Glucuronidation of benzidine and its metabolites by cDNA-expressed human UDP-glucuronosyltransferases and pH stability of glucuronides

Carcinogenesis

Volumn 20, Issue 10, 1999, Pages 1963-1969

  Ciotti, Marco ^a   Lakshmi, Vijaya M ^b   Basu, Nikhil ^a   Davis, Bernard B ^b   Owens, Ida S ^a   Zenser, Terry V ^b,c  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 BIPHENYLAMINE; AROMATIC AMINE; BENZIDINE; BENZIDINE DERIVATIVE; COMPLEMENTARY DNA; GLUCURONIDE; GLUCURONOSYLTRANSFERASE; HYDROXAMIC ACID;

ARTICLE; BLADDER CANCER; CELL STRAIN COS1; CONTROLLED STUDY; ENZYME METABOLISM; GLUCURONIDATION; PH; PRIORITY JOURNAL;

BASE SEQUENCE; BENZIDINES; DNA PRIMERS; DNA, COMPLEMENTARY; ENZYME STABILITY; GLUCURONIDES; GLUCURONOSYLTRANSFERASE; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; RECOMBINANT PROTEINS;

EID: 0032869568     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/20.10.1963     Document Type: Article

References (55)

1. Rehn, L. (1895) Blasengeschwulste bei fuchsinarbeitern. Arch. Klin. Chir., 50, 588-600.
2. Case, R.A.M., Hosker, M.W., McDonald, D.B. and Pearson, J.T. (1954) Tumors of the urinary bladder in workmen engaged in the manufacture and use of certain dyestuff intermediates in the British chemical industry. Br. J. Ind. Med., 11, 75-104.
3. Doll, R. and Peto, R. (1981) The Causes of Cancer. Oxford University Press, New York, NY.
4. Bi, W., Hayes, R.B., Feng, P., Qi, Y., You, X., Zhen, J., Zhang, M., Qu, B., Fu, Z., Chen, M., Co Chien, H.T. and Blot, W.J. (1992) Mortality and incidence of bladder cancer in benzidine-exposed workers in China. Am. J. Ind. Med., 21, 481-489.
5. Silverberg, E. and Lubera, J. (1987) Cancer statistics, 1987. CA Cancer J. Clin., 37, 2-19.
6. Parker, S.L., Tong, T., Bolden, S. and Wingo, P. (1996) Cancer statistics, 1996. CA Cancer J. Clin., 46, 5-27.
7. Kadlubar, F.F., Miller, J.A. and Miller, E.C. (1977) Hepatic microsomal N-glucuronidation and nucleic acid binding of N-hydroxy arylamines in relation to urinary bladder carcinogenesis. Cancer Res., 37, 805-814.
8. Lakshmi, V.M., Zenser, T.V. and Davis, B.B. (1998) N′-(3′-monophosphodeoxyguanosin-8-yl)-N-acetylbenzidine formation by peroxidative metabolism. Carcinogenesis, 19, 911-917.
9. Zenser, T.V., Mattammal, M.B., Armbrecht, H.J. and Davis, B.B. (1980) Benzidine binding to nucleic acids mediated by the peroxidative activity of prostaglandin endoperoxide synthetase. Cancer Res., 40, 2839-2845.
10. Zenser, T.V., Mattammal, M.B., Wise, R.W., Rice, J.R. and Davis, B.B. (1983) Prostaglandin H synthase-catalyzed activation of benzidine: a model to assess pharmacologic intervention of the initiation of chemical carcinogenesis. J. Pharmacol. Exp. Ther., 227, 545-550.
11. Miller, J.A. and Miller, E.C. (1977) The concept of reactive electrophilic metabolites in chemical carcinogenesis: recent results with aromatic amines, safrole, and aflatoxin B1. In Jollow, D.J., Kocsis, J.J., Snyder, R. and Vainio, H. (eds) Biological Reactive Intermediates. Plenum Publishing, New York, NY, pp. 6-24.
