Fruits and vegetables protect against the genotoxicity of heterocyclic aromatic amines activated by human xenobiotic-metabolizing enzymes expressed in immortal mammalian cells

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 703, Issue 2, 2010, Pages 90-98

  Platt, K L ^a   Edenharder, R ^a   Aderhold, S ^a   Muckel, E ^b   Glatt, H ^b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

Comet assay; Fruits; Genetically engineered hamster fibroblasts; Genotoxicity; Heterocyclic aromatic amines; IQ; PhIP; Protection; Vegetables

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 2 AMINO 3 METHYLIMIDAZO[4,5 F]QUINOLINE; ACYLTRANSFERASE; CYTOCHROME P450 1A2; SULFOTRANSFERASE 1A1;

ANIMAL CELL; ARTICLE; ENZYME ACTIVATION; FIBROBLAST; FRUIT; GENOTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VEGETABLE;

AMINES; ANIMALS; ANTIMUTAGENIC AGENTS; BEVERAGES; CELL LINE; CRICETINAE; CRICETULUS; CYTOCHROME P-450 CYP1A2; ENZYME ACTIVATION; FRUIT; HETEROCYCLIC COMPOUNDS; MUTAGENS; VEGETABLES;

ALLIUM CEPA; ANANAS COMOSUS; ASPALATHUS LINEARIS; BETA VULGARIS CICLA; BRASSICA OLERACEA VAR. BOTRYTIS; BRASSICA OLERACEA VAR. CAPITATA; BRASSICA OLERACEA VAR. ITALICA; CAPSICUM ANNUUM VAR. ANNUUM; CITRULLUS LANATUS VAR. LANATUS; CITRUS X PARADISI; CRICETINAE; CRICETULUS GRISEUS; CUCUMIS SATIVUS; FRAGARIA X ANANASSA; LYCOPERSICON ESCULENTUM; MALUS X DOMESTICA; MAMMALIA; PRUNUS AVIUM; PRUNUS CERASUS; PRUNUS DOMESTICA; RIBES HUDSONIANUM; RIBES RUBRUM; RUBUS; SPINACIA OLERACEA; VACCINIUM;

EID: 78549258809     PISSN: 13835718     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2010.08.007     Document Type: Article

References (66)

