Role of intestinal microflora in xenobiotic-induced toxicity

Molecular Nutrition and Food Research

Volumn 57, Issue 1, 2013, Pages 84-99

  Jeong, Hye Gwang ^a   Kang, Mi Jeong ^b   Kim, Hyung Gyun ^a   Oh, Do Gyeong ^b   Kim, Jin Sung ^b   Lee, Sang Kyu ^c   Jeong, Tae Cheon ^b  

^a Chungnam National University   (South Korea)

^b Yeungnam University   (South Korea)

^c Kyungpook National University   (South Korea)

Author keywords

In vitro; In vivo; Intestinal microflora; Toxicant; Xenobiotic metabolism

Indexed keywords

XENOBIOTIC AGENT;

ANIMAL; ANIMAL MODEL; DRUG DETOXIFICATION; HUMAN; INTESTINE; METABOLISM; MICROBIOLOGY; REVIEW;

ANIMALS; HUMANS; INTESTINES; METABOLIC DETOXICATION, DRUG; MODELS, ANIMAL; XENOBIOTICS;

EID: 84872147459     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200461     Document Type: Review

References (78)

1. Gorbach, S. L., Nahas, L., Lerner, P. I., Weinstein, L., Studies of intestinal microflora. Gastroenterology 1967, 53, 845-855.
2. Human Microbiome Project Consortium, Structure, function and diversity of the healthy human microbiome. Nature 2012, 486, 207-214.
3. Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I. et al., Human gut microbiome viewed across age and geography. Nature 2012, 486, 222-227.
4. Kim, B. S., Kim, J. N., Cerniglia, C. E., In vitro culture conditions for maintaining a complex population of human gastrointestinal tract microbiota. J. Biomed. Biotechnol. 2011, 2011, 838040.
5. Ley, R. E., Peterson, D. A., Gordon, J. I., Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006, 124, 837-838.
6. Blaut, M., Braune, A., Wunderlich, S., Sauer, P. et al., Mutagenicity of arbutin in mammalian cells after activation by human intestinal bacteria. Food Chem. Toxicol. 2006, 44, 1940-1947.
7. Bjorkholm, B., Bok, C. M., Lundin, A., Rafter, J. et al., Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS One 2009, 4, e6958.
8. Sousa, T., Paterson, R., Moore, V., Carlsson, A. et al., The gastrointestinal microbiota as a site for the biotransformation of drugs. Int. J. Pharm. 2008, 363, 1-25.
9. Jin, M. J., Kim, U., Kim, I. S., Kim, Y. et al., Effects of gut microflora on pharmacokinetics of hesperidin: a study on non-antibiotic and pseudo-germ-free rats. J. Toxicol. Environ. Health A 2010, 73, 1441-1450.
10. Khanal, T., Kim, H. G., Hwang, Y. P., Kong, M. J. et al., Role of metabolism by the human intestinal microflora in arbutin-induced cytotoxicity in HepG2 cell cultures. Biochem. Biophys. Res. Commun. 2011, 413, 318-324.
11. Khanal, T., Kim, H. G., Choi, J. H., Park, B. H. et al., Protective role of intestinal bacterial metabolism against baicalin-induced toxicity in HepG2 cell cultures. J. Toxicol. Sci. 2012, 37, 363-371.
12. Khanal, T., Kim, H. G., Choi, J. H., Do, M. T. et al., Biotransformation of geniposide by human intestinal microflora on cytotoxicity against HepG2 cells. Toxicol. Lett. 2012, 209, 246-254.
13. Khanal, T., Kim, H. G., Jin, S. W., Shim, E. et al., Protective role of metabolism by intestinal microflora in butyl paraben-induced toxicity in HepG2 cells cultures. Toxicol. Lett. 2012, 213, 174-183.
14. Gingell, R., Bridges, J. W., Intestinal azo reduction and glucuronide conjugation of prontosil. Biochem. J. 1971, 125, 24.
15. Kim, Y. S., Kim, J. J., Cho, K. H., Jung, W. S. et al., Biotransformation of ginsenoside Rb1, crocin, amygdalin, geniposide, puerarin, ginsenoside Re, hesperidin, poncirin, glycyrrhizin, and baicalin by human fecal microflora and its relations to cytotoxicity against tumor cells. J. Microbiol. Biotechnol. 2008, 18, 1109-1114.
16. Smith, G. E., Griffiths, L. A., Metabolism of N-acetylated and O-alkylated drugs by the intestinal microflora during anaerobic incubation in vitro. Xenobiotica 1974, 4, 477-487.
17. Holt, R., The bacterial degradation of chloramphenicol. Lancet 1967, 1, 1259-1260.
