Consumption of Brussels sprouts protects peripheral human lymphocytes against 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhiP) and oxidative DNA-damage: Results of a controlled human intervention trial

Molecular Nutrition and Food Research

Volumn 52, Issue 3, 2008, Pages 330-341

  Hoelzl, Christine ^a   Glatt, Hansruedi ^b   Meinl, Walter ^b   Sontag, Gerhard ^c   Haidinger, Gerald ^a   Kundi, Michael ^d   Simic, Tatjana ^e   Chakraborty, Asima ^a   Bichler, Julia ^a   Ferk, Franziska ^a   Angelis, Karel ^f   Nersesyan, Armen ^a   Knasmüller, Siegfried ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^c UNIVERSITY OF VIENNA   (Austria)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e UNIVERSITY OF BELGRADE   (Serbia)

^f INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

Author keywords

Antioxidant; Comet assay; Cruciferous vegetables; Heterocyclic aromatic amines; Sulfotransferase

Indexed keywords

BRASSICA OLERACEA VAR. GEMMIFERA;

2 AMINO 1 METHYL 6 PHENYLIMIDAZO(4,5 B)PYRIDINE; 2-AMINO-1-METHYL-6-PHENYLIMIDAZO(4,5-B)PYRIDINE; ANTINEOPLASTIC AGENT; ANTIOXIDANT; ARYL SULFOTRANSFERASE; ASCORBIC ACID; GLUTATHIONE PEROXIDASE; IMIDAZOLE DERIVATIVE; MONOAMINE SULFATING PHENOL SULFOTRANSFERASE; MONOAMINE-SULFATING PHENOL SULFOTRANSFERASE; REACTIVE OXYGEN METABOLITE; SULFOTRANSFERASE; SULT1A1 PROTEIN, HUMAN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; AUSTRIA; BLOOD; BRASSICA; CLINICAL TRIAL; DIET; DNA DAMAGE; DRUG EFFECT; FEMALE; HUMAN; LYMPHOCYTE; MALE; METABOLISM; OXIDATIVE STRESS;

ADULT; ANTICARCINOGENIC AGENTS; ANTIOXIDANTS; ARYLSULFOTRANSFERASE; ASCORBIC ACID; AUSTRIA; BRASSICA; DIET; DNA DAMAGE; FEMALE; GLUTATHIONE PEROXIDASE; HUMANS; IMIDAZOLES; LYMPHOCYTES; MALE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SULFOTRANSFERASES; SUPEROXIDE DISMUTASE;

EID: 41949089207     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200700406     Document Type: Article

References (91)

