Formation and biochemistry of carcinogenic heterocyclic aromatic amines in cooked meats

Toxicology Letters

Volumn 168, Issue 3, 2007, Pages 219-227

  Turesky, Robert J ^a  

^a WADSWORTH CENTER   (United States)

Author keywords

Biomarkers; Dietary carcinogens; Heterocyclic Aromatic amines; Metabolism

Indexed keywords

AROMATIC AMINE; BIOLOGICAL MARKER; HETEROCYCLIC COMPOUND;

ARTICLE; BODY FLUID; BREAST CANCER; CANCER RISK; CARCINOGENICITY; COLON CANCER; COOKING; DANGEROUS GOODS; DNA ADDUCT; EXHAUST GAS; FISH; GENOTOXICITY; HUMAN; MASS SPECTROMETRY; MEAT; NONHUMAN; POULTRY; PRIORITY JOURNAL; PROSTATE CANCER; RISK FACTOR; RODENT; SENSITIVITY AND SPECIFICITY; TOBACCO;

AMINES; ANIMALS; BIOLOGICAL MARKERS; CARCINOGENS; COOKERY; CYTOCHROME P-450 ENZYME SYSTEM; DNA ADDUCTS; ENVIRONMENTAL MONITORING; HETEROCYCLIC COMPOUNDS; HUMANS; MEAT; MUTAGENS; NEOPLASMS; SPECIES SPECIFICITY;

NICOTIANA TABACUM; RODENTIA;

EID: 33846211072     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2006.10.018     Document Type: Article

References (50)