12. Frederick, C.B., Weis, C.C., Flammang, T.J., Martin, C.N. and Kadlubar, F.F. (1985) Hepatic N-oxidation, acetyl-transfer and DNA-binding of the acetylated metabolites of the carcinogen benzidine. Carcinogenesis, 6, 959-965.
13. Lakshmi, V.M., Zenser, T.V. and Davis, B.B. (1997) Rat liver cytochrome P450 metabolism of N-acetylbenzidine and N,N′-diacetylbenzidine. Drug Metab. Dispos., 25, 481-488.
14. Dutton, G.J. (1980) Glucuronidation of Drugs and Other Compounds. CRC Press, Boca Raton, FL.
15. Mulder, G.J., Coughtrie, M.W.H. and Burchell, B. (1990) Glucuronidation. In Mulder, G.J. (ed.) Conjugation Reactions in Drug Metabolism: An Integrated Approach. Taylor & Francis, New York, NY, pp. 51-105.
16. Irving, C.C. (1977) Influence of the aryl group on the reaction of glucuronides of N-arylacethydroxamic acids with polynucleotides. Cancer Res., 37, 524-528.
17. Babu, S.R., Lakshmi, V.M., Hsu, F.F., Zenser, T.V. and Davis, B.B. (1995) Glucuronidation of N-hydroxy metabolites of N-acetylbenzidine. Carcinogenesis, 16, 3069-3074.
18. Babu, S.R., Lakshmi, V.M., Hsu, F.F., Zenser, T.V. and Davis, B.B. (1992) Role of N-glucuronidation in benzidine-induced bladder cancer in dog. Carcinogenesis, 13, 1235-1240.
19. Babu, S.R., Lakshmi, V.M., Hsu, F.F., Kane, K.E., Zenser, T.V. and Davis, B.B. (1993) N-Acetylbenzidine-N′-glucuronidation by human, dog, and rat liver. Carcinogenesis, 14, 2605-2611.
20. Rothman, N., Talaska, G., Hayes, R. et al. (1997) Acidic urine pH is associated with elevated levels of free urinary benzidine and N-acetylbenzidine and urothelial cell DNA adducts in exposed workers. Cancer Epidemiol. Biomarkers Prevent., 6, 1039-1042.
21. Green, M.D., Bishop, W.P. and Tephly, T.R. (1995) Expressed human UGT1.4 protein catalyzes the formation of quaternary ammonium-linked glucuronides. Drug Metab. Dispos., 23, 299-302.
22. Babu, S.R., Lakshmi, V.M., Zenser, T.V. and Davis, B.B. (1994) Glucuronidation of N-acetylbenzidine by human liver. Drug Metab. Dispos., 22, 922-927.
23. Babu, S.R., Lakshmi, V.M., Owens, I.S., Zenser, T.V. and Davis, B.B. (1994) Human liver glucuronidation of benzidine. Carcinogenesis, 15, 2003-2007.
24. Burchell, B., Nebert, D.W., Nelson, D.R. et al. (1991) The UDP-glucuronosyltransferase gene superfamily: suggested nomenclature based on evolutionary divergence. DNA Cell Biol., 10, 487-494.
25. Munzel, P.A., Bookjans, G., Mehner, G., Lehmkoster, T. and Bock, K.W. (1996) Tissue-specific 2,3,7,8-tetrachlorodibenzo-p-dioxin-inducible expression of human UDP-glucuronosyltransferase UGT1A6. Arch. Biochem. Biophys., 335, 205-210.
26. Ritter, J.K., Sheen, Y.Y. and Owens, I.S. (1990) Cloning and expression of human liver UDP-glucuronosyltransferase in COS-1 cells. J. Biol. Chem., 265, 7900-7906.
27. Jin, C., Miners, J.O., Lillywhite, K.J. and Mackenzie, P.I. (1993) Complementary deoxyribonucleic acid cloning and expression of a human liver uridine diphosphate-glucuronosyltransferase glucuronidating carboxylic acid-containing drugs. J. Pharmacol. Exp. Ther., 264, 475-479.
