O6-carboxymethylguanine DNA adduct formation and lipid peroxidation upon in vitro gastrointestinal digestion of haem-rich meat

Molecular Nutrition and Food Research

Volumn 58, Issue 9, 2014, Pages 1883-1896

  Bussche, Julie Vanden ^a   Hemeryck, Lieselot Y ^a   Van Hecke, Thomas ^a   Kuhnle, Gunter G C ^b,c   Pasmans, Frank ^a   Moore, Sharon A ^d   Van de Wiele, Tom ^a   De Smet, Stefaan ^a   Vanhaecke, Lynn ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF READING   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

Author keywords

In vitro gastrointestinal digestion; Malondialdehyde; Meat consumption; N nitroso compounds; O6 carboxymethylguanine

Indexed keywords

DNA ADDUCT; GUANINE; HEME; MALONALDEHYDE; NITROSO DERIVATIVE; O(6)-CARBOXYMETHYGUANINE;

ADULT; ANALOGS AND DERIVATIVES; ANALYSIS; ANIMAL; CACO 2 CELL LINE; CHICKEN; DIGESTION; DNA ADDUCT; FECES; FEMALE; HUMAN; IN VITRO STUDY; LIPID PEROXIDATION; MALE; MEAT; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PIG;

ADULT; ANIMALS; CACO-2 CELLS; CHICKENS; DIGESTION; DNA ADDUCTS; FECES; FEMALE; GUANINE; HEME; HUMANS; IN VITRO TECHNIQUES; LIPID PEROXIDATION; MALE; MALONDIALDEHYDE; MEAT; MIDDLE AGED; NITROSO COMPOUNDS; SWINE;

EID: 84908200512     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400078     Document Type: Article

References (80)