1. Alexander J., Heidenreich B., Reistad R., and Holme J.A. Metabolism of the food carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in the rat and other rodents. In: Adamson R.H., Gustafsson J.-A., Ito N., Nagao M., Sugimura T., Wakabayashi K., and Yamazoe Y. (Eds). Proceedings of the 23rd Princess Takamatusu Cancer Society on Heterocyclic amines in cooked foods: Possible human carcinogens (1995), Princeton Scientific Publishing Co., Inc, New Jersey 59-68
2. Alexander J., Reistad R., Hegstad S., Frandsen H., Ingebrigtsen K., Paulsen J.E., and Becher G. Biomarkers of exposure to heterocyclic amines: approaches to improve the exposure assessment. Food Chem. Toxicol. 40 (2002) 1131-1137
3. Barrett J.H., Smith G., Waxman R., Gooderham N., Lightfoot T., Garner R.C., Augustsson K., Wolf C.R., Bishop D.T., and Forman D. Investigation of interaction between N-acetyltransferase 2 and heterocyclic amines as potential risk factors for colorectal cancer. Carcinogenesis 24 (2003) 275-282
4. Crofts F.G., Sutter T.R., and Strickland P.T. Metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by human cytochrome P4501A1, P4501A2 and P4501B1. Carcinogenesis 19 (1998) 1969-1973
5. Cross A.J., and Sinha R. Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ. Mol. Mutagen. 44 (2004) 44-55
6. Dai Q., Shu X.O., Jin F., Gao Y.T., Ruan Z.X., and Zheng W. Consumption of animal foods, cooking methods, and risk of breast cancer. Cancer Epidemiol. Biomarkers Prev. 11 (2002) 801-808
7. Davies D.S., Gooderham N., Murray S., Lynch A.M., de la Torre R., Segura J., and Boobis A.R. Systemic exposure to dietary heterocyclic amines in man. In: Adamson R.H., Gustafsson J.-A., Ito N., Nagao M., Sugimura T., Wakabayashi K., and Yamazoe Y. (Eds). Proceedings of the 23rd Princess Takamatusu Cancer Society on Heterocyclic Amines in Cooked Foods: Possible Human Carcinogens (1995), Princeton Scientific Publishing Co., Inc., Princeton, New Jersey 190-196
8. Dingley K.H., Curtis K.D., Nowell S., Felton J.S., Lang N.P., and Turteltaub K.W. DNA and protein adduct formation in the colon and blood of humans after exposure to a dietary-relevant dose of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Cancer Epidemiol. Biomarkers Prev. 8 (1999) 507-512
9. 32P-postlabeling. Chem. Res. Toxicol. 7 (1994) 733-739
10. Fuscoe J.C., Wu R., Shen N.H., Healy S.K., and Felton J.S. Base-change analysis of revertants of the hisD3052 allele in Salmonella typhimurium. Mutat. Res. 201 (1988) 241-251
11. Glatt H., Pabel U., Meinl W., Frederiksen H., Frandsen H., and Muckel E. Bioactivation of the heterocyclic aromatic amine 2-amino-3-methyl-9H-pyrido [2,3-b]indole (MeAalphaC) in recombinant test systems expressing human xenobiotic-metabolizing enzymes. Carcinogenesis 25 (2004) 801-807
12. Gorlewska-Roberts K., Green B., Fares M., Ambrosone C.B., and Kadlubar F.F. Carcinogen-DNA adducts in human breast epithelial cells. Environ. Mol. Mutagen. 39 (2002) 184-192
13. Gross G.A., and Gruter A. Quantitation of mutagenic/carcinogenic heterocyclic aromatic amines in food products. J. Chromatogr. 592 (1992) 271-278
14. Hatch F.T., Knize M.G., and Colvin M.E. Extended quantitative structure-activity relationships for 80 aromatic and heterocyclic amines: structural, electronic, and hydropathic factors affecting mutagenic potency. Environ. Mol. Mutagen 38 (2001) 268-291
15. Hein D.W. Molecular genetics and function of NAT1 and NAT2: role in aromatic amine metabolism and carcinogenesis. Mutat. Res. 506-507 (2002) 65-77
16. Holland R.D., Taylor J., Schoenbachler L., Jones R.C., Freeman J.P., Miller D.W., Lake B.G., Gooderham N.J., and Turesky R.J. Rapid biomonitoring of heterocyclic aromatic amines in human urine by tandem solvent solid phase extraction liquid chromatography electrospray ionization mass spectrometry. Chem. Res. Toxicol. 17 (2004) 1121-1136
17. King R.S., Kadlubar F.F., and Turesky R.J. In vivo metabolism of heterocyclic amines. In: Nagao M., and Sugimura T. (Eds). Food Borne Carcinogens: Heterocyclic Amines (2000), John Wiley & Sons, Ltd., Chichester, England 90-111
