Combined Genotoxic Effects of a Polycyclic Aromatic Hydrocarbon (B(a)P) and an Heterocyclic Amine (PhIP) in Relation to Colorectal Carcinogenesis

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Jamin, Emilien L ^a,b   Riu, Anne ^a,b   Douki, Thierry ^c   Debrauwer, Laurent ^a,b   Cravedi, Jean Pierre ^a,b   Zalko, Daniel ^a,b   Audebert, Marc ^a,b  

^a CEMAGREF   (France)

^b TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^c CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; HETEROCYCLIC AMINE; HISTONE H2AX;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; COLORECTAL CANCER; CONTROLLED STUDY; CYTOTOXICITY; DISEASE COURSE; DNA ADDUCT; FOOD INTAKE; GENOTOXICITY; HETEROZYGOSITY; LIMIT OF QUANTITATION; MEAT; MOUSE; NONHUMAN;

ANIMALS; BENZO(A)PYRENE; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLORECTAL NEOPLASMS; DNA ADDUCTS; HISTONES; HUMANS; IMIDAZOLES; INTESTINAL MUCOSA; MEAT; MICE; MUTAGENICITY TESTS; PHOSPHORYLATION; TANDEM MASS SPECTROMETRY;

EID: 84874585293     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058591     Document Type: Article