28. Ciotti, M., Marrone, A., Potter, C. and Owens, I.S. (1997) Genetic polymorphism in the human UGT1A6 (planar phenol) UDP-glucuronosyltransferase: pharmacological implications. Pharmacogenetics, 7, 485-495.
29. Lakshmi, V.M., Mattammal, M.B., Spry, L.A., Kadlubar, F.F., Zenser, T.V. and Davis, B.B. (1990) Metabolism and disposition of benzidine in the dog. Carcinogenesis, 11, 139-144.
30. Lakshmi, V.M., Zenser, N.T., Hsu, F.F., Mattammal, M.B., Zenser, T.V. and Davis, B.B. (1996) NADPH-dependent oxidation of benzidine by rat liver. Carcinogenesis, 17, 1941-1947.
31. Ritter, J.K., Crawford, J.M. and Owens, I.S. (1991) Cloning of two human liver bilirubin UDP-glucuronosyltransferase cDNAs with expression in COS-1 cells. J. Biol. Chem., 266, 1043-1047.
32. Ciotti, M. and Owens, I.S. (1996) Evidence for overlapping active sites for 17α-ethynylestradiol and bilirubin in the human major bilirubin UDP-glucuronosyltransferase. Biochemistry, 35, 10119-10124.
33. Ritter, J.K., Yeatman, M.T., Kaiser, C., Gridelli, B. and Owens, I.S. (1993) A phenylalanine codon deletion at the UGT1 gene complex locus of a Crigler-Najjar Type 1 patient generates a pH-sensitive bilirubin UDP-glucuronosyltransferase. J. Biol. Chem., 268, 23573-23579.
34. Lakshmi, V.M., Bell, D.A., Watson, M.A., Zenser, T.V. and Davis, B.B. (1995) N-Acetylbenzidine and N,N′-diacetylbenzidine formation by rat and human liver slices exposed to benzidine. Carcinogenesis, 16, 1565-1571.
35. Ritter, J.K., Chen, F., Sheen, Y.Y., Tran, H.M., Kimura, S., Yeatman, M.T. and Owens, I.S. (1992) A novel complex locus UGT1 encodes human bilirubin, phenol, and other UDP-glucuronosyltransferase isozymes with identical carboxyl termini. J. Biol. Chem., 267, 3257-3261.
36. Zenser, T., Lakshmi, V. and Davis, B. (1999) Human and E.coli β-glucuronidase hydrolysis of glucuronide conjugates of benzidine and 4-aminobiphenyl, and their hydroxy metabolites. Drug Metab. Dispos., 27, in press.
37. Green, M.D. and Tephly, T.R. (1996) Glucuronidation of amines and hydroxylated xenobiotics and endobiotics catalyzed by expressed human UGT1.4 protein. Drug Metab. Dispos., 24, 356-363.
38. King, C.D., Green, M.D., Rios, G.R., Coffman, B.L., Owens, I.S., Bishop, W.P. and Tephly, T.R. (1996) The glucuronidation of exogenous and endogenous compounds by stably expressed rat and human UDP-glucuronosyltransferase 1.1. Arch. Biochem. Biophys., 332, 92-100.
39. Orzechowski, A., Schrenk, D., Bock-Hennig, B.S. and Bock, K.W. (1994) Glucuronidation of carcinogenic arylamines and their N-hydroxy derivatives by rat and human phenol UDP-glucuronosyltransferases of the UGT1 gene complex. Carcinogenesis, 15, 1549-1553.
40. Jin, C.-J., Miners, J.O., Burchell, B. and Mackenzie, P.I. (1993) The glucuronidation of hydroxylated metabolites of benzo[a]pyrene and 2-acetylaminofluorene by cDNA-expressed human UDP-glucuronosyltransferases. Carcinogenesis, 14, 2637-2639.
41. Strassburg, C.P., Manns, M.P. and Tukey, R.H. (1997) Differential down-regulation of the UDP-glucuronosyltransferase IA locus is an early event in human liver and biliary cancer. Cancer Res., 57, 2979-2985.
