Toxicological significance of azo dye metabolism by human intestinal microbiota

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 2, 2012, Pages 568-586

  Feng, Jinhui ^a   Cerniglia, Carl E ^a   Chen, Huizhong ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Azo dye; Azoreductase; Degradation; Genotoxicity; Intestinal Microbiota; Metabolite; Review

Indexed keywords

1 (4 PHENYLAZOPHENYLAZO) 2 NAPHTHALENOL; 1 [(2,4 DIMETHYL)AZO] 2,4 NAHPTHALENOL; 2 METHYLANILINE; 2 NAPHTHOL; 2,4 DIMETHYLANILINE; 4 NITROANILINE; ALLURA RED AC; AMINOAZOTOLUENE; ANILINE; AZO DYE; AZO REDUCTASE; BENZIDINE; CONGO RED; GIMERACIL PLUS OTERACIL POTASSIUM PLUS TEGAFUR; METHYL ORANGE; METHYL RED; N,N DIMETHYL 1,4 PHENYLENEDIAMINE; ORANGE G; ORANGE II; PARA RED; PHENYLENEDIAMINE; PONCEAU BS; PONCEAU S; QUERCETIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SMALL SUBUNIT RIBOSOMAL RNA; SULFANILIC ACID; SUNSET YELLOW; TARTRAZINE; UNCLASSIFIED DRUG; AZO COMPOUND; CARCINOGEN; COLORING AGENT;

ARTICLE; BACEROIDES FRAGILIS; BACTERIAL MEMBRANE; BACTEROIDES; BACTEROIDES DISTASONIS; BACTEROIDES OVATUS; BACTEROIDES THETAIOTAOMICRON; BACTEROIDES VULGATUS; BIFIDOBACTERIUM ADOLESCENTIS; BIFIDOBACTERIUM LONGUM; BIFIDOBACTERIUM LONGUM INFANTIS; BIODEGRADATION; CARCINOGENESIS; CHEMICAL STRUCTURE; CHROMOSOME ABERRATION; CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM DIFFICILE INFECTION; DECOLORIZATION; DEGRADATION; DENATURING GRADIENT GEL ELECTROPHORESIS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROTOXEMIA; ENVIRONMENTAL RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FOOD CONTAMINATION; GENE SEQUENCE; GENOTOXICITY; HUMAN; INTESTINE FLORA; LACTOBACILLUS PARACASEI; METABOLIC ACTIVATION; MICROBIAL DIVERSITY; MICROBIAL METABOLISM; MUTAGENESIS; NONHUMAN; SALMONELLA TYPHIMURIUM; BACTERIUM; INTESTINE; METABOLISM; MICROBIOLOGY; REVIEW;

MAMMALIA;

AZO COMPOUNDS; BACTERIA; CARCINOGENS; COLORING AGENTS; HUMANS; INTESTINES;

EID: 84860846336     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: None     Document Type: Article

References (142)

1. Bioassay of p-phenylenediamine dihydrochloride for possible carcinogenicity. Natl Cancer Inst Carcinog Tech Rep Ser 174:1-107 (1979)
2. IARC monographs on the evaluation of the carcinogenic risk of chemicals to man: some aziridines, N-, S- & Omustards and selenium. IARC Monogr Eval Carcinog Risk Chem Man 9:1-268 (1975)
3. NTP toxicology and carcinogenesis studies of pnitroaniline (CAS No. 100-01-6) in B6C3F1 mice (gavage studies). Natl Toxicol Program Tech Rep Ser 418:1-203 (1993)
4. Ortho-toluidine. IARC Monogr Eval Carcinog Risks Hum 77:267-322 (2000)
5. Overall evaluations of carcinogenicity: an updating of IARC Monographs volumes 1 to 42. IARC Monogr Eval Carcinog Risks Hum Suppl 7:1-440 (1987)
6. Ahmed, R., and D. Gray. Immunological Memory and Protective Immunity: Understanding Their Relation. Science 272:54-60 (1996)
7. Aires, J., P. Anglade, F. Baraige, M. Zagorec, M. C. Champomier-Verges, and M. J. Butel. Proteomic comparison of the cytosolic proteins of three Bifidobacterium longum human isolates and B. longum NCC2705. BMC Microbiol 10:29 (2010)..