18. Kataoka, K., Kinouchi, T., Akimoto, S., Ohnishi, Y., Bioactivation of cysteine conjugates of 1-nitropyrene oxides by cysteine conjugate β-lyase purified from Peptostreptococcus magnus. Appl. Environ. Microbiol. 1995, 61, 3781-3787.
19. Okuda, H., Nishiyama, T., Ogura, K., Nagayama, S. et al., Lethal drug interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. Drug Metab. Dispos. 1997, 25, 270-273.
20. Okuda, H., Ogura, K., Kato, A., Takubo, H. et al., A possible mechanism of eighteen patient deaths caused by interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. J. Pharmacol. Exp. Ther. 1998, 287, 791-799.
21. Bashir, M., Kingston, D. G., Carman, R. J., Van Tassell, R. L. et al., Anaerobic metabolism of 2-amino-3-methyl-3H-imidazo[4, 5-f]quinoline (IQ) by human fecal flora. Mutat. Res. 1987, 190, 187-190.
22. Carman, R. J., Van Tassell, R. L., Kingston, D. G., Bashir, M. et al., Conversion of IQ, a dietary pyrolysis carcinogen to a direct-acting mutagen by normal intestinal baceteria of humans. Mutat. Res. 1988, 206, 335-342.
23. Rummey, C. J., Rowland, I. R., O'Neill, I.K., Conversion of IQ to 7-OHIQ by gut microflora. Nutr. Cancer 1993, 19, 67-76.
24. 1H nuclear magnetic resonance spectroscopy-based studies of the metabolism of food-borne carcinogen 2-amino-3-methylimidazo[4, 5-f]quinoline by human intestinal microbiota. Appl. Environ. Microbiol. 2005, 71, 5116-5123.
25. Van Tassel, R. L., Kingston, D. G., Wilkins, T. D., Metabolism of dietary genotoxins by the human colonic microflora: the fecapentaenes and heterocyclic amines. Mutat. Res. 1990, 238, 209-221.
26. Deisinger, P. J., Hill, T. S., English, J. C., Human exposure to naturally occurring hydroquinone. J. Toxicol. Environ. Health 1996, 47, 31-46.
27. Kang, M. J., Ha, H. W., Kim, H. G., Lee, D. H. et al., Role of metabolism by intestinal bacteria in arbutin-induced toxicity in vitro. Arch. Pharm. Res. 2011, 34, 687-693.
28. Kang, M. J., Ha, H. W., Kim, G. H., Lee, S. K. et al., Role of metabolism by intestinal bacteria in arbutin-induced suppression of lymphoproliferative response in vitro. Biomol. Ther. 2012, 20, 196-200.
29. Tamura, G., Gold, C., Ferro-Luzzi, A., Ames, B. N. et al., A model for activation of dietary glycosides to mutagens by intestinal flora. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 4961-4965.
30. Kim, D. H., Yu, K. U., Bae, E. A., Han, M. J., Metabolism of puerarin and daidzin by human intestinal bacteria and their relation to in vitro cytotoxicity. Biol. Pharm. Bull. 1998, 21, 628-630.
31. Kang, M. J., Khanal, T., Kim, H. G., Lee, D. H. et al., Role of metabolism by human intestinal microflora in geniposide-induced toxicity in HepG2 cells. Arch. Pharm. Res. 2012, 35, 733-738.
32. Kinuchi, T., Kataoka, K., Miyanishi, K., Akimoto, S. et al., Role of intestinal microflora in metabolism of glutathione conjugates of 1-nitropyrene 4, 5-oxide and 1-nitropyrene 9, 10-oxide. Tohoku J. Exp. Med. 1992, 168, 119-122.
33. Yeo, H. K., Hyun, Y. J., Jang, S. E., Han, M. J. et al. Development of fecal microbial enzyme mix for mutagenicity assay of natural products. J. Microbiol. Biotechnol. 2012, 22, 838-848.
34. Upadhaya, S. D., Sung, H. G., Lee, C. H., Lee, S. Y. et al., Comparative study on the aflatoxin B1 degradation ability of rumenfluid from Holstein steers and Korean native goats. J. Vet. Sci. 2009, 10, 29-34.
35. 1. J. Agric. Food Chem. 1998, 46, 2707-2713.
36. Wong, J. J., Hsieh, D. P. H., Mutagenicity of aflatoxins related to their metabolism and carcinogenic potential. Proc. Natl. Acad. Sci. U.S.A. 1976, 73, 2241-2244.
37. Young, J. C., Zhou, T., Yu, H., Zhu, H. et al., Degradation of trichothecene mycotoxins by chicken intestinal microbes. Food Chem. Toxicol. 2007, 45, 136-143.