42. Strassburg, C.P., Oldhafer, K., Manns, M.P. and Tukey, R.H. (1997) Differential expression of the UGT1A locus in human liver, biliary, and gastric tissue: identification of UGT1A7 and UGT1A10 transcripts in extrahepatic tissue. Mol. Pharmacol., 52, 212-220.
43. McGurk, K.A., Brierley, C.H. and Burchell, B. (1998) Drug glucuronidation by human renal UDP-glucuronosyltransferases. Biochem. Pharmacol., 55, 1005-1012.
44. Ritter, J.K., Chen, F., Sheen, Y.Y., Lubet, R.A. and Owens, I.S. (1992) Two human liver cDNAs encode UDP-glucuronosyltransferases with two log differences in activity toward parallel substrates including hyodeoxycholic acid and certain estrogen derivatives. Biochemistry, 31, 3409-3414.
45. Sciarini, L.J. and Meigs, J.W. (1961) The biotransformation of benzidine. II. Studies in mouse and man. Arch. Environ. Health, 2, 423-428.
46. Lynn, R.K., Garvie-Gould, C., Milam, D.F., Scott, K.F., Eastman, C.L. and Rodgers, R.M. (1983) Metabolism of the human carcinogen, benzidine, in the isolated perfused rat liver. Drug Metab. Dispos., 11, 109-114.
47. Babu, S.R., Lakshmi, V.M., Huang, G.P.-W., Zenser, T.V. and Davis, B.B. (1996) Glucuronide conjugates of 4-aminobiphenyl and its N-hydroxy metabolites: pH stability and synthesis by human and dog liver. Biochem. Pharmacol., 51, 1679-1687.
48. Beland, F.A., Beranek, D.T., Dooley, K.L., Heflich, R.H. and Kadlubar, F.F. (1983) Arylamine-DNA adducts in vitro and in vivo: their role in bacterial mutagenesis and urinary bladder carcinogenesis. Environ. Health Perspect., 49, 125-134.
49. Melchior, W.B.Jr, Marques, M.M. and Beland, F.A. (1994) Mutations induced by aromatic amine DNA adducts in pBR322. Carcinogenesis, 15, 889-899.
50. Heflich, R.H., Morris, S.M., Beranek, D.T., McGarrity, L.J., Chen, J.J. and Beland, F.A. (1986) Relationships between the DNA adducts and the mutations and sister-chromatid exchanges produced in Chinese hamster ovary cells by N-hydroxy-2-aminofluorene, N-hydroxy-N′-acetylbenzidine and 1-nitrosopyrene. Mutagenesis, 1, 201-206.
51. Fox, T.R., Schumann, A.M., Watanabe, P.G., Yano, B.L., Maher, V.M. and McCormick, J.J. (1990) Mutational analysis of the H-ras oncogene in spontaneous C57BL/6×C3H/He mouse liver tumors and tumors induced with genotoxic and nongenotoxic hepatocarcinogens. Cancer Res., 50, 4014-4019.
52. Talaska, G., Au, W.W., Ward, J.B.Jr, Randerath, K. and Legator, M.S. (1987) The correlation between DNA adducts and chromosomal aberrations in the target organ of benzidine exposed, partially-hepatectomized mice. Carcinogenesis, 8, 1899-1905.
53. Remer, T. and Manz, F. (1995) Potential renal acid load of foods and its influence on urine pH. J. Am. Diet. Assoc., 95, 791-797.
54. Zenser, T.V., Lakshmi, V.M., Hsu, F.F. and Davis, B.B. (1999) Peroxygenase metabolism of N-acetylbenzidine by prostaglandin H synthase. J. Biol. Chem., 274, 14850-14856.
55. Rothman, N., Bhatnagar, V.K., Hayes, R.B. et al. (1996) The impact of interindividual variation in NAT2 activity on benzidine urinary metabolites and urothelial DNA adducts in exposed workers. Proc. Narl Acad. Sci. USA, 93, 5084-5089.