18. Knize M.G., Dolbeare F.A., Carroll K.L., Moore D.H., and Felton J.S. Effect of cooking time and temperature on the heterocyclic amine content of fried beef patties. Food Chem. Toxicol. 32 (1994) 595-603
19. Kulp K.S., Knize M.G., Fowler N.D., Salmon C.P., and Felton J.S. PhIP metabolites in human urine after consumption of well-cooked chicken. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 802 (2004) 143-153
20. Lang N.P., Butler M.A., Massengill J.P., Lawson M., Stotts R.C., Hauer-Jensen M., and Kadlubar F.F. Rapid metabolic phenotypes for acetyltransferase and cytochrome P4501A2 and putative exposure to food-borne heterocyclic amines increase the risk for colorectal cancer or polyps. Cancer Epidemiol. Biomarkers Prev. 3 (1994) 675-682
21. Le Marchand L., Hankin J.H., Pierce L.M., Sinha R., Nerurkar P.V., Franke A.A., Wilkens L.R., Kolonel L.N., Donlon T., Seifried A., Custer L.J., Lum-Jones A., and Chang W. Well-done red meat, metabolic phenotypes and colorectal cancer in Hawaii. Mutat. Res. 506-507 (2002) 205-214
22. Lin D.-X., Meyer D.J., Ketterer B., Lang N.P., and Kadlubar F.F. Effects of human and rat glutathione-S-transferase on the covalent binding of the N-acetoxy derivatives of heterocyclic amine carcinogens in vitro: a possible mechanism of organ specificity in their carcinogensis. Cancer Res. 54 (1994) 4920-4926
23. Magagnotti C., Orsi F., Bagnati R., Celli N., Rotilio D., Fanelli R., and Airoldi L. Effect of diet on serum albumin and hemoglobin adducts of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in humans. Int. J. Cancer 88 (2000) 1-6
24. Magagnotti C., Pastorelli R., Pozzi S., Andreoni B., Fanelli R., and Airoldi L. Genetic polymorphisms and modulation of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP)-DNA adducts in human lymphocytes. Int. J Cancer 107 (2003) 878-884
25. Malfatti M.A., and Felton J.S. Human UDP-glucuronosyltransferase 1A1 is the primary enzyme responsible for the N-glucuronidation of N-hydroxy-PhIP in vitro. Chem. Res. Toxicol. 17 (2004) 1137-1144
26. Matsumoto T., Yoshida D., and Tomita H. Determination of mutagens, amino-alpha-carbolines in grilled foods and cigarette smoke condensate. Cancer Lett. 12 (1981) 105-110
27. Nagao M., Ushijima T., Toyota M., Inoue R., and Sugimura T. Genetic changes induced by heterocyclic amines. Mutat. Res. 376 (1997) 161-167
28. Nowell S., Coles B., Sinha R., MacLeod S., Luke R.D., Stotts C., Kadlubar F.F., Ambrosone C.B., and Lang N.P. Analysis of total meat intake and exposure to individual heterocyclic amines in a case-control study of colorectal cancer: contribution of metabolic variation to risk. Mutat. Res. 506-507 (2002) 175-185
29. Peters U., DeMarini D.M., Sinha R., Brooks L.R., Warren S.H., Chatterjee N., and Rothman N. Urinary mutagenicity and colorectal adenoma risk. Cancer Epidemiol. Biomarkers Prev. 12 (2003) 1253-1256
30. Sachse C., Bhambra U., Smith G., Lightfoot T.J., Barrett J.H., Scollay J., Garner R.C., Boobis A.R., Wolf C.R., and Gooderham N.J. Polymorphisms in the cytochrome P450 CYP1A2 gene (CYP1A2) in colorectal cancer patients and controls: allele frequencies, linkage disequilibrium and influence on caffeine metabolism. Br. J. Clin. Pharmacol. 55 (2003) 68-76
31. Schut H.A., and Snyderwine E.G. DNA adducts of heterocyclic amine food mutagens: implications for mutagenesis and carcinogenesis. Carcinogenesis 20 (1999) 353-368
32. Sinha R., Chow W.H., Kulldorff M., Denobile J., Butler J., Garcia-Closas M., Weil R., Hoover R.N., and Rothman N. Well-done, grilled red meat increases the risk of colorectal adenomas. Cancer Res. 59 (1999) 4320-4324
33. Skog K.I., Johansson M.A., and Jagerstad M.I. Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence and intake. Food Chem. Toxicol. 36 (1998) 879-896
34. Stillwell W.G., Turesky R.J., Sinha R., Skipper P.L., and Tannenbaum S.R. Biomonitoring of heterocyclic aromatic amine metabolites in human urine. Cancer Lett. 143 (1999) 145-148