1. Steinmetz, K. A., Potter, J. D., Vegetables, fruit, and cancer prevention: a review, J. Am. Diet Assoc. 1996, 96, 1027-1039.
2. Van Poppel, G., Verhoeven, D. T., Verhagen, H., Goldbohm, R. A., Brassica vegetables and cancer prevention. Epidemiology and mechanisms, Adv. Exp. Med. Biol. 1999, 472, 159-168.
3. Lee, H. P., Gourley, L., Duffy, S. W., Esteve, J., et al., Colorectal cancer and diet in an Asian population-a case-control study among Singapore Chinese, Int. J. Cancer 1989, 43, 1007-1016.
4. Seow, A., Yuan, J. M., Sun, C. L., Van Den Berg, D., et al., Dietary isothiocyanates, glutathione S-transferase polymorphisms and colorectal cancer risk in the Singapore Chinese Health Study, Carcinogenesis 2002, 23, 2055-2061.
5. Schwab, C., Kassie, F., Qin, H.-M., Sanyal, R., et al., Development of test systems for the detection of compounds which prevent the genotoxic effects of heterocyclic aromatic amines: preliminary results with constituents of cruciferous vegetables and other dietary constituents, J. Environ. Pathol. Toxicol. Oncol. 1999, 18, 109-188.
6. Kassie, F., Uhl, M., Rabot, S., Grasl-Kraupp, B., et al., Chemoprevention of 2-amino-3-methylimidazo[4,5-f]quinoline (IQ)-induced colonic and hepatic preneoplastic lesions in the F344 rat by cruciferous vegetables administered simultaneously with the carcinogen, Carcinogenesis 2003, 24, 255-261.
7. Kassie, F., Rabot, S., Uhl, M., Huber, W., et al., Chemoprotective effects of garden cress (Lepidium sativum) and its constituents towards 2-amino-3-methyl-imidazo[4,5-f]quinoline (IQ)-induced genotoxic effects and colonic preneoplastic lesions, Carcinogenesis 2002, 23, 1155-1161.
8. Huber, W. W., McDaniel, L. P., Kaderlik, K. R., Teitel, C. H., et al., Chemoprotection against the formation of colon DNA adducts from the food-borne carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in the rat, Mutat. Res. 1997, 376, 115-122.
9. Jagerstad, M., Skog, K., Formation of meat mutagens, Adv. Exp. Med. Biol. 1991, 289, 83-105.
10. Augustsson, K., Skog, K., Jagerstad, M., Dickman, P. W., Steineck, G., Dietary heterocyclic amines and cancer of the colon, rectum, bladder, and kidney: a population-based study, Lancet 1999, 353, 703-707.
11. Schwab, C. E., Huber, W. W., Parzefall, W., Hietsch, G., et al., Search for compounds that inhibit the genotoxic and carcinogenic effects of heterocyclic aromatic amines, Crit .Rev. Toxicol. 2000, 30, 1-69.
12. Dashwood, R. H., Modulation of heterocyclic amine-induced mutagenicity and carcinogenicity: an ,A-to-Z' guide to chemopreventive agents, promoters, and transgenic models, Mutat. Res. 2002, 511, 89-112.
13. Frandsen, H., Frederiksen, H., Alexander, J., 2-Amino-1-methyl-6-(5- hydroxy-)phenylimidazo[4,5-b]pyridine (5-OHPhIP), a biomarker for the genotoxic dose of the heterocyclic amine, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), Food Chem. Toxicol. 2002, 40, 1125-1130.
14. Moller, P., Loft, S., Interventions with antioxidants and nutrients in relation to oxidative DNA damage and repair, Mutat. Res. 2004, 551, 79-89.
15. Moller, P., Loft, S., Oxidative DNA damage in human white blood cells in dietary antioxidant intervention studies, Am. J. Clin. Nutr. 2002, 76, 303-310.
16. Collins, A. R., Duthie, S. J., Dobson, V. L., Direct enzymic detection of endogenous oxidative base damage in human lymphocyte DNA, Carcinogenesis 1993, 14, 1733-1735.
17. Duthie, S. J., Collins, A. R., Duthie, G. G., Dobson, V. L., Quercetin and myricetin protect against hydrogen peroxide-induced DNA damage (strand breaks and oxidized pyrimidines) in human lymphocytes, Mutat. Res. 1997, 393, 223-231.