References (60)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, et al. (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127: 2893-2917.
2. Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, et al. (2011) Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS One 6: e20456.
3. Chao A, Thun MJ, Connell CJ, McCullough ML, Jacobs EJ, et al. (2005) Meat consumption and risk of colorectal cancer. JAMA 293: 172-182.
4. Cross AJ, Sinha R, (2004) Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ Mol Mutagen 44: 44-55.
5. Martinez ME, Jacobs ET, Ashbeck EL, Sinha R, Lance P, et al. (2007) Meat intake, preparation methods, mutagens and colorectal adenoma recurrence. Carcinogenesis 28: 2019-2027.
6. Sinha R, Peters U, Cross AJ, Kulldorff M, Weissfeld JL, et al. (2005) Meat, meat cooking methods and preservation, and risk for colorectal adenoma. Cancer Res 65: 8034-8041.
7. Nagao M, Wakabayashi K, Ushijima T, Toyota M, Totsuka Y, et al. (1996) Human exposure to carcinogenic heterocyclic amines and their mutational fingerprints in experimental animals. Environ Health Perspect 104 (Suppl 3): 497-501.
8. Toyota M, Ushijima T, Kakiuchi H, Canzian F, Watanabe M, et al. (1996) Genetic alterations in rat colon tumors induced by heterocyclic amines. Cancer 77: 1593-1597.
9. Sinha R, Kulldorff M, Gunter MJ, Strickland P, Rothman N, (2005) Dietary benzo[a]pyrene intake and risk of colorectal adenoma. Cancer Epidemiol Biomarkers Prev 14: 2030-2034.
10. Fearon ER, Vogelstein B, (1990) A genetic model for colorectal tumorigenesis. Cell 61: 759-767.
11. Narayan S, Roy D, (2003) Role of APC and DNA mismatch repair genes in the development of colorectal cancers. Mol Cancer 2: 41.
12. Steffensen IL, Paulsen JE, Eide TJ, Alexander J, (1997) 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine increases the numbers of tumors, cystic crypts and aberrant crypt foci in multiple intestinal neoplasia mice. Carcinogenesis 18: 1049-1054.
13. Marian B, (2002) In vitro models for the identification and characterization of tumor-promoting and protective factors for colon carcinogenesis. Food Chem Toxicol 40: 1099-1104.
14. Forest V, Clement M, Pierre F, Meflah K, Menanteau J, (2003) Butyrate restores motile function and actin cytoskeletal network integrity in apc mutated mouse colon epithelial cells. Nutr Cancer 45: 84-92.
15. Forest V, Pierre F, Bassonga E, Meflah K, Olivier C, et al. (2003) Apc+/Min colonic epithelial cells express TNF receptors and ICAM-1 when they are co-cultured with large intestine intra-epithelial lymphocytes. Cell Immunol 223: 70-76.
16. Pierre F, Tache S, Gueraud F, Rerole AL, Jourdan ML, et al. (2007) Apc mutation induces resistance of colonic cells to lipoperoxide-triggered apoptosis induced by faecal water from haem-fed rats. Carcinogenesis 28: 321-327.
17. Fenton JI, Hord NG, (2006) Stage matters: choosing relevant model systems to address hypotheses in diet and cancer chemoprevention research. Carcinogenesis 27: 893-902.
18. Turesky RJ, Le Marchand L, (2011) Metabolism and biomarkers of heterocyclic aromatic amines in molecular epidemiology studies: lessons learned from aromatic amines. Chem Res Toxicol 24: 1169-1214.
19. Xue W, Warshawsky D, (2005) Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol Appl Pharmacol 206: 73-93.
20. Brown K, Hingerty BE, Guenther EA, Krishnan VV, Broyde S, et al. (2001) Solution structure of the 2-amino-1- methyl-6-phenylimidazo[4,5-b]pyridine C8-deoxyguanosine adduct in duplex DNA. Proc Natl Acad Sci U S A 98: 8507-8512.
21. Bellocq D, Molina J, Rathahao E, Canlet C, Tache S, et al. (2008) High potency of bioactivation of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in mouse colon epithelial cells with Apc(Min) mutation. Mutat Res 653: 34-43.
22. Bellocq D, Molina J, Rathahao-Paris E, Tache S, Pierre F, et al. (2010) Metabolic bioactivation of oestradiol-17beta (E2beta) in mouse colon epithelial cells bearing ApcMin mutation. Steroids 75: 665-675.
23. Dingley KH, Curtis KD, Nowell S, Felton JS, Lang NP, et al. (1999) 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: 507-512.
24. Garner RC, Lightfoot TJ, Cupid BC, Russell D, Coxhead JM, et al. (1999) Comparative biotransformation studies of MeIQx and PhIP in animal models and humans. Cancer Lett 143: 161-165.
25. Turteltaub KW, Dingley KH, Curtis KD, Malfatti MA, Turesky RJ, et al. (1999) Macromolecular adduct formation and metabolism of heterocyclic amines in humans and rodents at low doses. Cancer Lett 143: 149-155.
26. Cosman M, de los Santos C, Fiala R, Hingerty BE, Singh SB, et al. (1992) Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA. Proc Natl Acad Sci U S A 89: 1914-1918.
27. Audebert M, Dolo L, Perdu E, Cravedi JP, Zalko D, (2011) Use of the gammaH2AX assay for assessing the genotoxicity of bisphenol A and bisphenol F in human cell lines. Arch Toxicol 85: 1463-1473.
28. Audebert M, Riu A, Jacques C, Hillenweck A, Jamin EL, et al. (2010) Use of the gammaH2AX assay for assessing the genotoxicity of polycyclic aromatic hydrocarbons in human cell lines. Toxicol Lett 199: 182-192.
29. Audebert M, Zeman F, Beaudoin R, Pery A, Cravedi JP, (2012) Comparative potency approach based on H2AX assay for estimating the genotoxicity of polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 260: 58-64.
30. Graillot V, Takakura N, Le Hegarat L, Fessard V, Audebert M, et al. (2012) Genotoxicity of pesticide mixtures in the diet of French population. Environ Mol Mutagen 53: 173-184.
31. Smart DJ, Ahmedi KP, Harvey JS, Lynch AM, (2011) Genotoxicity screening via the gammaH2AX by flow assay. Mutat Res 715: 25-31.
32. Watters GP, Smart DJ, Harvey JS, Austin CA, (2009) H2AX phosphorylation as a genotoxicity endpoint. Mutat Res 679: 50-58.
33. Zhou C, Li Z, Diao H, Yu Y, Zhu W, et al. (2006) DNA damage evaluated by gammaH2AX foci formation by a selective group of chemical/physical stressors. Mutat Res 604: 8-18.
