β-Glucuronidase in human intestinal microbiota is necessary for the colonic genotoxicity of the food-borne carcinogen 2-amino-3-methylimidazo[4,5-f]quinoline in rats

Carcinogenesis

Volumn 28, Issue 11, 2007, Pages 2419-2425

  Humblot, Christèle ^a,c   Murkovic, Michaël ^b   Rigottier Gois, Lionel ^a   Bensaada, Martine ^a   Bouclet, Anthony ^a   Andrieux, Claude ^a   Anba, Jamila ^a   Rabot, Sylvie ^a  

^a CEMAGREF   (France)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 3 METHYLIMIDAZO[4,5 F]QUINOLINE; BETA GLUCURONIDASE; CARCINOGEN; GLUCURONOSYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; CARCINOGENICITY; CHEMICAL STRUCTURE; COLORECTAL CANCER; COMET ASSAY; CONTROLLED STUDY; COOKING; DEFECATION; ENZYME DEFICIENCY; ESCHERICHIA COLI; FEEDING; FISH; FOOD CONTAMINATION; GASTROINTESTINAL ABSORPTION; GENOTOXICITY; GLUCURONIDATION; GNOTOBIOTICS; IN VIVO STUDY; INTELLIGENCE QUOTIENT; INTESTINE CELL; INTESTINE FLORA; LIVER CELL; LIVER METABOLISM; MALE; MEAT; NONHUMAN; PRIORITY JOURNAL; RAT; TOXICOKINETICS; URINARY EXCRETION; WILD TYPE;

ANIMALS; BACTERIA; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLON; COMET ASSAY; FECES; GLUCURONIDASE; HUMANS; INTESTINES; MALE; MASS SPECTROMETRY; MUTAGENS; QUINOLINES; RATS; RATS, INBRED F344;

EID: 36148986482     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgm170     Document Type: Article

References (46)