18. Anderson, D., Dobrzynska, M. M., Basaran, N., Basaran, A., Yu, T. W., Flavonoids modulate comet assay responses to food mutagens in human lymphocytes and sperm, Mutat. Res. 1998, 402, 269-277.
19. Anderson, D., Basaran, N., Dobrzynska, M. M., Basaran, A. A., Yu, T.W., Modulating effects of flavonoids on food mutagens in human blood and sperm samples in the comet assay, Teratog. Carcinog. Mutagen 1997, 17, 45-58.
20. Kassie, F., Parzefall, W., Musk, S., Johnson, I., et al., Genotoxic effects of crude juices from Brassica vegetables and juices and extracts from phytopharmaceutical preparations and spices of cruciferous plants origin in bacterial and mammalian cells, Chem. Biol. Interact. 1996, 102, 1-16.
21. Laky, B., Knasmuller, S., Gminski, R., Mersch-Sundermann, V. et al., Protective effects of Brussels sprouts towards B[a]P-induced DNA damage: a model study with the single-cell gel electrophoresis (SCGE)/Hep G2 assay, Food Chem. Toxicol. 2002, 40, 1077-1083.
22. W.H.O. IARC Heterocyclic aromatic amines, in: W.H.O. International Agency for Research on Cancer (Ed.), IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans: Some natural occuring substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mykotoxines, IARC, Lyon 1993, pp. 229-242.
23. W.H.O. IARC Trp-P-2 and its acetate, in: W.H.O. International Agency for Research on Cancer (Ed.), IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans:Some natural occuring substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mykotoxines, IARC, Lyon 1983, pp. 255-263.
24. W.H.O. IARC Heterocyclic aromatic amines, in: W.H.O. International Agency for Research on Cancer (Ed.), IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans: Some natural occuring substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mykotoxines, IARC, Lyon 1993, pp. 29.
25. Ito, N., Hasegawa, R., Sano, M., Tamano, S., et al., 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.
26. Knasmuller, S., Parzefall, W., Sanyal, R., Ecker, S., et al., Use of metabolically competent human hepatoma cells for the detection of mutagens and antimutagens, Mutat. Res. 1998, 402, 185-202.
27. Overvik, E., Gustafsson, J. A., Cooked-food mutagens: current knowledge of formation and biological significance, Mutagenesis 1990, 5, 437-446.
28. Jagerstad, M., Skog, K., Genotoxicity of heat-processed foods, Mutat. Res. 2005, 574, 156-172.
29. Ames, B. N., Shigenaga, M. K., Gold, L. S., DNA lesions, inducible DNA repair, and cell division: three key factors in mutagenesis and carcinogenesis, Environ. Health Perspect. 1993, 101 (Suppl. 5), 35-44.
30. Hussain, S. P., Hofseth, L. J., Harris, C. C., Radical causes of cancer, Nat. Rev. Cancer 2003, 3, 276-285.
31. Boiteux, S., O'Connor, T. R., Laval, J., Formamidopyrimidine-DNA glycosylase of Escherichia coli, cloning and sequencing of the fpg structural gene and overproduction of the protein, EMBO J. 1987, 6, 3177-3183.
32. Rogers, S. G., Weiss, B., Exonuclease III of Escherichia coli K-12, an AP endonuclease, Methods Enzymol. 1980, 65, 201-211.
33. Demirbag, R., Yilmaz, R., Gur, M., Celik, H., et al., DNA damage in metabolic syndrome and its association with antioxidative and oxidative measurements, Int. J. Clin. Pract. 2006, 60, 1187-1193.
34. Park, E., Kang, M. H., Smoking and high plasma triglyceride levels as risk factors for oxidative DNA damage in the Korean population, Ann. Nutr. Metab. 2004, 48, 36-42.
