Comparison of the effect of raw and blanched-frozen broccoli on DNA damage in colonocytes

Cell Biochemistry and Function

Volumn 33, Issue 5, 2015, Pages 266-276

  Lynn, Anthony ^a   Fuller, Zoë ^b   Collins, Andrew R ^c   Ratcliffe, Brian ^b  

^a SHEFFIELD HALLAM UNIVERSITY   (United Kingdom)

^b ROBERT GORDON UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Broccoli; Comet assay; DNA damage; Glucosinolates

Indexed keywords

ANTIOXIDANT; DRUG METABOLIZING ENZYME; POLYPHENOL; XENOBIOTIC AGENT; GLYCOSIDASE; THIOGLUCOSIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROCCOLI; CELL PROTECTION; COLONOCYTE; COLORECTAL CANCER; CONTROLLED STUDY; CYTOSOLIC FRACTION; DIET; DNA DAMAGE; EPITHELIUM CELL; EXPERIMENTAL PIG; FOOD FREEZING; FOOD INTAKE; GENETIC VARIABILITY; MALE; NONHUMAN; PLASMA; PRIORITY JOURNAL; RAW FOOD; SIBLING; VEGETABLE; ADVERSE EFFECTS; ANIMAL; BRASSICA; COLON; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PIG;

BRASSICA OLERACEA VAR. ITALICA; PIERIS BRASSICAE; SUIDAE; SUS;

ANIMALS; BRASSICA; COLON; DNA DAMAGE; FROZEN FOODS; GLYCOSIDE HYDROLASES; MALE; RAW FOODS; SWINE; XENOBIOTICS;

EID: 84937817603     PISSN: 02636484     EISSN: 10990844     Source Type: Journal    
DOI: 10.1002/cbf.3106     Document Type: Article

References (85)