1. Norat,T. et al. (2001) Meat consumption and colorectal cancer: A review of epidemiologic evidence. Nutr. Rev., 59, 37-47.
2. Augustsson,K. et al. (1999) Dietary heterocyclic amines and cancer of the colon, rectum, bladder, and kidney: A population-based study. Lancet, 353, 703-707.
3. Adamson,R.H. (2000) Carcinogenicity in animals and specific organs. II. Non human primates. In Nagao,M. and Sugimura,T. (eds.) Food Borne Carcinogens. Wiley, New York, pp. 31-71.
4. Ohgaki,H. (2000) Carcinogenicity in animals and specific organs. I. Rodents. In Nagao,M. and Sugimura,T (eds.) Food Borne Carcinogens. Wiley, New York, pp. 198-228.
5. Hirayama,K. et al. (2000) Effects of human intestinal flora on mutagenicity of and DNA adduct formation from food and environmental mutagens. Carcinogenesis, 21, 2105-2111.
6. Kassie,F. et al. (2001) Intestinal microflora. plays a crucial role in the genotoxicity of the cooked food mutagen 2-amino-3-methylimidazo [4,5-f] quinoline. Carcinogenesis, 22, 1721-1725.
7. Knasmüller,S. et al. (2001) Impact of bacteria in dairy products and of the intestinal microflora on the genotoxic and carcinogenic effects of hetero-cyclic aromatic amines. Mutat. Res. 480-481, 129-138.
8. Tavan,E. et al. (2002) Effects of dairy products on heterocyclic aromatic amine-induced rat colon carcinogenesis. Carcinogenesis, 23, 477-483.
9. Zsivkovits,M. et al. (2003) Prevention of heterocyclic amine-induced DNA damage in colon and liver of rats by different Lactobacillus strains. Carcinogenesis, 24, 1913-1918.
10. Bashir,M. et al. (1987) Anaerobic metabolism of 2-amino-3-methyl-3-methyl-3H-imidazo[4,5-f]quinoline (IQ) by human fecal flora. Mutat. Res., 190, 187-190.
11. Humblot,C. et al. (2005) 1H nuclear magnetic resonance spectroscopy-based studies of the metabolism of food-borne carcinogen 2-amino-3-methylimidazo[4,5-fquinoline by human intestinal microbiota. Appl. Environ. Microbiol., 71, 5116-5123.
12. Carman,R.J. et al. (1988) Conversion of IQ, a dietary pyrolysis carcinogen to a direct-acting mutagen by normal intestinal bacteria of humans. Mutat. Res., 206, 335-342.
13. Weisburger,J.H. et al. (1994) Genotoxicity and carcinogenicity in rats and mice of 2-amino-3,6-dihydro-3-methyl-7H-imidazolo[4,5-f quinolin-7-one: An intestinal bacterial metabolite of 2-amino-3-methyl-3H-imidazo [4,5-f]quinoline. J. Natl Cancer Inst., 86, 25-30.
14. Humblot,C. et al. (2004) Protective effect of Brussels sprouts, prebiotics and fermented milk towards IQ-induced genotoxicity in the human flora-associated F344 rat: Role of xenobiotic metabolizing enzymes and intestinal microflora. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 802, 231-237.
15. Rowland,I.R. et al. (1998) Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis, 19, 281-285.
16. Reddy,B.S. et al. (1977) Effect of high-risk diets for colon carcinogenesis on intestinal mucosal and bacterial β-glucuronidase activity in F344 rats. Cancer Res., 37, 3533-3536.
17. Jefferson,R.A. et al. (1986) β-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc. Natl Acad. Sci. USA., 83 8447-8451.
18. Novel,M. et al. (1976) Regulation of β-glucuronidase synthesis in Escherichia coli K-12: Constitutive mutants specifically derepressed for uidA expression. J. Bacteriol., 127, 406-417.
19. Datsenko,K.A. et al. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA., 97, 6640-6645.
20. Sambrook,J. et al. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
21. Lhoste,E.F. et al. (2003) The human colonic microflora influences the alterations of xenobiotic-metabolizing enzymes by catechins in male F344 rats. Food Chem Toxicol., 41, 695-702.
22. BradleyM.O. et al. (1982) Measurement by filter elution of DNA single-and double-strand breaks in rat hepatocytes: Effects of nitrosamines and γ-irradiation. Cancer Res., 42, 2592-2597.
23. Brendler,S.Y et al. (1992) In vivo and in vitro genotoxicity of several N-nitrosamines in extrahepatic tissues of the rat. Carcinogenesis, 13, 2435-2441.
24. Carter,V. et al. (2003) Isolation of Plasmodium berghei ookinetes in culture using Nycodenz density gradient columns and magnetic isolation. Malar. J., 2, 35.
25. Andrieux,C. et al. (1998) Ulva lactuca is poorly fermented but alters bacterial metabolism in rats inoculated with human faecal flora from methane and non-methane producers. J. Sci. Food Agric., 77, 25-30.
26. Lowry,O.H. et al. (1951) Protein measurement with folin phenol reagent. J. Biol. Chem., 193, 265-275.
27. Rigottier-Gois,L. et al. (2003) Fluorescent hybridisation combined with flow cytometry and hybridisation of total RNA to analyse the composition of microbial communities in human faeces using 16S rRNA probes. FEMS Microbiol. Ecol., 43, 237-245.
28. Singh,N.P. et al. (1991) A microgel electrophoresis technique for the direct quantitation of DNA damage and repair in individual fibroblasts cultured on microscope slides. Mutat. Res., 252, 289-296.
29. Helma,C. et al. (2000) A public domain image-analysis program for the single-cell gel-electrophoresis (comet) assay. Mutat. Res., 466, 9-15.
30. Kassie,F. et al. (2002) 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, 23 1155-1161.
31. Franke,A.A. et al. (1994) High-performance liquid chromatographic assay of isoflavonoids and coumestrol from human urine. J. Chromatogr B., 662, 47-60.
32. Rafter,J.J. et al. (1986) Metabolism of the dietary carcinogen TRP-P-1 in rats. Carcinogenesis, 7, 1291-1295.
33. Messner,C. et al. (2004) Evaluation of a new model system for studying the formation of heterocyclic amines. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 802, 19-26.
34. Snyderwine,E.G. et al. (1992) Metabolism of the food mmagen 2-amino-3-methylimidazo[4,5-f] quinoline in nonhuman primates undergoing carcinogen bioassay. Chem. Res. Toxicol., 5, 843-851.
35. Kestell,P. et al. (1999) Studies on the mechanism of cancer protection by wheat bran: Effects or the absorption, metabolism and excretion of the food carcinogen 2-amino-3-methylimidazo[4,5-f uinoline (IQ). Carcinogenesis, 20, 2253-2260.
36. Finegold,S.M. (1986) Normal human intestinal flora. Ann. Ist. Super. Sanitc., 22, 731-737.
37. Embola,C.W. et al. (2001) Green tea and the metabolism of 2-amino-3-methylimidazo[4,5-f] quinoline in F344 rats. Food Chem. Toxicol., 39, 629-633.
38. Embola,C.W. et al. (2001) Urinary excretion of N-OH-2-amino-3-methylimidazo[4,5-f] quinoline-N-glueuronide in F344 rats is enhanced by green tea. Carcinogenesis, 22, 1095-1098.
39. Turesky,R.J. et al. (1986) Sulfamate formation is a major route for detoxification of 2-amino-3-methylimidazo[4,5-f]quinoline in the rat. Carcinogenesis, 7, 1483-1485.
40. Luks,H.J. et al. (1989) Identification of sulfate and glucuronic acid conjugates of the 5-hydroxy derivative as major metabolites of 2-amino-3-methylimidazo[4.,5-f] quinoline in rats. Cancer Res. 49, 4407-4411.
41. McBain,A.J. et al. (1998) Ecological and physiological studies on large intestinal bacteria in relation to production of hydrolytic and reductive enzymes involved in formation of genotoxic metabolites. J. Med. Microbiol., 47, 407-416.
42. Hooper,L. et al. (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science, 291, 881-884.
43. Kaderlik,K.R. et al. (1994) Metabolic activation pathway for the formation of DNA adducts of the carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in rat extrahepatic tissues, Carcinogenesis, 15, 1703-1709.
44. Styczynski,P.B. et al. (1993) The direct glucuronidation of 2-amino-1-methyl-6-phenylimidazo[4,5-b] pyridine (PhIP) by human and rabbit liver microsomes. Chem. Res. Toxicol., 6, 846-851.
45. Van Loo,J. et al.(1999) Functional food properties of non-digestible oligosaccharides: A consensus report from the ENDO project (DGXII AIRII-CT94-1095). Br. J. Nutr., 81, 121-132.
46. Reddy,B.S. (1998) Prevention of colon cancer by pre- and probioties: evidence from laboratory studies. Br. J. Nutr., 80, S219-S223.