8. Anfossi, L., C. Baggiani, C. Giovannoli, and G. Giraudi. Development of enzyme-linked immunosorbent assays for Sudan dyes in chilli powder, ketchup and egg yolk. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 26:800-7 (2009)
9. Anuradha, S., S. Arora, S. Mehrotra, A. Arora, and P. Kar. Acute renal failure following para-phenylenediamine (PPD) poisoning: A case report and review. Ren Fail 26:329-32 (2004)
10. Ashby, J., D. Paton, P. A. Lefevre, J. A. Styles, and F. L. Rose. Evaluation of two suggested methods of deactivating organic carcinogens by molecular modification. Carcinogenesis 3:1277-82 (1982) 11. ATSDR. Toxicological Profile for Benzidine (2001)
11. Audy, J., S. Labrie, D. Roy, and G. Lapointe. Sugar source modulates exopolysaccharide biosynthesis in Bifidobacterium longum subsp. longum CRC 002. Microbiology 156:653-64 (2010).
12. Ben Mansour, H., D. Barillier, D. Corroler, K. Ghedira, L. Chekir-Ghedira, and R. Mosrati. In vitro study of DNA damage induced by acid orange 52 and its biodegradation derivatives. Environ Toxicol Chem 28:489-95 (2009)
13. Ben Mansour, H., D. Corroler, D. Barillier, K. Ghedira, L. Chekir, and R. Mosrati. Evaluation of genotoxicity and pro-oxidant effect of the azo dyes: acids yellow 17, violet 7 and orange 52, and of their degradation products by Pseudomonas putida mt-2. Food Chem Toxicol 45:1670-7 (2007).
14. Bik, E. M. Composition and function of the humanassociated microbiota. Nutr Rev 67 Suppl 2:S164-71 (2009)
15. Bin, Y., Z. Jiti, W. Jing, D. Cuihong, H. Hongman, S. Zhiyong, and B. Yongming. Expression and characteristics of the gene encoding azoreductase from Rhodobacter sphaeroides AS1.1737. FEMS Microbiol Lett 236:129-36 (2004).
16. Bjorkholm, B., C. M. Bok, A. Lundin, J. Rafter, M. L. Hibberd, and S. Pettersson. Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS One 4:e6958 (2009)
17. Blumel, S., H. J. Knackmuss, and A. Stolz. Molecular cloning and characterization of the gene coding for the aerobic azoreductase from Xenophilus azovorans KF46F. Appl Environ Microbiol 68:3948-55 (2002)
18. Blumel, S., and A. Stolz. Cloning and characterization of the gene coding for the aerobic azoreductase from Pigmentiphaga kullae K24. Appl Microbiol Biotechnol 62:186-90 (2003)
19. Bolt, H. M., and K. Golka. The debate on carcinogenicity of permanent hair dyes: new insights. Crit Rev Toxicol 37:521- 36 (2007)
20. Bomhard, E. M., and B. A. Herbold. Genotoxic activities of aniline and its metabolites and their relationship to the carcinogenicity of aniline in the spleen of rats. Crit Rev Toxicol 35:783-835 (2005)
21. Brenner, D. M., and W. D. Chey. Bifidobacterium infantis 35624: A novel probiotic for the treatment of irritable bowel syndrome. Rev Gastroenterol Disord 9:7-15 (2009).
22. Brenner, D. M., M. J. Moeller, W. D. Chey, and P. S. Schoenfeld. The utility of probiotics in the treatment of irritable bowel syndrome: A systematic review. Am J Gastroenterol 104:1033-49; quiz 1050 (2009)
23. Brigé, A., B. Motte, J. Borloo, G. Buysschaert, B. Devreese, and J. J. Van Beeumen. Bacterial decolorization of textile dyes is an extracellular process requiring a multicomponent electron transfer pathway. Microbial Biotechnology 1:40-52 (2008).
24. Brown, J. P., and P. S. Dietrich. Mutagenicity of selected sulfonated azo dyes in the Salmonella/microsome assay: use of aerobic and anaerobic activation procedures. Mutat Res 116:305-15 (1983)
25. Brown, J. P., G. W. Roehm, and R. J. Brown. Mutagenicity testing of certified food colors and related azo, xanthene and triphenylmethane dyes with the Salmonella/microsome system. Mutat Res 56:249-71 (1978).
26. Brown, M. A., and S. C. De Vito. Predicting azo dye toxicity. Critical Reviews in Environmental Science and Technology 23:249-324 (1993)
27. Calbiani, F., M. Careri, L. Elviri, A. Mangia, and I. Zagnoni. Accurate mass measurements for the confirmation of Sudan azo-dyes in hot chilli products by capillary liquid chromatography-electrospray tandem quadrupole orthogonalacceleration time of flight mass spectrometry. J Chromatogr A 1058:127-35 (2004).