35. Kazimirova, A., Barancokova, M., Volkovova, K., Staruchova, M., et al., Does a vegetarian diet influence genomic stability? Eur. J. Nutr. 2004, 43, 32-38.
36. Hoelzl, C., Bichler, J., Ferk, F., Simic, T., et al., Methods for the detection of antioxidants which prevent age related diseases: a critical review with particular emphasis on human intervention studies, J. Physiol. Pharmacol. 2005, 56 (Suppl. 2), 49-64.
37. Hartmann, A., Plappert, U., Raddatz, K., Grunert-Fuchs, M., Speit, G., Does physical activity induce DNA damage? Mutagenesis 1994, 9, 269-272.
38. Duthie, S. J., Ross, M., Collins, A. R., The influence of smoking and diet on the hypoxanthine phosphoribosyltransferase (hprt) mutant frequency in circulating T lymphocytes from a normal human population, Mutat. Res. 1995, 331, 55-64.
39. Tice, R. R., Agurell, E., Anderson, D., Burlinson, B., et al., Single-cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing, Environ. Mol. Mutagen. 2000, 35, 206-221.
40. Lindl, T., Bauer, J., Zell- und Gewebekultur, Fischer Stuttgart, Jena, New York 1994.
41. Collins, A. R., Dobson, V. L., Dusinska, M., Kennedy, G., Stetina, R., The comet assay: what can it really tell us? Mutat. Res. 1997, 375, 183-193.
42. Helma, C., Uhl, M., A public domain image-analysis program for the single-cell gel-electrophoresis (comet) assay, Mutat. Res. 2000, 466, 9-15.
43. Misra, H. P., Fridovich, I., The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase, J. Biol. Chem. 1972, 247, 3170-3175.
44. Gunzler, W. A., Kremers, H., Flohe, L., An improved coupled test procedure for glutathione peroxidase (EC 1-11-1-9) in blood, Z. Klin. Chem. Klin. Biochem. 1974, 12, 444-448.
45. Foldes, A., Meek, J. L., Rat brain phenolsulfotransferase: partial purification and some properties, Biochim. Biophys. Acta 1973, 327, 365-374.
46. Tovey, E. R., Baldo, B. A., Comparison of semidry and conventional tankbuffer electrotransfer of proteins from polyacrylamide gels to nitrocellulose membranes, Electrophoresis 1987, 8, 384-387.
47. Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 1970, 227, 680-685.
48. Richard, K., Hume, R., Kaptein, E., Stanley, E. L., et al., Sulfation of thyroid hormone and dopamine during human development: ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung, and brain, J. Clin. Endocrinol. Metab. 2001, 86, 2734-2742.
49. Rose, R. C., Bode, A. M., Analysis of water-soluble antioxidants by high-pressure liquid chromatography, Biochem. J. 1995, 306, 101-105.
50. Muckel, E., Frandsen, H., Glatt, H. R., Heterologous expression of human N-acetyltransferases 1 and 2 and sulfotransferase 1A1 in Salmonella typhimurium for mutagenicity testing of heterocyclic amines, Food Chem. Toxicol. 2002, 40, 1063-1068.
51. Glatt, H. R., Activation and inactivation of carcinogens by human sulfotransferases. In: Pacifici, G. M., Coughtrie, M. W. H. (Eds.), Human sulfotransferases, Taylor & Francis, London 2005, pp. 281-306.
52. Felton, J. S., Knize, M. G., Bennett, L. M., Malfatti, M. A., et al., Impact of environmental exposures on the mutagenicity/carcinogenicity of heterocyclic amines, Toxicology 2004, 198, 135-145.
53. Steinkellner, H., Rabot, S., Freywald, C., Nobis, E., et al., Effects of cruciferous vegetables and their constituents on drug metabolizing enzymes involved in the bioactivation of DNA-reactive dietary carcinogens, Mutat. Res. 2001, 480-481, 285-297.
54. Raucy, J. L., Ingelman-Sundberg, M., Carpenter, S., Rannug, A., et al., Drug metabolizing enzymes in lymphocytes, J. Biochem. Mol. Toxicol. 1999, 13, 223-226.