1. Lijinsky W. The formation and occurrence of polynuclear aromatic hydrocarbons associated with food. Mutat. Res. 1991, 259:251-261.
2. Sugimura T., Sato S. Mutagens-carcinogens in foods. Cancer Res. 1983, 43:2415s-2421s.
3. Knize M.G., Salmon C.P., Pais P., Felton J.S. Food heating and the formation of heterocyclic aromatic amine and polycyclic aromatic hydrocarbon mutagens/carcinogens. Adv. Exp. Med. Biol. 1999, 459:179-193.
4. Goldman R., Shields P.G. Food mutagens. J. Nutr. 2003, 133:965S-973S.
5. Sinha R., Gustafson D.R., Kulldorff M., Wen W.-Q., Cerhan J.R., Zheng W. 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine, a carcinogen in high-temperature-cooked meat, and breast cancer risk. J. Natl. Cancer Inst. 2000, 92:1352-1354.
6. Sinha R., Kulldorff M., Gunter M.J., Strickland P., Rothman N. Dietary benzo[a]pyrene intake and risk of colorectal adenoma. Cancer Epidemiol. Biomarkers Prev. 2005, 14:2030-2034.
7. Butler L.M., Sinha R., Millikan R.C., Martin C.F., Newman B., Gammon M.D., Ammerman A.S., Sandler R.S. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am. J. Epidemiol. 2003, 157:434-445.
8. Li D., Day R.S., Bondy M.L., Sinha R., Nguyen N.T., Evans D.B., Abbruzzese J.L., Hassan M.M. Dietary mutagen exposure and risk of pancreatic cancer. Cancer Epidemiol. Biomarkers Prev. 2007, 16:655-661.
9. Cross A.J., Peters U., Kirsh V.A., Andriole G.L., Reding D., Hayes R.B., Sinha R. A prospective study of meat and meat mutagens and prostate cancer risk. Cancer Res. 2005, 65:11779-11784.
10. Block G., Patterson B., Subar A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr. Cancer 1992, 18:1-29.
11. Weisburger J.H. Antimutagens, anticarcinogens, and effective worldwide cancer prevention. J. Environ. Pathol. Toxicol. Oncol. 1999, 18:85-93.
12. Kapiszewska M. A vegetable to meat consumption ratio as a relevant factor determining cancer preventive diet. The Mediterranean versus other European countries. Local Mediterranean Food Plants and Nutraceuticals 2006, 130-153. Forum Nutr. Basel, S. Karger, Basel. M. Heinrich, W.E. Müller, C. Galli (Eds.).
13. Schwab C.E., Huber W.W., Parzefall W., Hietsch G., Kassie F., Schulte-Hermann R., Knasmüller S. Search for compounds that inhibit the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Crit. Rev. Toxicol. 2000, 30:1-69.
14. Edenharder R., Kurz P., John K., Burgard S., Seeger K. In vitro effect of vegetable and fruit juices on the mutagenicity of 2-amino-3-methylimidazo[4,5-f]quinoline, 2-amino-3,4-dimethylimidazo[4,5-f]quinoline and 2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline. Food Chem. Toxic. 1994, 32:443-459.
15. Knasmüller S., Parzefall W., Sanyal R., Ecker S., Schwab C., Uhl M., Mersch-Sundermann V., Williamson G., Hietsch G., Langer T., Darroudi F., Natarajan A.T. Use of metabolically competent human hepatoma cells for the detection of mutagens and antimutagens. Mutat. Res. 1998, 402:185-202.
16. Edenharder R., Sager J.W., Glatt H., Muckel E., Platt K.L. Protection by beverages, fruits, vegetables, herbs, and flavonoids against genotoxicity of 2-acetylaminofluorene and 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in metabolically competent V79 cells. Mutat. Res. 2002, 521:57-72.
17. Hoelzl C., Knasmüller S., Mišik M., Collins A., Dušinská M., Nersesyan A. Use of single cell gel electrophoresis assays for the detection of DNA-protective effects of dietary factors in humans: recent results and trends. Mutat. Res. 2009, 681:68-79.
18. Turesky R.J. Heterocyclic aromatic amine metabolism, DNA adduct formation, mutagenesis, and carcinogenesis. Drug Metab. Rev. 2002, 34:625-650.
19. 2-oxidized species of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in rat liver. Carcinogenesis 1991, 12:2239-2245.
20. 2-glucuronide conjugate of 2-hydroxyamino-MeIQx in urine. Cancer Res. 1999, 59:5154-5159.
21. Doehmer J. V79 Chinese hamster cells genetically engineered for cytochrome P450 and their use in mutagenicity and metabolism studies. Toxicology 1993, 82:105-118.
22. Yanagawa Y., Sawada M., Deguchi T., Gonzalez F.J., Kamataki T. Stable expression of human CYP1A2 and N-acetyltransferases in Chinese hamster CHL cells: mutagenic activation of 2-amino-3-methylimidazo[4,5-f]quinoline and 2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline. Cancer Res. 1994, 54:3422-3427.