1. Norat, T., Bingham, S., Riboli, E., Re: meat, fish, and colorectal cancer risk: the European prospective investigation into cancer and nutrition - Reply. J. Natl. Cancer Inst. 2005, 97, 1787-1788.
2. Norat, T., Chan, D., Lau, R., Aune, D., Vieira, R., The associations between food, nutrition and physical activity and the risk of colorectal cancer. WCRF/AICR Systematic Literature Review Continuous Update Project Report, Imperial College London, London, UK 2010.
3. Micha, R., Wallace, S. K., Mozaffarian, D., Red and processes meat consumption and risk of incident coronary heart disease, stroke, and diabetes mellitus: a systematic review and meta-analysis. Circulation 2010, 121, 2271-2283.
4. Pan, A., Sun, Q., Bernstein, A. M., Manson, J. E. et al., Changes in red meat consumption and subsequent risk of type 2 diabetes mellitus. JAMA Intern. Med. 2013, 173, 1328-1335.
5. Männistö, S., Kontto, J., Kataja-Toumola, M., Albanes, D. et al., High processed meat consumption is a risk factor of type 2 diabetes in the ATBC study. Br. J. Nutr. 2010, 103, 1817-1822.
6. Larsson, S. C., Orsini, N., Wolk, A., Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J. Natl. Cancer Inst. 2005, 97, 1679-1687.
7. Giovanucci, E., Metabolic syndrome, hyperinsulinemia, and colon cancer: a review. Am. J. Clin. Nutr. 2007, 86, 836S-842S.
8. Bingham, S. A., Pignatelli, B., Pollock, J. R. A., Ellul, A. et al., Does increased endogenous formation of N-nitroso compounds in the human colon explain the association between red meat and colon cancer? Carcinogenesis 1996, 17, 515-523.
9. Hughes, R., Cross, A. J., Pollock, J. R. A., Bingham, S., Dose-dependent effect of dietary meat on endogenous colonic N-nitrosation. Carcinogenesis 2001, 22, 199-202.
10. Bingham, S. A., Hughes, R., Cross, A. J., Effect of white versus red meat on endogenous N-nitrosation in the human colon and further evidence of a dose response. J. Nutr. 2002, 132, 3522s-3525s.
11. Lombardi-Boccia, G., Martinez-Dominguez, B., Aguzzi, A., Total heme and non-heme iron in raw and cooked meats. J. Food Sci.: Food Chem. Toxicol. 2002, 67, 1738-1741.
12. Cross, A. J., Pollock, J. R. A., Bingham, S. A., Haem, not protein or inorganic iron, is responsible for endogenous intestinal N-nitrosation arising from red meat. Cancer Res. 2003, 63, 2358-2360.
13. Bonnett, R., Charalambides, A. A., Martin, R. A., Sales, K. D. et al., Reactions of nitrous acid and nitric oxide with porphyrins and haems. Nitrosylhaems as nitrosating agents. J. Chem. Soc., Chem. Commun. 1975, 21, 884-885.
14. Corpet, D. E., Red meat and colon cancer: should we become vegetarians, or can we make meat safer? Meat Sci. 2011, 89, 310-316.
15. Mirvish, S. S., Formation of N-nitroso compounds: chemistry, kinetics, and in vivo occurrence. Toxicol. Appl. Pharmacol. 1975, 31, 325-351.
16. 6-methylguanine in DNA. Cancer Res. 1997, 57, 366-369.
17. 4-carboxymethylthymidine and their formation in DNA. Nucleic Acids Res. 2009, 37, 336-345.
18. 6-methyl-2'-deoxyguanosine in DNA exposed to nitrosated glycine derivatives using a combined immunoaffinity/HPLC method. Chem. Res. Toxicol. 1999, 12, 106-111.
19. 6-carboxymethyl-2'-deoxyguanosine in DNA following reaction of nitric oxide with glycine and in human blood DNA using a quantitative immunoslot blot assay. Chem. Res. Toxicol. 2004, 17, 294-300.
20. Mirvish, S. S., Role of N-nitroso compounds (NOC) and N-nitrosation in etiology of gastric, esophageal, nasopharyngeal and bladder cancer and contribution to cancer of known exposures to NOC. Cancer Lett. 1995, 93, 17-48.
21. Challis, B. C., Chemistry and biology of nitrosated peptides. Cancer Surv. 1989, 8, 363-384.
22. Hall, C. N., Badawi, A. F., O'Connor, P. J., Saffhill, R., The detection of alkylation damage in the DNA of human gastrointestinal tissues. Br. J. Cancer 1991, 64, 59-63.
23. Lewin, M. H., Bailey, N., Bandaletova, T., Bowman, R. et al., Red meat enhances the colonic formation of the DNA adduct O-6-carboxymethyl guanine: implications for colorectal cancer risk. Cancer Res. 2006, 66, 1859-1865.
24. Moore, S. A., Xeniou, O., Zeng, Z. T. T., Humphreys, E. et al., Optimizing immunoslot blot assays and application to low DNA adduct levels using an amplification approach. Anal. Biochem. 2010, 403, 67-73.
25. Nair, U., Bartsch, H., Nair, J., Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. Free Radic. Biol. Med. 2007, 43, 1109-1120.
26. Phillips, D. H., Arlt, V. M., The P-32-postlabeling assay for DNA adducts. Nat. Protoc. 2007, 2, 2772-2281.