28. Carreon, T., M. J. Hein, S. M. Viet, K. W. Hanley, A. M. Ruder, and E. M. Ward. Increased bladder cancer risk among workers exposed to o-toluidine and aniline: A reanalysis. Occup Environ Med 67:348-50 (2010)
29. Chen, H. Recent advances in azo dye degrading enzyme research. Curr Protein Pept Sci 7:101-11 (2006).
30. Chen, H., J. Feng, O. Kweon, H. Xu, and C. Cerniglia. Identification and molecular characterization of a novel flavinfree NADPH preferred azoreductase encoded by azoB in Pigmentiphaga kullae K24. BMC Biochemistry 11:13 (2010)
31. Chen, H., S. L. Hopper, and C. E. Cerniglia. Biochemical and molecular characterization of an azoreductase from Staphylococcus aureus, a tetrameric NADPH-dependent flavoprotein. Microbiology 151:1433-41 (2005).
32. Chen, H., R. F. Wang, and C. E. Cerniglia. Molecular cloning, overexpression, purification, and characterization of an aerobic FMN-dependent azoreductase from Enterococcus faecalis. Protein Expr Purif 34:302-10 (2004)
33. Chen, H., H. Xu, O. Kweon, S. Chen, and C. E. Cerniglia. Functional role of Trp-105 of Enterococcus faecalis azoreductase (AzoA) as resolved by structural and mutational analysis. Microbiology 154:2659-67 (2008).
34. Chen, Y., T. Kinouchi, K. Kataoka, S. Akimoto, and Y. Ohnishi. Purification and characterization of a fibrinogen-degrading protease in Bacteroides fragilis strain YCH46. Microbiol Immunol 39:967-77 (1995)
35. Chung, K. T. The significance of azo-reduction in the mutagenesis and carcinogenesis of azo dyes. Mutat Res 114:269-81 (1983).
36. Chung, K. T., G. E. Fulk, and A. W. Andrews. Mutagenicity testing of some commonly used dyes. Appl Environ Microbiol 42:641-8 (1981)
37. Chung, K. T., G. E. Fulk, and M. Egan. Reduction of azo dyes by intestinal anaerobes. Appl Environ Microbiol 35:558-62 (1978).
38. Chung, K. T., S. E. Stevens, Jr., and C. E. Cerniglia. The reduction of azo dyes by the intestinal microflora. Crit Rev Microbiol 18:175-90 (1992)
39. Collier, S. W., J. E. Storm, and R. L. Bronaugh. Reduction of azo dyes during in vitro percutaneous absorption. Toxicol Appl Pharmacol 118:73-9 (1993)
40. Combes, R. D., and R. B. Haveland-Smith. A review of the genotoxicity of food, drug and cosmetic colours and other azo, triphenylmethane and xanthene dyes. Mutat Res 98:101-248 (1982)
41. D'Elia, J. N., and A. A. Salyers. Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 178:7180-6 (1996).
42. Dafale, N., N. N. Rao, S. U. Meshram, and S. R. Wate. Decolorization of azo dyes and simulated dye bath wastewater using acclimatized microbial consortium-biostimulation and halo tolerance. Bioresour Technol 99:2552-8 (2008)
43. Danford, N. The genetic toxicology of ortho-toluidine. Mutat Res 258:207-36 (1991)
44. De Flora, S., A. Camoirano, P. Zanacchi, and C. Bennicelli. Mutagenicity testing with TA97 and TA102 of 30 DNAdamaging compounds, negative with other Salmonella strains. Mutat Res 134:159-65 (1984)
45. De Flora, S., P. Zanacchi, A. Camoirano, C. Bennicelli, and G. S. Badolati. Genotoxic activity and potency of 135 compounds in the Ames reversion test and in a bacterial DNArepair test. Mutat Res 133:161-98 (1984).
46. Degawa, M., C. Kanazawa, and Y. Hashimoto. In vitro metabolism of o-aminoazotoluene and mutagenesis of Salmonella by the metabolites. Carcinogenesis 3:1113-7 (1982)
47. Delclos, K. B., W. G. Tarpley, E. C. Miller, and J. A. Miller. 4-aminoazobenzene and N,N-dimethyl-4- aminoazobenzene as equipotent hepatic carcinogens in male C57BL/6 X C3H/He F1 mice and characterization of N- (Deoxyguanosin-8-yl)-4-aminoazobenzene as the major persistent hepatic DNA-bound dye in these mice. Cancer Res 44:2540-50 (1984).