1. Kassie F, Uhl M, Rabot S, Grasl-Kraupp B, Verkerk R, 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.
2. Smith TK, Mithen R, Johnson IT. Effects of Brassica vegetable juice on the induction of apoptosis and aberrant crypt foci in rat colonic mucosal crypts in vivo. Carcinogenesis 2003; 24: 491-495.
3. Arikawa AY, Gallaher DD. Cruciferous vegetables reduce the morphological markers of colon cancer risk in dimethylhydrazine-treated rats. J Nutr 2008; 138: 526-532.
4. DeSouza S, Eitenmiller RR. Effects of processing and storage on the folate content of spinach and broccoli. J Food Sci 1986; 51: 626-628.
5. Price KR, Casuscelli F, Colquhoun IJ, Rhodes MJC. Composition and content of flavonol glycosides in broccoli florets (Brassica olearacea) and their fate during cooking. J Sci Food Agr 1998; 77: 468-472.
6. Kurilich AC, Tsau GJ, Brown A, Howard L, Klein BP, Jeffery EH, Kushad M, Wallig MA, Juvik JA. Carotene, tocopherol, and ascorbate contents in subspecies of Brassica oleracea. J Agric Food Chem 1999; 47: 1576-1581.
7. Johnson IT. Glucosinolates: bioavailability and importance to health. Int J Vitam Nutr Res 2002; 72: 26-31.
8. Holst B, Williamson G. A critical review of the bioavailability of glucosinolates and related compounds. Nat Prod Rep 2004; 21: 425-447.
9. Bones AM, Rossiter JT. The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol Plant 1996; 97: 194-208.
10. Shapiro TA, Fahey JW, Wade KL, Stephenson KK, Talalay P. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol, Biomarkers Prevent 1998; 7: 1091-1110.
11. Conaway CC, Getahun SM, Liebes LL, Pusateri DJ, Topham DKW, et al. Disposition of glucosinolates and sulforaphane in humans after ingestion of steamed and fresh broccoli. Nutr Cancer 2000; 38: 168-178.
12. Rouzard G, Young SA, Duncan A. Hydrolysis of glucosinolates to isothiocyanates after ingestion of raw or microwaved cabbage by human volunteers. Cancer Epidemiol Biomarkers Prev 2004; 13: 125-131.
13. Combourieu B, Elfoul L, Delort AM, Rabot S. Identification of new derivatives of sinigrin and glucotropaeolin produced by the human digestive microflora using H-1 NMR spectroscopy analysis of in vitro incubations. Drug Metab Dispos 2001; 29: 1440-1445.
14. Cheng DL, Hashimoto K, Uda Y. In vitro digestion of sinigrin and glucotropaeolin by single strains of Bifidobacterium and identification of the digestive products. Food Chem Toxicol 2004; 42: 351-7.
15. Bonnesen C, Stephensen PU, Andersen O, Sorensen H, Vang O. Modulation of cytochrome P-450 and glutathione S-transferase isoform expression in vivo by intact and degraded indolyl glucosinolates. Nutr Cancer 1999; 33: 178-187.
16. Gamet-Payrastre L, Li P, Lumeau S, Cassar G, Dupont MA, et al. Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res 2000; 60: 1426-1433.
17. Visanji JM, Duthie SJ, Pirie L, Thompson DC, Padfield PJ. Dietary isothiocyanates inhibit Caco-2 cell proliferation and induce G2/M phase cell cycle arrest, DNA damage, and G2/M checkpoint activation. J Nutr 2004; 134: 3121-3126.
18. Keck AS, Qiao QY, Jeffery EH. Food matrix effects on bioactivity of broccoli-derived sulforaphane in liver and colon of F344 rats. J Agric Food Chem 2003; 51: 3320-3327.
19. Plate AYA, Gallaher DD. Effects of indole-3-carbinol and phenethyl isothiocyanate on colon carcinogenesis induced by azoxymethane in rats. Carcinogenesis 2006; 27: 287-292.
20. Rychlik J, Olejnik A, Olkowicz M, et al. Antioxidant capacity of broccoli sprouts subjected to gastrointestinal digestion. J Sci Food Agric 2014. DOI: 10.1002/jsfa.6895
21. Dinokova-Kostova AT, Talalay P. Direct and indirect antioxidant properties of inducers of cytoprotective proteins. Mol Nutr Food Res 2008; 52: S128-S138.
22. Goodrich RM, Anderson JL, Stoewsand GS. Glucosinolate changes in blanched broccoli and Brussels sprouts. J Food Process Preserv 1989; 13: 275-280.
23. Rodrigues AS, Rosa EAS. Effect of post-harvest treatments on the level of glucosinolates in broccoli. J Sci Food Agric 1999; 79: 1028-1032.