27. van Sittert, N. J., Boogaard, P. J., Natarajan, A. T., Tates, A. D. et al., Formation of DNA adducts and induction of mutagenic effects in rats following 4 weeks inhalation exposure to ethylene oxide as a basis for cancer risk assessment. Mutat. Res. 2000, 447, 27-48.
28. 6-methyl-2'-deoxyguanosine DNA adducts: relevance for gastrointestinal cancer. Carcinogenesis 2007, 28, 356-362.
29. Farmer, P. B., Brown, K., Tompkins, E., Emms, V. L. et al., DNA adducts: mass spectrometry methods and future prospects. Toxicol. Appl. Pharmacol. 2005, 207, 293-301.
30. Singh, R., Farmer, P. B., Liquid chromatography-electrospray ionization-mass spectrometry: the future of DNA adduct detection. Carcinogenesis 2006, 27, 178-196.
31. Himmelstein, M. W., Boogaard, P. J., Cadet, J., Farmer, P. B. et al., Creating context for the use of DNA adduct data in cancer risk assessment: II. Overview of methods of identification and quantitation of DNA damage. Crit. Rev. Toxicol. 2009, 39, 679-694.
32. 6-methylguanine adducts in DNA by liquid chromatography-positive electrospray tandem mass spectrometry. J. Chrom. B 2006, 833, 141-148.
33. 6-carboxymethylguanine DNA adducts in intestinal cell lines. J. Chromatogr. A 2012, 1257, 25-33.
34. Niki, E., Lipid peroxidation: physiological levels and dual biological effects. Free Radic. Biol. Med. 2009, 47, 469-484.
35. Del Rio, D., Stewart, A. J., Pellegrini, N., A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr. Metab. Cardiovasc. Dis. 2005, 15, 316-328.
36. Marnett, L. J., Oxy radicals, lipid peroxidation and DNA damage. Toxicology 2002, 181-182, 219-222.
37. Grotto, D., Santa Maria, L. D., Boeira, S., Valentini, J. et al., Rapid quantification of malondialdehyde in plasma by high performance liquid chromatography-visible detection. J. Pharm. Biomed. Anal. 2007, 43, 619-624.
38. Knight, J. A., Pieper, R. K., McClellan, L., Specificity of the thiobarbituric acid reaction: its use in studies of lipid peroxidation. Clin. Chem. 1988, 34, 2433-2438.
39. Van de Wiele, T., Vanhaecke, L., Boeckaert, C., Peru, K. et al., Human colon microbiota transform polycyclic aromatic hydrocarbons to estrogenic metabolites. Environ. Health Perspect. 2005, 113, 6-10.
40. Hornsey, H. C., The color of cooked cured pork. I. Estimation of the nitric oxide-haem pigments. J. Sci. Food Agr. 1956, 7, 534-540.
41. Jonas, C. R., Estivariz, C. F., Jones, D. P., Gu, L. H. et al., Keratinocyte growth factor enhances glutathione redox state in rat intestinal mucosa during nutritional repletion. J. Nutr. 1999, 129, 1278-1284.
42. Ishiyama, M., Tominaga, H., Shiga, M., Sasamoto, K. et al., A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Biol. Pharm. Bull. 1996, 19, 1518-1520.
43. Slater, T. F., Sawyer, B., Sträuli, U., Studies on succinate-tetrazolium reductase systems. III. Points of coupling of four different tetrazolium salts. Biochim. Biophys. Acta 1963, 77, 383-393.
44. Carlson, M. A., Technical note: assay of cell quantity in the fibroblast-populated collagen matrix with a tetrazolium reagent. Eur. Cells Mater. 2006, 12, 44-48.
45. Kuhnle, G. G., Story, G. W., Reda, T., Mani, A. R. et al., Diet-induced endogenous formation of nitroso compounds in the GI tract. Free Radic. Biol. Med. 2007, 43, 1040-1047.
46. Sawa, T., Akaike, T., Kida, K., Fukushima, Y. et al., Lipid peroxyl radicals from oxidized oils and heme-iron: implication of a high-fat diet in colon carcinogenesis. Cancer Epidemiol. Biomarkers Prev. 1998, 7, 1007-1012.
47. Bastide, N. M., Pierre, F. H., Corpet, D. E., Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev. Res. 2011, 4, 177-184.
48. Cummings, J. H., Short chain fatty acids in the human colon. Gut 1981, 22, 763-779.
49. Massay, R. C., Key, P. E., Mallett, A. K., Rowland, I. R., An investigation of the endogenous formation of apparent total N-nitroso compounds in conventional microflora and germ-free rats. Food Chem. Toxicol. 1988, 26, 595-600.
50. Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M. et al., The human microbiome project. Nature 2007, 449, 804-810.
51. Leach, S. A., Thompson, M., Hill, M., Bacterially catalysed N-nitrosation reactions and their relative importance in the human stomach. Carcinogenesis 1987, 8, 1907-1912.
52. Engemann, A., Focke, C., Humpf, H.-U., Intestinal formation of N-nitroso compounds in the pig cecum model. J. Agric. Food Chem. 2013, 61, 998-1005.
53. Suzuki, K., Mitsuoka, T., N-nitrosamine formation by intestinal bacteria. IARC Sci. Publ. 1984, 57, 275-281.