35. Sugimura T., Nagao N., Kawachi T., Honda M., Yahagi T., Seino Y., Stao S., Matsukura N., Matsushima T., Shirai A., Sawamura M., and Matsumoto H. Mutagen-carcinogens in food, with special reference to highly mutagenic pyrolytic products in broiled foods. In: Hiatt H.H., Watson J.D., and Winstein J.A. (Eds). Origins of Human Cancer (1977), Book C Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 1561-1577
36. Sugimura T., Wakabayashi K., Nakagama H., and Nagao M. Heterocyclic amines: mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci. 95 (2004) 290-299
37. 2-(deoxyguanosin-8-yl)-2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline (dG-C8-MeIQx) in human tissues. Carcinogenesis 17 (1996) 1029-1034
38. Turesky R.J., Constable A., Richoz J., Varga N., Markovic J., Martin M.V., and Guengerich F.P. Activation of heterocyclic aromatic amines by rat and human liver microsomes and by purified rat and human cytochrome P450 1A2. Chem. Res. Toxicol. 11 (1998) 925-936
39. Turesky R.J., Garner R.C., Welti D.H., Richoz J., Leveson S.H., Dingley K.H., Turteltaub K.W., and Fay L.B. Metabolism of the food-borne mutagen 2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline in humans. Chem. Res. Toxicol. 11 (1998) 217-225
40. Turesky R.J., Parisod V., Huynh-Ba T., Langouet S., and Guengerich F.P. Regioselective differences in C(8)- and N-oxidation of 2-amino-3,8- dimethylimidazo[4,-f]quinoxaline by human and rat liver microsomes and cytochromes P450 1A2. Chem. Res. Toxicol. 14 (2001) 901-911
41. Turesky R.J., Guengerich F.P., Guillouzo A., and Langouet S. Metabolism of heterocyclic aromatic amines by human hepatocytes and cytochrome P4501A2. Mutat. Res. 506-507 (2002) 187-195
42. Turesky R.J., and Vouros P. Formation and analysis of heterocyclic aromatic amine-DNA adducts in vitro and in vivo. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 802 (2004) 155-166
43. Turesky R.J., Taylor J., Schnackenberg L., Freeman J.P., and Holland R.D. Quantitation of carcinogenic heterocyclic aromatic amines and detection of novel heterocyclic aromatic amines in cooked meats and grill scrapings by HPLC/ESI-MS. J. Agric. Food Chem. 53 (2005) 3248-3258
44. Turesky, R.J., Goodenough, A., Ni, W., McLaughton, L., LeMaster, D., Wu, R., Felton, J.S., 2006. Identification of 2-amino-1,7-dimethylimidazo[4 5-g]quinoxaline: an abundant mutagenic heterocyclic aromatic amine formed in cooked beef, submitted for publication.
45. Wakabayashi K., Kim I.S., Kurosaka R., Yamaizumi Z., Ushiyama H., Takahashi M., Koyota S., Tada A., Nukaya H., and Goto S. Identification of new mutagenic heterocyclic amines and quantification of known heterocyclic amines. In: Adamson R.H., Gustafson D.R., Ito N., Nagao M., Sugimura T., Wakabayashi K., and Yamazoe Y. (Eds). Proceedings of the 23rd International Princess Takamatsu Symposium on Heterocyclic Aromatic Amines: Possible Human Carcinogens. 23 ed. (1995), Princeton Scientific Publishing Co., Inc, Princeton 39-49
46. Walters D.G., Young P.J., Agus C., Knize M.G., Boobis A.R., Gooderham N.J., and Lake B.G. Cruciferous vegetable consumption alters the metabolism of the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in humans. Carcinogenesis 25 (2004) 1659-1669
47. Wogan G.N., Hecht S.S., Felton J.S., Conney A.H., and Loeb L.A. Environmental and chemical carcinogenesis. Semin. Cancer Biol. 14 (2004) 473-486
48. Wu R.W., Panteleakos F.N., Kadkhodayan S., Bolton-Grob R., McManus M.E., and Felton J.S. Genetically modified Chinese hamster ovary cells for investigating sulfotransferase-mediated cytotoxicity and mutation by 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine. Environ. Mol. Mutagen. 35 (2000) 57-65
49. Wu R.W., Tucker J.D., Sorensen K.J., Thompson L.H., and Felton J.S. Differential effect of acetyltransferase expression on the genotoxicity of heterocyclic amines in CHO cells. Mutat. Res. 390 (1997) 93-103
50. Zhu J., Chang P., Bondy M.L., Sahin A.A., Singletary S.E., Takahashi S., Shirai T., and Li D. Detection of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine-DNA adducts in normal breast tissues and risk of breast cancer. Cancer Epidemiol. Biomarkers Prev. 12 (2003) 830-837