24. Vallejo F, Tomas-Barberan FA, Garcia-Viguera C. Glucosinolates and vitamin C content in edible parts of broccoli florets after domestic cooking. Eur Food Res Technol 2002; 215: 310-316.
25. Benner M, Geerts RFR, Linnemann AR, Jongen WMF, Folstar P, Cnossen HJ. A chain information model for structured knowledge management: towards effective and efficient food product improvement. Trends Food Sci Tech 2003; 14: 469-477.
26. Matusheski NV, Juvik JA, Jeffery EH. Heating decreases epithiospecifier protein activity and increases sulforaphane formation in broccoli. Phytochemistry 2004; 65: 1273-1281.
27. Rungapamestry V, Duncan AJ, Fuller Z, Ratcliffe B. Effect of meal composition and cooking duration on the fate of sulforaphane following consumption of broccoli by healthy human subjects. Br J Nutr 2007; 97: 644-52.
28. Bongoni R, Verkerk R, Dekker M, Steenbekkers LPA. Consumer behaviour towards vegetables: a study on domestic processing of broccoli and carrots by Dutch households. J Hum Nutr Diet 2014. DOI: 10.1111/jhn.12245 [Epub ahead of print]
29. Ratcliffe B, Collins AR, Glass HJ, Hillman K. The effect of physical processing on the protective effect of broccoli in relation to damage to DNA in colonocytes. In Natural Antioxidants and Anticarcinogens in Nutrition, Health and Disease. Kumpulainen J. T, Salonen JT (eds). The Royal Society of Chemistry: Cambridge, UK, 1999; 440-442.
30. Ratcliffe B, Collins AR, Glass HJ, Hillman K, Kemble RT. The effect of cooking on the protective effect of broccoli against DNA damage in colonocytes. In Dietary Anticarcinogens and Antimutagens-Chemical and Biological Aspects. Johnson IT, Fenwick GR (eds). The Royal Society of Chemistry: Cambridge, UK, 2000; 161-164.
31. Zhu N, Soendergaard M, Jeffery EH, Lai RH. The impact of loss of myrosinase on the bioactivity of broccoli products in F344 rats. J Agric Food Chem 2010; 58: 1558-1563.
32. IARC. Fruit and vegetables. IARC Handbooks of Cancer Prevention No. 8. Vainio H, Bianchini F (eds). IARC Press: Lyon, 2003.
33. Mintel. Frozen and canned fruit and vegetables in the UK-June 2007. [online] Mintel Group. Retail Intelligence Reports from Mintel, last accessed 10 January 2010. (2007). Available from http://report.mintel.com.
34. Galgano F, Favati F, Caruso M, Peitrafesa A, Natella S. The influence of processing and preservation on the retention of health-promoting compounds in broccoli. J Food Sci 2007; 72: S130-S135.
35. Dosz EB, Jeffery EH. Commercially produced frozen broccoli lacks the ability to form sulforaphane. J Func Food 2013; 5: 987-990.
36. Shapiro TA, Fahey JW, Wade KL, et al. Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiol Biomarkers Prev 2001; 10: 501-508.
37. Rungapamestry V, Duncan AJ, Fuller Z, Ratcliffe B. Changes in glucosinolate concentrations, myrosinase activity and production of metabolites of glucosinolates in cabbage (Brassica oleracea var. capitata) cooked for different durations. J Agric Food Chem 2006; 54: 7628-7634.
38. Brendler-Schwaab S, Hartman A, Pfuhler S, Speit G. The in vivo comet assay: use and status in genotoxicity testing. Mutagenesis 2005; 20: 245-54.
39. Nijhoff WA, Peters WHM. Induction of rat hepatic and intestinal glutathione S-transferase by dietary butylated hydroxyanisole. Biochem Pharmacol 1992; 44: 596-600.
40. Pearce RE, McIntyre CJ, Madan A, Sanzgiri U, Draper AJ, et al. Effects of freezing, thawing, and storing human liver microsomes on cytochrome P450 activity. Arch Biochem Biophys 1996; 331: 145-169.
41. Ross MA. Determination of ascorbic acid and uric acid in plasma by high performance liquid chromatography. J Chromatogr B Biomed Appl 1994; 657: 197-200.
42. Hess D, Keller HE, Oberlin B, Bonfanti R, Schuep W. Simultaneous determination of retinol, tocopherols, carotenoids and lycopene in plasma by means of high-performance liquid chromatography on reversed phase. Int J Vitam Nutr Res 1991; 61: 232-238.