55. Deep, G., Agarwal, R., Chemopreventive efficacy of silymarin in skin and prostate cancer, Integr. Cancer Ther. 2007, 6, 130-145.
56. Ren, W., Qiao, Z., Wang, H., Zhu, L., Zhang, L., Flavonoids: promising anticancer agents, Med. Res. Rev. 2003, 23, 519-534.
57. Sanchez-Perez, Y., Carrasco-Legleu, C., Garcia-Cuellar, C., Perez-Carreon, J., et al., Oxidative stress in carcinogenesis. Correlation between lipid peroxidation and induction of preneoplastic lesions in rat hepatocarcinogenesis, Cancer Lett. 2005, 217, 25-32.
58. Yanaida, Y., Kohno, H., Yoshida, K., Hirose, Y., et al., Dietary silymarin suppresses 4-nitroquinoline 1-oxide-induced tongue carcinogenesis in male F344 rats, Carcinogenesis 2002, 23, 787-794.
59. Visser, T. J., Kaptein, E., Glatt, H., Bartsch, I., et al., Characterization of thyroid hormone sulfotransferases, Chem. Biol. Interact. 1998, 109, 279-291.
60. Daimon, H., Sawada, S., Asakura, S., Sagami, F., Inhibition of sulfotransferase affecting in vivo genotoxicity and DNA adducts induced by safrole in rat liver, Teratog. Carcinog. Mutagen. 1997, 17, 327-337.
61. Hölzl, C., Schutzeffekte von Kohlsprossen vor freien Sauerstoffradikalen und heterozyklischen Aminen, Nutritional Sciences, University of Vienna, Vienna 2004, Thesis, pp. 72.
62. King, R. S., Teitel, C. H., Kadlubar, F. F., In vitro bioactivation of N-hydroxy-2-amino-alpha-carboline, Carcinogenesis 2000, 21, 1347-1354.
63. Boelsterli, U. A., Ho, H. K., Zhou, S., Leow, K. Y., Bioactivation and hepatotoxicity of nitroaromatic drugs, Curr. Drug Metab. 2006, 7, 715-727.
64. Hempel, N., Gamage, N., Martin, J. L., McManus, M. E., Human cytosolic sulfotransferase SULT1A1, Int. J. Biochem. Cell. Biol. 2007, 39, 685-689.
65. Ku, W. W., Bigger, A., Brambilla, G., Glatt, H., et al., Strategy for genotoxicity testing-metabolic considerations, Mutat. Res. 2007, 627, 59-77.
66. Glatt, H., Sulfotransferases in the bioactivation of xenobiotics, Chem. Biol. Interact. 2000, 129, 141-170.
67. Glatt, H., Meinl, W., Use of genetically manipulated Salmonella typhimurium strains to evaluate the role of sulfotransferases and acetyltransferases in nitrofen mutagenicity, Carcinogenesis 2004, 25, 779-786.
68. Meinl, W., Meerman, J. H., Glatt, H., Differential activation of promutagens by alloenzymes of human sulfotransferase 1A2 expressed in Salmonella typhimurium, Pharmacogenetics 2002, 12, 677-689.
69. Futakuchi, M., Cheng, J. L., Hirose, M., Kimoto, N., et al., Inhibition of conjugated fatty acids derived from safflower or perilla oil of induction and development of mammary tumors in rats induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), Cancer Lett. 2002, 178, 131-139.
70. Cavin, C., Holzhaeuser, D., Scharf, G., Constable, A., et al., Cafestol and kahweol, two coffee specific diterpenes with anticarcinogenic activity, Food Chem. Toxicol. 2002, 40, 1155-1163.
71. Huber, W. W., Teitel, C. H., Coles, B. F., King, R. S. et al., Potential chemoprotective effects of the coffee components kahweol and cafestol palmitates via modification of hepatic N-acetyltransferase and glutathione S-transferase activities, Environ. Mol. Mutagen. 2004, 44, 265-276.
72. Mori, Y., Koide, A., Tatematsu, K., Sugie, S., Mori, H., Effects of alpha-naphthyl isothiocyanate and a heterocyclic amine, PhIP, on cytochrome P-450, mutagenic activation of various carcinogens and glucuronidation in rat liver, Mutagenesis 2005, 20, 15-22.