48. Dethlefsen, L., M. McFall-Ngai, and D. A. Relman. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811-8 (2007)
49. Dillon, D., R. Combes, and E. Zeiger. Activation by caecal reduction of the azo dye D & C red no. 9 to a bacterial mutagen. Mutagenesis 9:295-9 (1994)
50. Duchmann, R., I. Kaiser, E. Hermann, W. Mayet, K. Ewe, and K. H. Meyer zum Buschenfelde. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol 102:448-55 (1995)
51. Eckburg, P. B., E. M. Bik, C. N. Bernstein, E. Purdom, L. Dethlefsen, M. Sargent, S. R. Gill, K. E. Nelson, and D. A. Relman. Diversity of the human intestinal microbial flora. Science 308:1635-8 (2005).
52. Elhkim, M. O., F. Heraud, N. Bemrah, F. Gauchard, T. Lorino, C. Lambre, J. M. Fremy, and J. M. Poul. New considerations regarding the risk assessment on Tartrazine An update toxicological assessment, intolerance reactions and maximum theoretical daily intake in France. Regul Toxicol Pharmacol 47:308-16 (2007)
53. Fassina, G., A. Abbondandolo, L. Mariani, M. Taningher, and S. Parodi. Mutagenicity in V79 cells does not correlate with carcinogenity in small rodents for 12 aromatic amines. J Toxicol Environ Health 29:109-30 (1990).
54. Feng, J., T. M. Heinze, H. Xu, C. E. Cerniglia, and H. Chen. Evidence for significantly enhancing reduction of Azo dyes in Escherichia coli by expressed cytoplasmic Azoreductase (AzoA) of Enterococcus faecalis. Protein Pept Lett 17:578-84 (2010)
55. Fisher, K., and C. Phillips. The ecology, epidemiology and virulence of Enterococcus. Microbiology 155:1749-57 (2009).
56. Flint, H. J., E. A. Bayer, M. T. Rincon, R. Lamed, and B. A. White. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6:121-31 (2008)
57. Garrigue, J. L., M. Ballantyne, T. Kumaravel, M. Lloyd, G. J. Nohynek, D. Kirkland, and H. Toutain. In vitro genotoxicity of para-phenylenediamine and its Nmonoacetyl or N,N'-diacetyl metabolites. Mutat Res 608:58-71 (2006).
58. Golka, K., S. Kopps, and Z. W. Myslak. Carcinogenicity of azo colorants: influence of solubility and bioavailability. Toxicol Lett 151:203-10 (2004)
59. Gopinath, K. P., H. Asan Meera Sahib, K. Muthukumar, and M. Velan. Improved biodegradation of Congored by using Bacillus sp. Bioresour Technol 100:670-675 (2009).
60. Gottlieb, A., C. Shaw, A. Smith, A. Wheatley, and S. Forsythe. The toxicity of textile reactive azo dyes after hydrolysis and decolourisation. J Biotechnol 101:49-56 (2003)
61. Haley, T. J. Benzidine revisited: A review of the literature and problems associated with the use of benzidine and its congeners. Clin Toxicol 8:13-42 (1975).
62. Han, D., M. Yu, D. Knopp, R. Niessner, M. Wu, and A. Deng. Development of a highly sensitive and specific enzyme-linked immunosorbent assay for detection of Sudan I in food samples. J Agric Food Chem 55:6424-30 (2007)
63. Han, J., L. C. Antunes, B. B. Finlay, and C. H. Borchers. Metabolomics: towards understanding host-microbe interactions. Future Microbiol 5:153-61 (2010)
64. He, L., Y. Su, B. Fang, X. Shen, Z. Zeng, and Y. Liu. Determination of Sudan dye residues in eggs by liquid chromatography and gas chromatography-mass spectrometry. Anal Chim Acta 594:139-46 (2007)