23. Glatt H., Pabel U., Meinl W., Frederiksen H., Frandsen H., Muckel E. Bioactivation of the heterocyclic aromatic amine 2-amino-3-methyl-9H-pyrido[2,3-b]indole (MeAαC) in recombinant test systems expressing human xenobiotic-metabolizing enzymes. Carcinogenesis 2004, 25:801-807.
24. Natarajan A.T., Darroudi F. Use of human hepatoma cells for in vitro metabolic activation of chemical mutagens/carcinogens. Mutagenesis 1991, 6:399-403.
25. Sugimura T., Wakabayashi K., Nakagama H., Nagao M. Heterocyclic amines: mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci. 2004, 95:290-299.
26. Felton J.S., Knize M.G. Occurrence, identification, and bacterial mutagenicity of heterocyclic amines in cooked food. Mutat. Res. 1991, 259:205-217.
27. Richling E., Häring D., Herderich M., Schreier P. Determination of heterocyclic aromatic amines (HAA) in commercially available meat products and fish by high performance liquid chromatography-electrospray tandem mass spectrometry (HPLC-ESI-MS-MS). Chromatographia 1998, 48:258-262.
28. Platt K.L., Oesch F. Efficient synthesis of non-K-region trans-dihydro diols of polycyclic aromatic hydrocarbons from o-quinones and catechols. J. Org. Chem. 1983, 48:265-268.
29. Czich A., Bartsch I., Dogra S., Hornhardt S., Glatt H.R. Stable heterologous expression of hydroxysteroid sulphotransferase in Chinese hamster V79 cells and their use for toxicological investigations. Chem. -Biol. Interact. 1994, 92:119-128.
30. Olive P.L., Banáth J.P., Durand R.E. Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the " comet" assay. Radiat. Res. 1990, 122:86-94.
31. Burke M.D., Mayer R.T. Ethoxyresorufin: direct fluorimetric assay of a microsomal O-dealkylation which is preferentially inducible by 3-methylcholanthrene. Drug Metab. Dispos. 1974, 2:583-588.
32. Lubet R.A., Nims R.W., Mayer R.T., Cameron J.W., Schechtman L.M. Measurement of cytochrome P-450 dependent dealkylation of alkoxyphenoxazones in hepatic S9s and hepatocytes homogenates: effects of dicumarol. Mutat. Res. 1985, 142:127-131.
33. Platt K.L., Utesch D., Gemperlein-Mertes I., Glatt H.R., Oesch F. Metabolizing systems in short-term in vitro tests for carcinogenicity. Food Chem. Toxicol. 1986, 24:721-729.
34. PA (P-450IA2), the phenacetin O-deethylase, is primarily responsible for the hepatic 3-demethylation of caffeine and N-oxidation of carcinogenic arylamines. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:7696-7700.
35. Turesky R.J., Guengerich F.P., Guillouzo A., Langouët S. Metabolism of heterocyclic aromatic amines by human hepatocytes and cytochrome P4501A2. Mutat. Res. 2002, 506-507:187-195.
36. Turesky R.J. Formation and biochemistry of carcinogenic heterocyclic aromatic amines in cooked meats. Toxicol. Lett. 2007, 168:219-227.
37. Meyer U.A., Zanger U.M. Molecular mechanisms of genetic polymorphisms of drug metabolism. Annu. Rev. Pharmacol. Toxicol. 1997, 37:269-296.
38. Glatt H. Sulphotransferases. Enzyme Systems that Metabolise Drugs and Other Xenobiotics 2002, 353-439. J. Wiley, Chichester. C. Ioannides (Ed.).
39. Martin F.L., Cole K.J., Orme M.H., Grover P.L., Phillips D.H., Venitt S. The DNA repair inhibitors hydroxyurea and cytosine arabinoside enhance the sensitivity of the alkaline single-cell gel electrophoresis ('comet') assay in metabolically-competent MCL-5 cells. Mutat. Res. 1999, 445:21-43.
40. Watanabe M., Matsuoka A., Yamazaki N., Hayashi M., Deguchi T., Nohmi T., Sofuni T. New sublines of Chinese hamster CHL stably expressing human NAT1 or NAT2 N-acetyltransferases or Salmonella typhimurium O-acetyltransferase: comparison of the sensitivities to nitroarenes and aromatic amines using the in vitro micronucleus test. Cancer Res. 1994, 54:1672-1677.
41. Wild D., Feser W., Michel S., Lord H.L., Josephy P.D. Metabolic activation of heterocyclic aromatic amines catalyzed by human arylamine N-acetyltransferase isozymes (NAT1 and NAT2) expressed in Salmonella typhimurium. Carcinogenesis 1995, 16:643-648.
42. Abu-Zeid M., Yamazoe Y., Kato R. Sulfotransferase-mediated DNA binding of N-hydroxyarylamines(amide) in liver cytosols from human and experimental animals. Carcinogenesis 1992, 13:1307-1314.
43. Davis C.D., Schut H.A.J., Snyderwine E.G. Enzymatic phase II activation of the N-hydroxylamines of IQ, MeIQx and PhIP by various organs of monkeys and rats. Carcinogenesis 1993, 14:2091-2096.