43. Collins A, Dušinská M, Franklin M, et al. Comet assay in human biomonitoring studies: reliability, validation, and applications. Env Mol Mutagen 1997; 30: 139-146.
44. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-275.
45. Ohnishi TS, Barr JK. A simplified method of quantitating protein using the biuret and phenol reagents. Anal Biochem 1978; 86: 193-200.
46. Matsubara T, Koike M, Touchi A, Tochino Y, Sugeno K. Quantitative determination of cytochrome P-450 in rat liver homogenate. Anal Biochem 1976; 75: 596-603.
47. Burke MD, Thompson S, Elcombe CR, Halpert J, Haaparanta T, et al. Ethoxy-, pentoxy- and benzyloxyphenoxazones and homologues: a series of substrates to distinguish between different induced cytochromes P-450. Biochem Pharmacol 1985; 34: 3337-3345.
48. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974; 249: 7130-7139.
49. Ernster L. DT diaphorase. Meth Enzymol 1967; 10: 309-317.
50. Benson AM, Hunkeler MJ, Talalay P. Increase of NAD(P)H:quinone reductase by dietary antioxidants: possible role in protection against carcinogenesis and toxicity. Proc Natl Acad Sci U S A 1980; 77: 5216-5220.
51. Baasanjav-Gerber C, Monien BH, Mewis I, Schreiner M, Barillari J, et al. Identification of glucosinolate congeners able to form DNA adducts and to induce mutations upon activation by myrosinase. Mol Nutr Food Res 2011; 55: 783-792.
52. Kushad MM, Brown AF, Kurilich AC, Juvik JA, Klein BP, et al. Variation of glucosinolates in vegetable crops of Brassica oleracea. J Agric Food Chem 1999; 47: 1541-1548.
53. Vang O, Frandsen H, Hansen KT, Sorensen JN, Sorensen H, et al. Biochemical effects of dietary intakes of different broccoli samples. I. Differential modulation of cytochrome P-450 activities in rat liver, kidney and colon. Metabolism 2001; 50: 1123-1129.
54. Vallejo F, Tomas-Barberan F, Garcia-Viguera C. Health-promoting compounds in broccoli as influenced by refrigerated transport and retail sale period. J Agric Food Chem 2003; 51: 3029-3034.
55. Sorensen M, Jensen BR, Poulsen HE, Deng XS, Tygstrup N, et al. Effects of a Brussels sprouts extract on oxidative DNA damage and metabolising enzymes in rat liver. Food Chem Toxicol 2001; 39: 533-540.
56. Charron CS, Clevidence BA, Albaugh GA, Kramer MH, Vinyard BT, et al. Assessment of DNA damage and repair in adults consuming allyl isothiocyanate or Brassica vegetables. J Nutr Biochem 2013; 24: 894-902.
57. Verhagen H, Poulsen HE, Loft S, Vanpoppel G, Willems MI, et al. Reduction of oxidative DNA-damage in humans by Brussels-sprouts. Carcinogenesis 1995; 16: 969-970.
58. Verhagen H, de Vries A, Nijhoff WA, Schouten A, van Poppel G, et al. Effect of Brussels sprouts on oxidative DNA-damage in man. Cancer Lett 1997; 114: 127-130.
59. Murashima M, Watanabe S, Zhou XG, Uehara M, Kurashige A. Phase I study of multiple biomarkers for metabolism and oxidative stress after 1 week intake of broccoli sprouts. Biofactors 2004; 22: 271-275.
60. Gill CIR, Halder S, Boyd LA, Bennett R, Whitefold J, et al. Watercress supplementation in diet reduces lymphocyte DNA damage and alters blood antioxidant status in healthy adults. Am J Clin Nutr 2007; 68: 1081-1087.
61. Hoelz C, Glatt H, Meini W, Sontag G, Haidinger G, et al. 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. Mol Nutr Food Res 2008; 52: 330-341.
62. Riso P, Martini D, Visioli F, Martinetti A, Porrini M. Effect of broccoli intake on markers related to oxidative stress and cancer risk in healthy smokers and nonsmokers. Nutr Cancer 2009; 61: 232-237.
63. Loft S, Poulsen HE. Cancer risk and oxidative DNA damage in man. J Mol Med 1996; 74: 297-312.
64. Kassie F, Laky B, Gminski R, Mersch-Sundermann V, Scharf G, et al. Effects of garden and water cress juices and their constituents, benzyl and phenethyl isothiocyanates, towards benzo(a)pyrene-induced DNA damage: a model study with the single cell gel electrophoresis/Hep G2 assay. Chem-Biol Interact 2003; 142: 285-296.