38. Kollarczik, B., Gareis, M., Hanelt, M., In vitro transformation of the Fusarium mycotoxins deoxynivalenol and zearalenone by the normal gut microflora of pigs. Natural Toxin. 1994, 2, 105-110.
39. King, L. C., Kohan, J., Geroge, S. E., Lewtas, J. et al., Metabolism of 1-nitropyrene by human, rat, and mouse intestinal flora: mutagenicity of isolated metabolism by direct analysis of HPLC fractions with a microsuspension reverse mutation assay. J. Toxicol. Environ. Health 1990, 31, 179-192.
40. Manning, B. W., Cerniglia, C. E., Federle, T. W., Biotransformation of 1-nitropyrene to 1-aminopyrene and N-formyl-1-aminopyrene by the human intestinal microbiota. J. Toxicol. Environ. Health 1986, 18, 339-346.
41. Ei-Bayoumy, K., Sharma, C., Louis, Y. M., Reddy, B. et al., The role of intestinal microflora in the metabolic reduction of 1-nitropyrene to 1-aminopyrene in conventional and germ-free rats and in humans. Cancer Lett. 1983, 19, 311-316.
42. Howard, P. C., Beland, F. A., Cerniglia, C. E., Reduction of the carcinogen 1-nitropyrene to 1-aminopyrene by rat intestinal bacteria. Carcinogenesis 1983, 4, 985-990.
43. Hult, K., Teiling, A., Gatenbeck, S., Degradation of ochratoxin A by a ruminant. Appl. Environ. Microbiol. 1976, 32, 443-444.
44. Schatzmayr, G., Zehner, F., Täubel, M., Schatzmayr, D. et al., Microbiologicals for deactivating mycotoxins. Mol. Nutr. Food Res. 2006, 50, 543-551.
45. Fuchs, S., Sontag, G., Stidl, R., Ehrlich, V., et al., Detoxification of patulin and ochratoxin A, two abundant mycotoxins, by lactic acid bacteria. Food Chem. Toxicol. 2008, 46, 1398-1407.
46. Allison, M. J., Cook, H. M., Milne, D. B., Gallagher, S., Oxalate degradation by gastrointestinal bacteria from humans. J. Nutr. 1986, 116, 455-460.
47. Daniel, S. L., Hartman, P. A., Allison, M. J., Microbial degradation of oxalate in the gastrointestinal tracts of rats. Appl. Environ. Microbiol, 1987, 53, 1793-1797.
48. Hirayama, K., Baranczewski, P., Åkerlund, J. E., Midtvedt, T. et al., Effects of human intestinal flora on mutagenicity of and DNA adduct formation from food and environmental mutagens. Carcinogenesis 2000, 21, 2105-2111.
49. Kassie, F., Rabot, S., Kundi, M., Chabicovsky, M. et al., Intestinal microflora plays a crucial role in the genotoxicity of the cooked food mutagen 2-amino-3-methylimidazo[4, 5-f]quinoline (IQ). Carcinogenesis 2001, 22, 1721-1725.
50. Kassie, F., Lhoste, E. F., Bruneau, A., Zsivkovits, M., Effect of intestinal microflora from vegetarians and meat eaters on the genotoxicity of 2-amino-3-methylimidazo[4, 5-f]quinolin, a carcinogenic heterocyclic amine. J. Chromatogr. B 2004, 802, 211-215.
51. Humblot, C., Murkovic, M., Rogottier-Gois, L., Bensaada, M. et al., β-Glucuronidase in human intestinal microbiota is necessary for the colonic genotoxicity of the food-borne carcinogen 2-amino-3-methylimidazo[4, 5-f]quinolone in rats. Carcinogenesis 2007, 28, 2419-2425.
52. Weisburger, J. H., Rivenson, A., Reinhardt, J., Aliaga, C. et al., 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. 1994, 86, 25-30.
53. Carter, J. H., McLafferty, M. A., Goldman, P., Role of the gastrointestinal microflora in amygdalin (laetrile)-induced cyanide toxicity. Biochem. Pharmacol. 1980, 29, 301-304.
54. Reddy, B. S., Narisawa, T., Wright, P., Vukusich, D. et al., Colon carcinogenesis with azoxymethane and dimethylhydrazine in germ-free rats. Cancer Res. 1975, 35, 287-290.
55. Reddy, B. S., Narisawa, T., Weisburger, J. H., Colon carcinogenesis in germ-free rats with intrarectal 1, 2-dimethylhydrazine and subcutaneous azoxymethane. Cancer Res. 1976, 36, 2874-2876.
56. Takada, H., Hirooka, T., Hiramatsu, Y., Yamamoto, M., Effect of β-glucuronidase inhibitor on azoxymethane-induced colonic carcinogenesis in rats. Cancer Res. 1982, 42, 331-334.
57. Huber, B., Dammann, P., Krüger, C., Kirsch, P. et al., Production of toxic volatile trimethylbismuth by the intestinal microbiota of mice. J. Toxicol. 2011, 2011, 491039.