73. Dashwood, R. H., Xu, M., The disposition and metabolism of 2-amino-3-methylimidazo-[4,5-f]quinoline in the F344 rat at high versus low doses of indole-3-carbinol, Food Chem. Toxicol. 2003, 41, 1185-1192.
74. Walters, D. G., Young, P. J., Agus, C., Knize, M. G., et al., Cruciferous vegetable consumption alters the metabolism of the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in humans, Carcinogenesis 2004, 25, 1659-1669.
75. Zhu, C., Poulsen, H. E., Loft, S., Inhibition of oxidative DNA damage in vitro by extracts of brussels sprouts, Free Radic. Res. 2000, 33, 187-196.
76. Podsedek, A., Sosnowska, D., Redzynia, M., Anders, B., Antioxidant capacity and content of Brassica oleracea dietary antioxidants, Int. J. Food Sci. Technol. 2006, 41(s1), 49-58.
77. Panayiotidis, M., Collins, A. R., Ex vivo assessment of lymphocyte antioxidant status using the comet assay, Free Radic. Res. 1997, 27, 533-537.
78. Welch, R.W., Turley, E., Sweetman, S. F., Kennedy, G., et al., Dietary antioxidant supplementation and DNA damage in smokers and nonsmokers, Nutr. Cancer 1999, 34, 167-172.
79. Anderson, D., Phillips, B. J., Yu, T. W., Edwards, A. J., et al., The effects of vitamin C supplementation on biomarkers of oxygen radical generated damage in human volunteers with "low" or "high" cholesterol levels, Environ. Mol. Mutagen. 1997, 30, 161-174.
80. Brennan, L. A., Morris, G. M., Wasson, G. R., Hannigan, B. M., Barnett, Y. A., The effect of vitamin C or vitamin E supplementation on basal and H2O2-induced DNA damage in human lymphocytes, Br. J. Nutr. 2000, 84, 195-202.
81. Williamson, G., Faulkner, K., Plumb, G. W., Glucosinolates and phenolics as antioxidants from plant foods, Eur. J. Cancer Prev. 1998, 7, 17-21.
82. Verhagen, H., Poulsen, H. E., Loft, S., van Poppel, G., et al., Reduction of oxidative DNA-damage in humans by brussels sprouts, Carcinogenesis 1995, 16, 969-970.
83. Verhagen, H., de Vries, A., Nijhoff, W. A., Schouten, A., et al., Effect of Brussels sprouts on oxidative DNA-damage in man, Cancer Lett. 1997, 114, 127-130.
84. Deng, X. S., Tuo, J., Poulsen, H. E., Loft, S., Prevention of oxidative DNA damage in rats by Brussels sprouts, Free Radic. Res. 1998, 28, 323-333.
85. Gedik, C. M., Boyle, S. P., Wood, S. G., Vaughan, N. J., Collins, A. R., Oxidative stress in humans: validation of biomarkers of DNA damage, Carcinogenesis 2002, 23, 1441-1446.
86. Porrini, M., Riso, P., Lymphocyte lycopene concentration and DNA protection from oxidative damage is increased in women after a short period of tomato consumption, J. Nutr. 2000, 130, 189-192.
87. Collins, B. H., Horska, A., Hotten, P. M., Riddoch, C., Collins, A. R., Kiwifruit protects against oxidative DNA damage in human cells and in vitro, Nutr. Cancer 2001, 39, 148-153.
88. van den Berg, R., van Vliet, T., Broekmans, W. M., Cnubben, N. H. et al., A vegetable/fruit concentrate with high antioxidant capacity has no effect on biomarkers of antioxidant status in male smokers, J. Nutr. 2001, 131, 1714-1722.
89. Moller, P., Vogel, U., Pedersen, A., Dragsted, L. O., et al., No effect of 600 grams fruit and vegetables per day on oxidative DNA damage and repair in healthy nonsmokers, Cancer Epidemiol. Biomarkers Prev. 2003, 12, 1016-1022.
90. Wiseman, A., Dietary anticancer isothiocyanates (ITC) in Brassica raise the reduced-glutathione barrier to DNA-damage in the colon, Trends Food Sci. Technol. 2005, 16, 215-216.
91. Verhoeven, D. T., Goldbohm, R. A., van Poppel, G., Verhagen, H., van den Brandt, P. A., Epidemiological studies on Brassica vegetables and cancer risk, Cancer Epidemiol. Biomarkers Prev. 1996, 5, 733-748.