65. Hill, M. J. Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6 Suppl 1:S43-5 (1997)
66. Hooper, L. V., and J. I. Gordon. Commensal Host- Bacterial Relationships in the Gut. Science 292:1115-1118 (2001)
67. Hooper, L. V., and A. J. Macpherson. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10:159-169 (2010).
68. Ito, K., M. Nakanishi, W. C. Lee, H. Sasaki, S. Zenno, K. Saigo, Y. Kitade, and M. Tanokura. Three-dimensional structure of AzoR from Escherichia coli. An oxidereductase conserved in microorganisms. J Biol Chem 281:20567-76 (2006)
69. Ito, K., M. Nakanishi, W. C. Lee, Y. Zhi, H. Sasaki, S. Zenno, K. Saigo, Y. Kitade, and M. Tanokura. Expansion of substrate specificity and catalytic mechanism of azoreductase by X-ray crystallography and site-directed mutagenesis. J Biol Chem 283:13889-96 (2008)
70. Jadhav, J. P., G. K. Parshetti, S. D. Kalme, and S. P. Govindwar. Decolourization of azo dye methyl red by Saccharomyces cerevisiae MTCC 463. Chemosphere 68:394-400 (2007)
71. Kawakami, T., K. Isama, H. Nakashima, T. Tsuchiya, and A. Matsuoka. Analysis of primary aromatic amines originated from azo dyes in commercial textile products in Japan. J Environ Sci Health A Tox Hazard Subst Environ Eng 45:1281- 95 (2010).
72. Klare, I., C. Konstabel, D. Badstubner, G. Werner, and W. Witte. Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int J Food Microbiol 88:269-90 (2003)
73. Kolekar, Y. M., S. P. Pawar, K. R. Gawai, P. D. Lokhande, Y. S. Shouche, and K. M. Kodam. Decolorization and degradation of Disperse Blue 79 and Acid Orange 10, by Bacillus fusiformis KMK5 isolated from the textile dye contaminated soil. Bioresour Technol 99:8999-9003 (2008).
74. Lazear, E. J., and S. C. Louie. Mutagenicity of some congeners of benzidine in the Salmonella typhimurium assay system. Cancer Lett 4:21-5 (1978)
75. Lee do, K., S. Jang, M. J. Kim, J. H. Kim, M. J. Chung, K. J. Kim, and N. J. Ha. Anti-proliferative effects of Bifidobacterium adolescentis SPM0212 extract on human colon cancer cell lines. BMC Cancer 8:310 (2008)
76. Leroy, F., M. R. Foulquie Moreno, and L. De Vuyst. Enterococcus faecium RZS C5, an interesting bacteriocin producer to be used as a co-culture in food fermentation. Int J Food Microbiol 88:235-40 (2003)
77. Levine, W. G. Metabolism of azo dyes: implication for detoxication and activation. Drug Metab Rev 23:253-309 (1991).
78. Li, X., G. F. Fu, Y. R. Fan, W. H. Liu, X. J. Liu, J. J. Wang, and G. X. Xu. Bifidobacterium adolescentis as a delivery system of endostatin for cancer gene therapy: selective inhibitor of angiogenesis and hypoxic tumor growth. Cancer Gene Ther 10:105-11 (2003)
79. Liger, D., M. Graille, C. Z. Zhou, N. Leulliot, S. Quevillon-Cheruel, K. Blondeau, J. Janin, and H. van Tilbeurgh. Crystal structure and functional characterization of yeast YLR011wp, an enzyme with NAD(P)H-FMN and ferric iron reductase activities. J Biol Chem 279:34890-7 (2004)
80. Liu, Z. J., H. Chen, N. Shaw, S. L. Hopper, L. Chen, S. Chen, C. E. Cerniglia, and B. C. Wang. Crystal structure of an aerobic FMN-dependent azoreductase (AzoA) from Enterococcus faecalis. Arch Biochem Biophys 463:68-77 (2007)
81. Macpherson A., Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria
82. Macpherson, A., U. Y. Khoo, I. Forgacs, J. Philpott- Howard, and I. Bjarnason. Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria. Gut 38:365-75 (1996) 83. Macwana, S. R., S. Punj, J. Cooper, E. Schwenk, and G. H. John. Identification and Isolation of an Azoreductase from Enterococcus faecium. Curr Issues Mol Biol 12:43-48 (2009)
83. Mamber, S. W., V. Bryson, and S. E. Katz. The Escherichia coli WP2/WP100 rec assay for detection of potential chemical carcinogens. Mutat Res 119:135-44 (1983).
84. Mansour, H. B., R. Mosrati, D. Corroler, K. Ghedira, D. Barillier, and L. Chekir-Ghedira. Mutagenicity and genotoxicity of acid yellow 17 and its biodegradation products. Drug Chem Toxicol 32:222-9 (2009)
85. Marhold, J., V. Rambousek, J. Pipalova, and M. Matrka. Oxidation of carcinogenic azo-dyes. VII. Metabolites of some 4'-substituted derivatives of dimethylaminoazobenzene in the bile of rats. Neoplasma 16:191-4 (1969)
86. McBain, A. J., and G. T. Macfarlane. 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 47:407-16 (1998)
87. McCarroll, N. E., C. E. Piper, and B. H. Keech. An E coli microsuspension assay for the detection of DNA damage induced by direct-acting agents and promutagens. Environ Mutagen 3:429-44 (1981).