44. Glatt H. Factors affecting the mutagenicity of heterocyclic amines. Acrylamide and Other Health Hazardous Compounds in Heat-treated Foods 2006, 358-404. Woodhead Publishing, Cambridge. K. Skog, J. Alexander (Eds.).
45. Ozawa S., Chou H.-C., Kadlubar F.F., Nagata K., Yamazoe Y., Kato R. Activation of 2-hydroxyamino-1-methyl-6-phenylimidazo[4,5-b]pyridine by cDNA-expressed human and rat arylsulfotransferases. Jpn. J. Cancer Res. 1994, 85:1220-1228.
46. Wiebel F.J., Singh J., Schindler E., Summer K.-H. UDP-glucuronosyl-, phenol sulfo-, and glutathione-S-transferase activities of mammalian cells in permanent culture. Toxicology 1980, 17:123-126.
47. Holme J.A., Wallin H., Brunborg G., Søderlund E.J., Hongslo J.K., Alexander J. Genotoxicity of the food mutagen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP): formation of 2-hydroxamino-PhIP, a directly acting genotoxic metabolite. Carcinogenesis 1989, 10:1389-1396.
48. Kuroda Y., Hara Y. Antimutagenic and anticarcinogenic activity of tea polyphenols. Mutat. Res. 1999, 436:69-97.
49. Hernaez J., Xu M., Dashwood R. Effects of tea and chlorophyllin on the mutagenicity of N-hydroxy-IQ: studies of enzyme inhibition, molecular complex formation, and degradation/scavenging of the active metabolites. Environ. Mol. Mutagen. 1997, 30:468-474.
50. Lin D.-X., Thompson P.A., Teitel C., Chen J.-S., Kadlubar F.F. Direct reduction of N-acetoxy-PhIP by tea polyphenols: a possible mechanism for chemoprevention against PhIP-DNA adduct formation. Mutat. Res. 2003, 523-524:193-200.
51. Wolter F., Stein J. Biological activities of resveratrol and its analogs. Drug Fut. 2002, 27:949-959.
52. Kim D.-O., Heo H.J., Kim Y.J., Yang H.S., Lee C.Y. Sweet and sour cherry phenolics and their protective effects on neuronal cells. J. Agric. Food Chem. 2005, 53:9921-9927.
53. Kahle K., Kraus M., Richling E. Polyphenol profiles of apple juices. Mol. Nutr. Food Res. 2005, 49:797-806.
54. 4 on L1210 cells. Cancer Res. 1978, 38:1677-1687.
55. Fuhr U., Klittich K., Staib A.H. Inhibitory effect of grapefruit juice and its bitter principal, naringenin, on CYP1A2 dependent metabolism of caffeine in man. Br. J. Clin. Pharmacol. 1993, 35:431-436.
56. Aden D.P., Fogel A., Plotkin S., Damjanov I., Knowles B.B. Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 1979, 282:615-616.
57. Glatt H., Gemperlein I., Setiabudi F., Platt K.L., Oesch F. Expression of xenobiotic-metabolizing enzymes in propagatable cell cultures and induction of micronuclei by 13 compounds. Mutagenesis 1990, 5:241-249.
58. Kassie F., Mersch Sundermann V., Edenharder R., Platt K.L., Darroudi F., Lhoste E., Humbolt C., Muckel E., Uhl M., Kundi M., Knasmüller S. Development and application of test methods for the detection of dietary constituents which protect against heterocyclic aromatic amines. Mutat. Res. 2003, 523-524:183-192.
59. Dunn W.C., Regan J.D. Inhibition of DNA excision repair in human cells by arabinofuranosyl cytosine: effect on normal and xeroderma pigmentosum cells. Mol. Pharmacol. 1979, 15:367-374.
60. Doostdar H., Duthie S.J., Burke M.D., Melvin W.T., Grant M.H. The influence of culture medium composition on drug metabolising enzyme activities of the human liver derived Hep G2 cell line. FEBS Lett. 1988, 241:15-18.
61. Nakama A., Kuroda K., Yamada A. Induction of cytochrome P450-dependent monooxygenase in serum-free cultured Hep G2 cells. Biochem. Pharmacol. 1995, 50:1407-1412.
62. Kim D.-O., Chun O.K., Kim Y.J., Moon H.-Y., Lee C.Y. Quantification of polyphenolics and their antioxidant capacity in fresh plums. J. Agric. Food Chem. 2003, 51:6509-6515.
63. Chakraborty M., Savarese M., Harbertson E., Harbertson J., Ringer K.L. Effect of the novel radiant zone drying method on anthocyanins and phenolics of three blueberry liquids. J. Agric. Food Chem. 2010, 58:324-330.
64. Sommerburg O., Keunen J.E.E., Bird A.C., van Kuijk F.J.G.M. Fruits and vegetables that are sources for lutein and zeaxanthin: the macular pigment in human eyes. Br. J. Ophthalmol. 1998, 82:907-910.
65. Slimestad R., Fossen T., Vågen I.M. Onions: a source of unique dietary flavonoids. J. Agric. Food Chem. 2007, 55:10067-10080.
66. Eggler A.L., Gay K.A., Mesecar A.D. Molecular mechanisms of natural products in chemoprevention: induction of cytoprotective enzymes by Nrf2. Mol. Nutr. Food Res. 2008, 52:S84-S94.