Suau, A.; Bonnet, R.; Sutren, M.; Godon, J. J.; Gibson, G. R.; Collins, M. D.; Dore, J. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 1999, 65, 4799-4807.
29. Jonas, C. R.; Estívariz, C. F.; JoneS, D. P.; Gu, L. H.; Wallace, T. M.; Diaz, E. E.; Pascal, R. R.; Cotsonis, G. A.; Ziegler, T. R. Keratinocyte growth factor enhances glutathione redox state in rat intestinal mucosa during nutritional repletion. J. Nutr. 1999, 129, 1278-1284.
30. Collins, C. J.; Bupp, J. E.; Tanga, M. J. Synthesis of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), a heterocyclic food mutagen. Arkivoc 2002, 90-96.
31. Crofts, F. G.; Strickland, P. T.; Hayes, C. L.; Sutter, T. R. Metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) by human cytochrome P4501B1. Carcinogenesis 1997, 18, 1793-1798.
32. Turesky, R. J.; Guengerich, F. P.; Guillouzo, A.; Langouet, S. Metabolism of heterocyclic aromatic amines by human hepatocytes and cytochrome P4501A2. Mutat. Res.-Fundam. Mol. Mech. Mutagen. 2002, 506, 187-195.
33. Crofts, F. G.; Sutter, T. R.; Strickland, P. T. Metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by human cytochrome P4501A1, P4501A2 and P4501B1. Carcinogenesis 1998, 19, 1969-1973.
34. Ilett, K. F.; Tee, L. B. G.; Reeves, P. T.; Minchin, R. F. Metabolism of drugs and other xenobiotics in the gut lumen and wall. Pharmacol. Ther. 1990, 46, 67-93.
35. Rowland, I. R.; Grasso, P. Degradation of N-nitrosamines by intestinal bacteria. Appl. Microbiol. 1975, 29, 7-12.
36. Oatley, J. T.; Rarick, M. D.; Ji, G. E.; Linz, J. E. Binding of aflatoxin B-1 to bifidobacteria in vitro. J. Food Prot. 2000, 63, 1133-1136.
37. Van de Wiele, T.; Vanhaecke, L.; Boeckaert, C.; Peru, K.; Headley, J.; Verstraete, W.; Siciliano, S. Human colon microbiota transform polycyclic aromatic hydrocarbons to estrogenic metabolites. Environ. Health Perspect. 2005, 113, 6-10.
38. Wang, R. F.; Chen, H. H.; Paine, D. D.; Cerniglia, C. E. Microarray method to monitor 40 intestinal bacterial species in the study of azo dye reduction. Biosens. Bioelectron. 2004, 20, 699-705,
39. Ristic, A.; Cichna, A.; Sontag, G. Determination of less polar heterocyclic aromatic amines in standardised beef extracts and cooked meat consumed in Austria by liquid chromatography and fluorescence detection. J. Chromatogr. B 2004, 802, 87-94.
40. Pais, P.; Knize, M. G. Chromatographic and related techniques for the determination of aromatic heterocyclic amines in foods. J. Chromatogr. B 2000, 747, 139-169.
41. Vantassell, R. L.; Kingston, D. G. I.; Wilkins, T. D. Metabolism of dietary genotoxins by the human colonic microflora - The fecapentaenes and heterocyclic amines. Mutat. Res. 1990, 238, 209-221.
42. Bolognani, F.; Rumney, C. J.; Rowland, I. R. Influence of carcinogen binding by lactic acid-producing bacteria on tissue distribution and in vivo mutagenicity of dietary carcinogens. Food Chem. Toxicol. 1997, 35, 535-545.
43. Ungell, A. L.; Nylander, S.; Bergstrand, S.; Sjoberg, A.; Lennernas, H. Membrane transport of drugs in different regions of the intestinal tract of the rat. J. Pharm. Sci. 1998, 87, 360-366.
44. van der Bijl, P.; van Eyk, A. D. Comparative in vitro permeability of human vaginal, small intestinal and colonic mucosa. Int. J. Pharm. 2003, 261, 147-152.
45. Decroos, K.; Vanhemmens, S.; Cattoir, S.; Boon, N.; Verstraete, W. Isolation and characterisation of an equol-producing mixed microbial culture from a human faecal sample and its activity under gastrointestinal conditions. Arch. Microbiol. 2005, 183, 45-55.
46. Wang, X. L.; Hur, H. G.; Lee, J. H.; Kim, K. T.; Kim, S. I. Enantioselective synthesis of S-equol from dihydrodaidzein by a newly isolated anaerobic human intestinal bacterium. Appl. Environ. Microbiol. 2005, 71, 214-219.
47. Rowland, I. R.; Wiseman, H.; Sanders, T. A. B.; Adlercreutz, H.; Bowey, E. A. Interindividual variation in metabolism of soy isoflavones and lignans: Influence of habitual diet on equol production by the gut microflora. Nutr. Cancer 2000, 36, 27-32.
48. Possemiers, S.; Heyerick, A.; Robbens, V.; De Keukeleire, D.; Verstraete, W. Activation of proestrogens from hops (Humulus lupulus L.) by intestinal microbiota; Conversion of isoxantho-humol into 8-prenylnaringenin. J. Agric. Food Chem. 2005, 53, 6281-6288.