58. Wheeler, L. A., Soderberg, F. B., Goldman, P., The reduction of N-hydroxy-4-acetylaminobiphenyl by the intestinal microflora of the rat. Cancer Res. 1975, 35, 2962-2968.
59. Brandi, G., Dabard, J., Raibaud, P., Di Battista, M. et al., Intestinal microflora and digestive toxicity of irinotecan in mice. J. Natl. Cancer Inst. 2006, 12, 1299-1307.
60. Möller, L., Zeisig, M., Midtvedt, T., Gustafsson, J., Intestinal microflora enhances formation of DNA adducts following administration of 2-NF and 2-AAF. Carcinogenesis 1994, 15, 857-861.
61. Ball, L. M., Rafter, J. J., Gustafsson, J., Gustafsson, B. E. et al., Formation of mutagenic urinary metabolites from 1-nitropyrene in germ-free and conventional rats: role of the gut flora. Carcinogenesis 1991, 12, 1-5.
62. Kinouchi, T., Morotomi, M., Mutai, M., Fifer, E. K. et al., Metabolism of 1-nitropyrene in germ-free and conventional rats. Jpn. J. Cancer Res. 1986, 77, 356-369.
63. Karam, E. L. B., Bayoumy, K., Sharma, C., Louis, Y. M. et al., The role of intestinal microflora in the metabolic reduction of 1-nitropyrene to 1-aminopyrene in conventional and germfree rats and in humans. Cancer Lett. 1983, 19, 311-316.
64. Lennernas, H., Abrahamsson, B., The use of biopharmaceutic classification of drugs in drug discovery and development: current status and future extension. J. Pharm. Pharmacol. 2005, 57, 273-285.
65. Amidon, G. L., Lennernas, H., Shah, V. P., Crison, J. R., A theoretical basis for a biopharmaceutics drug classification: the correlation of in vitro drug product dissolution and in vivo bioavailability. Pharm. Res. 1995, 12, 413-420.
66. Dressman, J. B., Amidon, G. L., Reppas, C., Shah, V. P., Dissolution testing as a prognostic tool for oral drug absorption: immediate release dosage forms. Pharm. Res. 1998, 15, 11-22.
67. Lindahl, A., Ungell, A.-L., Knutson, L., Lennernas, H., Characterization of fluids from the stomach and proximal jejunum in men and women. Pharm. Res. 1997, 14, 497-502.
68. McConnell, E. L., Fadda, H. M., Basit, A. W., Gut instincts: explorations in intestinal physiology and drug delivery. Int. J. Pharm. 2008, 364, 213-226.
69. Shamat, M. A., The role of the gastrointestinal microflora in the metabolism of drugs. Int. J. Pharm. 1993, 97, 1-13.
70. Ames, B. A., Durston, W. E., Yamasaki, E., Lee, F. D., Carcinogens are mutagens: a simple test system combining liver homogenates for activation and bacteria for detection. Proc. Natl. Acad. Sci. USA 1973, 70, 2281-2285.
71. Mortelmans, K., Zeiger, E., The Ames Salmonella/ microsome mutagenicity assay. Mutat. Res. 2000, 455, 29-60.
72. Eckburg, P. B., Bik, E. M., Berstein, C. N, Purdom, E. et al., Diversity of the human intestinal microbial flora. Science 2005, 308, 1635-1638.
73. De Preter, V., Hamer, H. M., Windey, K., Verbeke, K., The impact of pre- and/or probiotics on human colonic metabolism: does it affect human health? Mol. Nutr. Food Res. 2011, 55, 46-57.
74. Nam, Y. D., Jung, M. J., Roh, S. W., Kim, M. S., Bae, J. W., Comparative analysis of Korean human gut microbiota by barcoded pyrosequencing. PLoS One 2011, 6, e22109.
75. Laube, B., Winkler, S., Ladstetter, B., Scheller, T., Schwarz, L. R., Establishment of a novel in vitro system for studying the interaction of xenobiotic metabolism of liver and intestinal microflora. Arch. Toxicol. 2000, 74, 379-387.
76. Wilson, I. D., Nicholson, J. K., The role of gut microbiota in drug response. Curr. Pharm. Des. 2009, 15, 1519- 1523.
77. Mercado-Lubo, R., McCormick, B. A., The interaction of gut microbes with host ABC transporters. Gut Microbes 2010, 1, 301-306.
78. Meinl, W., Sczesny, S., Brigelius-Flohe, R., Blaut, M. et al., Impact of gut microbiota on intestinal and hepatic levels of phase 2 xenobiotic-metabolizing enzymes in the rat. Drug Metab. Dispos. 2009, 37, 1179-1186.