88. McVey, D. C., R. A. Liddle, J. Riggs-Sauthier, N. Ekwuribe, and S. R. Vigna. Inhibition of Clostridium difficile toxin A-induced colitis in rats by APAZA. Dig Dis Sci 50:565-73 (2005)
89. Moller, P., and H. Wallin. Genotoxic hazards of azo pigments and other colorants related to 1-phenylazo-2- hydroxynaphthalene. Mutat Res 462:13-30 (2000)
90. Moncrief, J. S., R. Obiso, Jr., L. A. Barroso, J. J. Kling, R. L. Wright, R. L. Van Tassell, D. M. Lyerly, and T. D. Wilkins. The enterotoxin of Bacteroides fragilis is a metalloprotease. Infect Immun 63:175-81 (1995)
91. Moore, W. E., and L. V. Holdeman. Human fecal flora: The normal flora of 20 Japanese-Hawaiians. Appl Microbiol 27:961-79 (1974).
92. Morokutti, A., A. Lyskowski, S. Sollner, E. Pointner, T. B. Fitzpatrick, C. Kratky, K. Gruber, and P. Macheroux. Structure and function of YcnD from Bacillus subtilis, a flavincontaining oxidoreductase. Biochemistry 44:13724-33 (2005)
93. Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695-700 (1993).
94. Nakanishi, M., C. Yatome, N. Ishida, and Y. Kitade. Putative ACP phosphodiesterase gene (acpD) encodes an azoreductase. J Biol Chem 276:46394-9 (2001)
95. Nelson, A. A., and G. Woodard. Tumors of the urinary bladder, gall bladder, and liver in dogs fed o-aminoazotoluene or p-dimethylaminoazobenzene. J Natl Cancer Inst 13:1497- 1509 (1953).
96. Osano, O., W. Admiraal, H. J. Klamer, D. Pastor, and E. A. Bleeker. Comparative toxic and genotoxic effects of chloroacetanilides, formamidines and their degradation products on Vibrio fischeri and Chironomus riparius. Environ Pollut 119:195-202 (2002)
97. Osano, O., A. A. Oladimeji, M. H. Kraak, and W. Admiraal. Teratogenic effects of amitraz, 2,4- dimethylaniline, and paraquat on developing frog (Xenopus) embryos. Arch Environ Contam Toxicol 43:42-9 (2002)
98. Peck, M. W. Biology and genomic analysis of Clostridium botulinum. Adv Microb Physiol 55:183-265, 320 (2009)
99. Perez-Diaz, I. M., R. E. Kelling, S. Hale, F. Breidt, and R. F. McFeeters. Lactobacilli and tartrazine as causative agents of red-color spoilage in cucumber pickle products. J Food Sci 72:M240-5 (2007)
100. Perez-Diaz, I. M., and R. F. McFeeters. Modification of azo dyes by lactic acid bacteria. J Appl Microbiol 107:584-9 (2009)
101. Prival, M. J., S. J. Bell, V. D. Mitchell, M. D. Peiperl, and V. L. Vaughan. Mutagenicity of benzidine and benzidinecongener dyes and selected monoazo dyes in a modified Salmonella assay. Mutat Res 136:33-47 (1984)
102. Rafii, F., and C. E. Cerniglia. Comparison of the azoreductase and nitroreductase from Clostridium perfringens. Appl Environ Microbiol 59:1731-4 (1993)
103. Rafii, F., and C. E. Cerniglia. Reduction of azo dyes and nitroaromatic compounds by bacterial enzymes from the human intestinal tract. Environ Health Perspect 103 Suppl 5:17-9 (1995)
104. Rafii, F., W. Franklin, and C. E. Cerniglia. Azoreductase activity of anaerobic bacteria isolated from human intestinal microflora. Appl Environ Microbiol 56:2146-51 (1990)
105. Rafii, F., J. D. Hall, and C. E. Cerniglia. Mutagenicity of azo dyes used in foods, drugs and cosmetics before and after reduction by Clostridium species from the human intestinal tract. Food Chem Toxicol 35:897-901 (1997)
106. Rafii, F., D. B. Smith, R. W. Benson, and C. E. Cerniglia. Immunological homology among azoreductases from Clostridium and Eubacterium strains isolated from human intestinal microflora. J Basic Microbiol 32:99-105 (1992)
107. Rebane, R., I. Leito, S. Yurchenko, and K. Herodes. A review of analytical techniques for determination of Sudan IIV dyes in food matrixes. J Chromatogr A 1217:2747-57 (2010)