65. Latte KP, Appel KE, Lampen A. Health benefits and possible risks of broccoli-an overview. Food Chem Toxicol 2011; 49: 3287-3309.
66. Saha S, Hollands W, Teucher B, Needs PW, Narbad A, et al. Isothiocyanate concentrations and interconversion of sulforaphane to erucin in human subjects after consumption of commercial frozen broccoli compared to fresh broccoli. Mol Nutr Food Res 2012; 56: 1906-1916.
67. Vallejo F, Tomas-Barberan FA, Garcia-Viguera C. Phenolic compound contents in edible parts of broccoli inflorescences after domestic cooking. J Sci Food Agric 2003; 83: 1511-1516.
68. Eberhardt MV, Kobira K, Keck AS, Juvik JA, Jeffery EH. Correlation analyses of phytochemical composition, chemical, and cellular measures of antioxidant activity of broccoli (Brassica oleracea L. Var. italica). J Agric Food Chem 2005; 53: 7421-7431.
69. Willett WC, Stampfler MJ, Underwood BA, Taylor JO, Hennekens CH. Vitamins A, E and carotene: effects of supplementation on their plasma levels. Am J Clin Nutr 1983; 38: 559-566.
70. Yen JT, Pond WG. Effect of dietary vitamin C addition on performance, plasma vitamin C and hematic iron status in weanling pigs. J Anim Sci 1981; 53: 1292-6.
71. Mahan DC, Saif LJ. Efficacy of vitamin C supplementation for weanling swine. J Anim Sci 1983; 56: 631-639.
72. Pointillart A, Denis I, Colin C, Lacroix H. Vitamin C supplementation does not modify bone mineral content or mineral absorption in growing pigs. J Nutr 1997; 127: 1514-1518.
73. Audet I, Laforest JP, Martineau GP, Matte JJ. Effect of vitamin supplements on some aspects of performance, vitamin status, and semen quality in boars. J Anim Sci 2004; 82: 626-633.
74. Mahan DC, Ching S, Dabrowski K. Developmental aspects and factors influencing the synthesis and status of ascorbic acid in the pig. Ann Rev Nutr 2004; 24: 79-103.
75. Micozzi MS, Brown ED, Edwards BK, Bieri JG, Taylor PR, et al. Plasma carotenoid response to chronic intake of selected foods and beta-carotene supplements in men. Am J Clin Nutr 1992; 55: 1120-1125.
76. Granado F, Olmedilla B, Herrero C, Perez-Sacristan B, Blanco I, et al. Bioavailability of carotenoids and tocopherols from broccoli: in vivo and in vitro assessment. Ex Biol Med 2006; 231: 1733-38.
77. Talalay P. Chemoprotection against cancer by induction of phase 2 enzymes. Biofactors 2000; 12: 5-11.
78. Keck AS, Qiao QY, Jeffery EH. Food matrix effects on bioactivity of broccoli-derived sulforaphane in liver and colon of F344 rats. J Agric Food Chem 2003; 51: 3320-3327.
79. Hwang ES, Jeffery EH. Effects of different processing methods on induction of quinone reductase by dietary broccoli in rats. J Med Food 2004; 7: 95-99.
80. Aspry KE, Bjeldanes LF. Effects of dietary broccoli and butylated hydroxyanisole on liver-mediated metabolism of benzo[a]pyrene. Food Chem Toxicol 1983; 21: 133-142.
81. Ramsdell HS, Eaton DL. Modification of aflatoxin B1 biotransformation in vitro and DNA binding in vivo by dietary broccoli in rats. J Toxicol Environ Health 1988; 25: 269-284.
82. Nerurkar PV, Park SS, Thomas PE, Nims RW, Lubet RA. Methoxyresorufin and benzyloxyresorufin-substrates preferentially metabolized by cytochrome-P4501a2 and cytochrome-2b, respectively, in the rat and mouse. Biochem Pharmacol 1993; 46: 933-943.
83. Zamaratskaia G, Zlabek V. EROD and MROD as markers of cytochrome P450 1A activities in hepatic microsomes from entire and castrated male pigs. Sensors 2009; 9: 2134-2147.
84. Kall MA, Vang O, Clausen J. Effects of dietary broccoli on human in vivo drug metabolising enzymes: evaluation of caffeine, oestrone and chlorzoxazone metabolism. Carcinogenesis 1996; 17: 793-799.
85. Amon M, Dobeic M, Misselbroook TH, Pain BF, Phillips VR, Sneath RW. A farm scale study on the use of De-Odorase® for reducing odour and ammonia emissions from intensive fattening piggeries. Bioresource Technol 1995; 51: 163-169.