34. Graillot V, Tomasetig F, Cravedi JP, Audebert M, (2012) Evidence of the in vitro genotoxicity of methyl-pyrazole pesticides in human cells. Mutat Res 748: 8-16.
35. Baradat M, Jouanin I, Dalleau S, Tache S, Gieules M, et al. (2011) 4-Hydroxy-2(E)-nonenal metabolism differs in Apc(+/+) cells and in Apc(Min/+) cells: it may explain colon cancer promotion by heme iron. Chem Res Toxicol 24: 1984-1993.
36. Jacques C, Jamin EL, Perdu E, Duplan H, Mavon A, et al. (2010) Characterisation of B(a)P metabolites formed in an ex vivo pig skin model using three complementary analytical methods. Anal Bioanal Chem 396: 1691-1701.
37. Ravanat JL, Douki T, Duez P, Gremaud E, Herbert K, et al. (2002) Cellular background level of 8-oxo-7,8-dihydro-2'-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up. Carcinogenesis 23: 1911-1918.
38. Marie C, Maitre A, Douki T, Gateau M, Tarantini A, et al. (2008) Influence of the metabolic properties of human cells on the kinetic of formation of the major benzo[a]pyrene DNA adducts. J Appl Toxicol 28: 579-590.
39. Jamin EL, Arquier D, Canlet C, Rathahao E, Tulliez J, et al. (2007) New insights in the formation of deoxynucleoside adducts with the heterocyclic aromatic amines PhIP and IQ by means of ion trap MSn and accurate mass measurement of fragment ions. J Am Soc Mass Spectrom 18: 2107-2118.
40. Rindgen D, Turesky RJ, Vouros P, (1995) Determination of in vitro formed DNA adducts of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine using capillary liquid chromatography/electrospray ionization/tandem mass spectrometry. Chem Res Toxicol 8: 1005-1013.
41. Louiz I, Kinani S, Gouze ME, Ben-Attia M, Menif D, et al. (2008) Monitoring of dioxin-like, estrogenic and anti-androgenic activities in sediments of the Bizerta lagoon (Tunisia) by means of in vitro cell-based bioassays: contribution of low concentrations of polynuclear aromatic hydrocarbons (PAHs). Sci Total Environ 402: 318-329.
42. Hakura A, Tsutsui Y, Sonoda J, Kai J, Imade T, et al. (1998) Comparison between in vivo mutagenicity and carcinogenicity in multiple organs by benzo[a]pyrene in the lacZ transgenic mouse (Muta Mouse). Mutat Res 398: 123-130.
43. Alexandrov K, Rojas M, Kadlubar FF, Lang NP, Bartsch H, (1996) Evidence of anti-benzo[a]pyrene diolepoxide-DNA adduct formation in human colon mucosa. Carcinogenesis 17: 2081-2083.
44. Steffensen IL, Alexander J, (2006) Impact of genetic background on spontaneous or 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP)-induced intestinal tumorigenesis in Min/+ mice. Cancer Lett 240: 289-296.
45. Steffensen IL, Schut HA, Paulsen JE, Andreassen A, Alexander J, (2001) Intestinal tumorigenesis in multiple intestinal neoplasia mice induced by the food mutagen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine: perinatal susceptibility, regional variation, and correlation with DNA adducts. Cancer Res 61: 8689-8696.
46. Fontana RJ, Lown KS, Paine MF, Fortlage L, Santella RM, et al. (1999) Effects of a chargrilled meat diet on expression of CYP3A, CYP1A, and P-glycoprotein levels in healthy volunteers. Gastroenterology 117: 89-98.
47. Diggs DL, Harris KL, Rekhadevi PV, Ramesh A, (2012) Tumor microsomal metabolism of the food toxicant, benzo(a)pyrene, in Apc(Min) mouse model of colon cancer. Tumour Biol 33: 1255-1260.
48. Loeppen S, Koehle C, Buchmann A, Schwarz M, (2005) A beta-catenin-dependent pathway regulates expression of cytochrome P450 isoforms in mouse liver tumors. Carcinogenesis 26: 239-248.
49. Kemp MG, Lindsey-Boltz LA, Sancar A, (2011) The DNA damage response kinases DNA-dependent protein kinase (DNA-PK) and ataxia telangiectasia mutated (ATM) Are stimulated by bulky adduct-containing DNA. J Biol Chem 286: 19237-19246.
50. Yilmaz S, Sancar A, Kemp MG, (2011) Multiple ATR-Chk1 pathway proteins preferentially associate with checkpoint-inducing DNA substrates. PLoS One 6: e22986.
51. McGregor WG, Wei D, Chen RH, Maher VM, McCormick JJ, (1997) Relationship between adduct formation, rates of excision repair and the cytotoxic and mutagenic effects of structurally-related polycyclic aromatic carcinogens. Mutat Res 376: 143-152.
52. Shimada T, Guengerich FP, (2006) Inhibition of human cytochrome P450 1A1-, 1A2-, and 1B1-mediated activation of procarcinogens to genotoxic metabolites by polycyclic aromatic hydrocarbons. Chem Res Toxicol 19: 288-294.
53. Girard H, Butler LM, Villeneuve L, Millikan RC, Sinha R, et al. (2008) UGT1A1 and UGT1A9 functional variants, meat intake, and colon cancer, among Caucasians and African-Americans. Mutat Res 644: 56-63.
54. Keating GA, Bogen KT, (2004) Estimates of heterocyclic amine intake in the US population. J Chromatogr B Analyt Technol Biomed Life Sci 802: 127-133.
55. Knize MG, Salmon CP, Pais P, Felton JS, (1999) Food heating and the formation of heterocyclic aromatic amine and polycyclic aromatic hydrocarbon mutagens/carcinogens. Adv Exp Med Biol 459: 179-193.
56. Ferrucci LM, Sinha R, Huang WY, Berndt SI, Katki HA, et al. (2012) Meat consumption and the risk of incident distal colon and rectal adenoma. Br J Cancer 106: 608-616.
57. Reeves DA, Mu H, Kropachev K, Cai Y, Ding S, et al. (2011) Resistance of bulky DNA lesions to nucleotide excision repair can result from extensive aromatic lesion-base stacking interactions. Nucleic Acids Res 39: 8752-8764.
58. Gil J, Ramsey D, Stembalska A, Karpinski P, Pesz KA, et al. (2012) The C/A polymorphism in intron 11 of the XPC gene plays a crucial role in the modulation of an individual's susceptibility to sporadic colorectal cancer. Mol Biol Rep 39: 527-534.
59. Joshi AD, Corral R, Siegmund KD, Haile RW, Le Marchand L, et al. (2009) Red meat and poultry intake, polymorphisms in the nucleotide excision repair and mismatch repair pathways and colorectal cancer risk. Carcinogenesis 30: 472-479.
60. Slyskova J, Naccarati A, Pardini B, Polakova V, Vodickova L, et al. (2012) Differences in nucleotide excision repair capacity between newly diagnosed colorectal cancer patients and healthy controls. Mutagenesis 27: 225-232.