108. Reeves, A. R., G. R. Wang, and A. A. Salyers. Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 179:643-9 (1997)
109. Robinson, T., G. McMullan, R. Marchant, and P. Nigam. Remediation of dyes in textile effluent: A critical review on current treatment technologies with a proposed alternative. Bioresour Technol 77:247-55 (2001)
110. Rosenkranz, H. S., and G. Klopman. Structural basis of the mutagenicity of 1-amino-2-naphthol-based azo dyes. Mutagenesis 5:137-46 (1990)
111. Ruseler-van Embden, J. G., R. van der Helm, and L. M. van Lieshout. Degradation of intestinal glycoproteins by Bacteroides vulgatus. FEMS Microbiol Lett 49:37-41 (1989)
112. Ryan, A., N. Laurieri, I. Westwood, C. J. Wang, E. Lowe, and E. Sim. A novel mechanism for azoreduction. J Mol Biol 400:24-37 (2010)
113. Saitoh, S., S. Noda, Y. Aiba, A. Takagi, M. Sakamoto, Y. Benno, and Y. Koga. Bacteroides ovatus as the predominant commensal intestinal microbe causing a systemic antibody response in inflammatory bowel disease. Clin Diagn Lab Immunol 9:54-9 (2002)
114. Sakagami, Y., H. Yamazaki, N. Ogasawara, H. Yokoyama, Y. Ose, and T. Sato. The evaluation of genotoxic activities of disinfectants and their metabolites by umu test. Mutat Res 209:155-60 (1988)
115. Sakamoto, M., and Y. Benno. Reclassification of Bacteroides distasonis, Bacteroides goldsteinii and Bacteroides merdae as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov. and Parabacteroides merdae comb. nov. Int J Syst Evol Microbiol 56:1599-605 (2006)
116. Samejima, K., Z. Tamura, and M. Ishidate. Metabolism of 4-dimethylaminoazobenzene and related compounds. IV. Metabolites of o-aminoazotoluene in rat bile. Chem Pharm Bull (Tokyo) 15:964-75 (1967)
117. Sandhu, P., and J. K. Chipman. Bacterial mutagenesis and hepatocyte unscheduled DNA synthesis induced by chrysoidine azo-dye components. Mutat Res 240:227-36 (1990)
118. Saratale, R. G., G. D. Saratale, J. S. Chang, and S. P. Govindwar. Decolorization and biodegradation of textile dye Navy blue HER by Trichosporon beigelii NCIM-3326. J Hazard Mater 166:1421-8 (2009)
119. Saratale, R. G., G. D. Saratale, D. C. Kalyani, J. S. Chang, and S. P. Govindwar. Enhanced decolorization and biodegradation of textile azo dye Scarlet R by using developed microbial consortium-GR. Bioresour Technol 100:2493-2500 (2009)
120. Savage, D. C. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107-33 (1977)
121. Seesuriyachan, P., S. Takenaka, A. Kuntiya, S. Klayraung, S. Murakami, and K. Aoki. Metabolism of azo dyes by Lactobacillus casei TISTR 1500 and effects of various factors on decolorization. Water Res 41:985-92 (2007)
122. Sellers, C., and S. Markowitz. Reevaluating the carcinogenicity of ortho-toluidine: A new conclusion and its implications. Regul Toxicol Pharmacol 16:301-17 (1992)
123. Shahin, M. M. Mutagenicity evaluation of nitroanilines and nitroaminophenols in Salmonella typhimurium. Int J Cosmet Sci 7:277-89 (1985)
124. Shannon-Lowe, J., N. J. Matheson, F. J. Cooke, and S. H. Aliyu. Prevention and medical management of Clostridium difficile infection. BMJ 340:c1296 (2010)
125. Sharma, P., L. Singh, and N. Dilbaghi. Optimization of process variables for decolorization of Disperse Yellow 211 by Bacillus subtilis using Box- Behnken design. J Hazard Mater 164:1024-9 (2009)
126. Slokar, Y. M., and A. Majcen Le Marechal. Methods of decoloration of textile wastewaters. Dyes and Pigments 37:335-356 (1998)