54. Hill, M. J. (Ed.), The Role of Gut Bacteria in Human Toxicology and Pharmacology, Taylor & Francis, London 1995.
55. Sekirov, I., Russell, S. L., Antunes, I. C., Finlay, B., Gut microbiota in health and disease. Physiol. Rev. 2010, 90, 859-904.
56. Culpepper, T. B. S., Volker, M., Evidence for contributions of gut microbiota to colorectal carcinogenesis. Curr. Nutr. Rep. 2013, 2, 10-18.
57. Decroos, K., Cattoir, S., Boon, N., Verstraete, W., In vitro production of Equol by human intestinal microbiota. J. Nutr. 2004, 134, 1283S-1284S.
58. Kassie, F., Rabot, S., Kundi, M., Chabikovsky, M. et al., Intestinal microflora plays a crucial role in the genotoxicity of the cooked food mutagen 2-amino-3-methylimidazo[4, 5-f]quinolone (IQ). Carcinogenesis 2001, 22, 1721-1725.
59. Wickham, M., Faulks, R., Mills, C., In vitro digestion methods for assessing the effect of food structure on allergen breakdown. Mol. Nutr. Food Res. 2009, 53, 952-958.
60. Hur, S. J., Lim, B. O., Decker, E. A., McClements, D. J., In vitro human digestion models for food applications. Food Chem. 2011, 125, 1-12.
61. Van de Wiele, T., Gallawa, C. M., Kubachka, K. M., Creed, J. T. et al., Arsenic metabolism by human gut microbiota upon in vitro digestion of contaminated soils. Environ. Health Perspect. 2010, 118, 1004-1009.
62. Oomen, A. G., Hack, A., Minekus, M., Zeijdner, E. et al., Comparison of five in vitro digestion models to study the bioaccessibility of soil contaminants. Environ. Sci. Technol. 2002, 36, 3326-3334.
63. Stuff, J. E., Goh, E. T., Barrera, S. L., Bondy, M. L. et al., Construction of an N-nitroso database for assessing dietary intake. J. Food Compost. Anal. 2009, 22, S42-S47.
64. Manco, M., Putignani, L., Bottazzo, G. F., Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr. Rev. 2010, 31, 817-844.
65. O'Driscoll, M., Macpherson, P., Xu, Y. Z., Karran, P., The cytotoxicity of DNA carboxymethylation and methylation by the model carboxymethylating agent azaserine in human cells. Carcinogenesis 1999, 20, 1855-1862.
66. 6-methylguanine in genomic DNA. Free Radical Biol. Med. 2013, 60, 41-48.
67. 6-methylguanine-DNA methyltransferase. Nucleic Acids Res. 2013, 41, 3047-3055.
68. Jerome, K. R., Sloan, D. D., Aubert, M., Measurement of CTL-induced cytotoxicity: the caspase 3 assay. Apoptosis 2003, 8, 563-571.
69. Liao, T. T., Jia, R. W., Shi, Y. L., Jia, J. W. et al., Propidium iodide staining method for testing the cytotoxicity of 2, 4, 6-trichlorophenol and perfluorooctane sulfonate at low concentrations with Vero cells. J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng. 2011, 46, 1769-1775.
70. Nosova, T., Jokelainen, K., Kaihovaara, P., Jousimies-Somer, H. et al., Aldehyde dehydrogenase activity and acetate production by aerobic bacteria representing the normal flora of human large intestine. Alcohol Alcohol. 1996, 31, 555-564.
71. Hur, S. J., Lim, B. O., Park, G. B., Joo, S. T., Effects of various fibre additions on lipid digestion during in vitro digestion of beef patties. J. Food Sci. 2009, 74, C653-C657.
72. Ijssennagger, N., Derrien, M., van Doorn, G. M., Rijnierse, A. et al., Dietary heme alters microbiota of mouse colon without changes in host-microbe cross-talk. PLoS One 2012, 7, e49868.
73. Sobko, T., Reinders, C. I., Jansson, E. A., Norin, E.et al., Gastrointestinal bacteria generate nitric oxide from nitrate and nitrite. Nitric Oxide 2005, 13, 272-278.
74. Darley-Usmar, V., Wiseman, H., Halliwell, B., Nitric oxide and oxygen radicals: a question of balance. FEBS Lett. 1995, 2-3, 131-135.
75. Amate, L., Gil, A., Ramirez, M., Dietary long-chain polyunsaturated fatty acids from different sources affect fat and fatty acid excretions in rats. Am. J. Nutr. 2001, 131, 3216-3221.
76. Walker, A. W., Duncan, S. H., Leitch, E. C. M., Child, M. W. et al., pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol. 2005, 71, 3692-3700.
77. Barcenilla, A., Pryde, S. E., Martin, J. C., Duncan, S. H. et al., Phylogenetic relationships of dominant butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 2000, 66, 1654-1661.
78. Csordas, A., Butyrate, aspirin and colorectal cancer. Eur. J. Cancer Prev. 1996, 5, 221-231.
79. McIntyre, A., Gibson, P. R., Young, G. P., Butyrate production from dietary fiber and protection against large bowel cancer in a rat model. Gut 1993, 34, 386-391.
80. Janero, D. R., Burghardt, B., Thiobarbituric acid-reactive malondialdehyde formation during superoxide-dependent, iron-catalyzed lipid peroxidation: influence of peroxidation conditions. Lipids 1989, 24, 125-131.