127. Stingley, R. L., W. Zou, T. M. Heinze, H. Chen, and C. E. Cerniglia. Metabolism of azo dyes by human skin microbiota. J Med Microbiol 59:108-14 (2010)
128. Suzuki, Y., T. Yoda, A. Ruhul, and W. Sugiura. Molecular cloning and characterization of the gene coding for azoreductase from Bacillus sp. OY1-2 isolated from soil. J Biol Chem 276:9059-65 (2001)
129. Sweeney, E. A., J. K. Chipman, and S. J. Forsythe. Evidence for direct-acting oxidative genotoxicity by reduction products of azo dyes. Environ Health Perspect 102 Suppl 6:119-22 (1994)
130. Tamura, Z., and K. Semejima. Metabolism of 4- dimethylaminoazobenzene and related compounds. 3. Metabolites of 4-dimethylaminoazobenzene in rat bile and influence of DAB feeding on their amounts. Chem Pharm Bull (Tokyo) 11:1014-21 (1963)
131. Uter, W., G. Stropp, A. Schnuch, and H. Lessmann. Aniline-a 'historical' contact allergen? Current data from the IVDK and review of the literature. Ann Occup Hyg 51:219-26 (2007)
132. Walker, R., R. Gingell, and D. F. Murrells. Mechanisms of azo reduction by Streptococcus faecalis. I. Optimization of assay conditions. Xenobiotica 1:221-9 (1971)
133. Wang, C. J., C. Hagemeier, N. Rahman, E. Lowe, M. Noble, M. Coughtrie, E. Sim, and I. Westwood. Molecular cloning, characterisation and ligand-bound structure of an azoreductase from Pseudomonas aeruginosa. J Mol Biol 373:1213-28 (2007)
134. Wang, C. J., N. Laurieri, A. Abuhammad, E. Lowe, I. Westwood, A. Ryan, and E. Sim. Role of tyrosine 131 in the active site of paAzoR1, an azoreductase with specificity for the inflammatory bowel disease prodrug balsalazide. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:2-7 (2010)
135. Watanabe, M., and M. Ishidate. Metabolism of 4- dimethylaminoazobenzene and related compounds. V. Quantitative analysis of biliary and urinary metabolites of 4-dimethylamino-azobenzene in rat. Chem Pharm Bull (Tokyo) 15:1461-9 (1967)
136. Wostmann, B. S. The germfree animal in nutritional studies. Annu Rev Nutr 1:257-79 (1981)
137. Xu, H., T. M. Heinze, S. Chen, C. E. Cerniglia, and H. Chen. Anaerobic metabolism of 1-amino-2-naphthol-based azo dyes (Sudan dyes) by human intestinal microflora. Appl Environ Microbiol 73:7759-62 (2007)
138. Xu, H., T. M. Heinze, D. D. Paine, C. E. Cerniglia, and H. Chen. Sudan azo dyes and Para Red degradation by prevalent bacteria of the human gastrointestinal tract. Anaerobe 16:114-9 (2010)
139. Yasunaga, K., A. Kiyonari, M. Nakagawa, and K. Yoshikawa. Different results of the Salmonella umu test between three isomers of phenylenediamine (PDA) derivatives. Drug Chem Toxicol 29:203-13 (2006)
140. Yoshimi, N., S. Sugie, H. Iwata, K. Niwa, H. Mori, C. Hashida, and H. Shimizu. The genotoxicity of a variety of aniline derivatives in a DNA repair test with primary cultured rat hepatocytes. Mutat Res 206:183-91 (1988)
141. You, Z., M. D. Brezzell, S. K. Das, B. H. Hooberman, and J. E. Sinsheimer. Substituent effects on the in vitro and in vivo genotoxicity of 4-aminobiphenyl and 4- aminostilbene derivatives. Mutat Res 320:45-58 (1994)
142. Zocco, M. A., M. E. Ainora, G. Gasbarrini, and A. Gasbarrini. Bacteroides thetaiotaomicron in the gut: Molecular aspects of their interaction. Digestive and Liver Disease 39:707-712 (2007) Key Words: Azo dye, Azoreductase, Degradation, Metabolite, Genotoxicity, Intestinal Microbiota, Review Send correspondence to: Huizhong Chen, Division of Microbiology, National Center for Toxicological Research, U.S. FDA, 3900 NCTR Rd., Jefferson, AR 72079-9502, USA, Tel: 870-543-7410; Fax: 870-543-7307, E-mail: huizhong.chen@fda.hhs.gov