Androgen receptor signals regulate UDP-glucuronosyltransferases in the urinary bladder: A potential mechanism of androgen-induced bladder carcinogenesis

Molecular Carcinogenesis

Volumn 52, Issue 2, 2013, Pages 94-102

  Izumi, Koji ^a   Zheng, Yichun ^a   Hsu, Jong Wei ^a   Chang, Chawnshang ^a   Miyamoto, Hiroshi ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Androgen deprivation; Chemical carcinogens; Glucuronidation; Knockout mouse model; SVHUC cell line

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 1A1; GLUCURONOSYLTRANSFERASE 1A10; GLUCURONOSYLTRANSFERASE 1A8; GLUCURONOSYLTRANSFERASE 1A9; HYDROXYFLUTAMIDE; MESSENGER RNA;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLADDER CARCINOGENESIS; CASTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYSTECTOMY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UROTHELIUM; WESTERN BLOTTING;

AGED; AGED, 80 AND OVER; ANDROGEN ANTAGONISTS; ANIMALS; CELL LINE; CYSTECTOMY; DIHYDROTESTOSTERONE; DOWN-REGULATION; FEMALE; FLUTAMIDE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONOSYLTRANSFERASE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; ORCHIECTOMY; RECEPTORS, ANDROGEN; REFERENCE VALUES; SIGNAL TRANSDUCTION; URINARY BLADDER; URINARY BLADDER NEOPLASMS;

MUS;

EID: 84872600630     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.21833     Document Type: Article

References (39)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Hartge P, Harvey EB, Linehan WM, et al. Unexplained excess risk of bladder cancer in men. J Natl Cancer Inst 1990; 82: 1636-1640.
3. Miyamoto H, Yang Z, Chen Y-T, et al. Promotion of bladder cancer development and progression by androgen receptor signals. J Natl Cancer Inst 2007; 99: 558-568.
4. Bock KW. Roles of UDP-glucuronosyltransferases in chemical carcinogenesis. Crit Rev Biochem Mol Biol 1991; 26: 129-150.
5. Zenser TV, Lakshmi VM, Hsu FF, Davis BB. Metabolism of N-acetylbenzidine and initiation of bladder cancer. Mutat Res 2002; 506-507: 29-40.
6. Hecht SS. Human urinary carcinogen metabolites: Biomarkers for investigating tobacco and cancer. Carcinogenesis 2002; 23: 907-922.
7. 7-methylguanine in urothelial carcinoma patients. Cancer Epidemiol Biomarkers Prev 2008; 17: 3390-3395.
8. Desai AA, Innocenti F, Ratain MJ. UGT pharmacogenomics: Implications for cancer risk and cancer therapeutics. Pharmacogenetics 2003; 13: 517-523.
9. Mackenzie PI, Bock KW, Burchell B, et al. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics 2005; 15: 677-685.
10. Ciotti M, Lakshmi VM, Basu N, Davis BB, Owens IS, Zenser TV. Glucuronidation of benzidine and its metabolites by cDNA-expressed human UDP-glucuronosyltransferases and pH stability of glucuronides. Carcinogenesis 1999; 10: 1963-1969.
11. Wiener D, Doerge DR, Fang J-L, Upadhyaya P, Lazarus P. Characterization of N-glucuronidation of the lung carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) in human liver: Importance of UDP-glucuronosyltransferase 1A4. Drug Metab Dispos 2004; 32: 72-79.
12. Gregory PA, Lewinsky RH, Gardner-Stephen DA, Mackenzie PI. Regulation of UDP glucuronosyltransferases in the gastrointestinal tract. Toxicol Appl Pharmacol 2004; 15: 354-363.
13. Soars MG, Burchell B, Riley RJ. In vitro analysis of human drug glucuronidation and prediction of in vivo metabolic clearance. J Pharmacol Exp Ther 2002; 301: 382-390.
14. Zheng Z, Fang J-L, Lazarus P. Glucuronidation: An important mechanism for detoxification of benzo[A]pyrene metabolites in aerodigestive tract tissues. Drug Metab Dispos 2002; 30: 397-403.
15. Nakamura A, Nakajima M, Yamanaka H, Fujiwara R, Yokoi T. Expression of UGT1A and UGT2B mRNA in human normal tissues and various cell lines. Drug Metab Dispos 2008; 36: 1461-1464.
16. Giuliani L, Gazzaniga P, Caporuscio F, Ciotti M, Frati L, Aglianò AM. Can down-regulation of UDP-glucuronosyltransferases in the urinary bladder tissue impact the risk of chemical carcinogenesis? Int J Cancer 2001; 91: 141-143.
17. Giuliani L, Ciotti M, Stoppacciaro A, et al. UDP-glucuronosyltransferases 1A expression in human urinary bladder and colon cancer by immunohistochemistry. Oncol Rep 2005; 13: 185-191.
18. Takayama K, Kaneshiro K, Tsutsumi S, et al. Identification of novel androgen response genes in prostate cancer cells by coupling chromatin immunoprecipitation and genomic microarray analysis. Oncogene 2007; 26: 4453-4463.
19. Canacci AM, Izumi K, Zheng Y, Gordetsky J, Yao JL, Miyamoto H. Expression of semenogelins I and II and its prognostic significance in human prostate cancer. Prostate 2011; 71: 1108-1114.
20. Yeh S, Tsai M-Y, Xu Q, et al. Generation and characterization of androgen receptor knockout (ARKO) mice: An in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci USA 2002; 99: 13498-13503.
21. Zheng Y, Izumi K, Yao JL, Miyamoto H. Dihydrotestosterone upregulates the expression of epidermal growth factor receptor and ERBB2 in androgen receptor-positive bladder cancer cells. Endocr-Relat Cancer 2011; 18: 451-464.
22. Bock KW. Functions and transcriptional regulation of adult human hepatic UDP-glucuronosyl-transferases (UGTs): Mechanisms responsible for interindividual variation of UGT levels. Biochem Pharmacol 2010; 80: 771-777.
23. Iida K, Itoh K, Kumagai Y, et al. Nrf2 is essential for the chemopreventive efficacy of oltipraz against urinary bladder carcinogenesis. Cancer Res 2004; 15: 6424-6431.
24. Iida K, Mimura J, Itoh K, et al. Suppression of AhR signaling pathway is associated with the down-regulation of UDP-glucuronosyltransferases during BBN-induced urinary bladder carcinogenesis in mice. J Biochem 2010; 147: 353-360.
25. Verreault M, Kaeding J, Caron P, et al. Regulation of endobiotics glucuronidation by ligand-activated transcription factors: Physiological function and therapeutic potential. Drug Metab Rev 2010; 42: 106-118.
26. Buckley DB, Klaassen CD. Mechanism of gender-divergent UDP-glucuronosyltransferase mRNA expression in mouse liver and kidney. Drug Metab Dispos 2009; 37: 834-840.
27. Stern ST, Tallman MN, Miles KK, Ritter JK, Smith PC. Androgen regulation of renal uridine diphosphoglucuronosyltransferase 1A1 in rats. Drug Metab Dispos 2008; 36: 1737-1739.
28. Barbier C, Bélanger A. Inactivation of androgens by UDP-glucuronosyltransferases in the human prostate. Best Pract Res Clin Endocrinol Metab 2008; 22: 259-270.
29. Sanada N, Gotoh Y, Shimazawa R, Klinge CM, Kizu R. Repression of activated aryl hydrocarbon receptor-induced transcriptional activation by 5α-dihydrotestosterone in human prostate cancer LNCaP and human breast cancer T47D cells. J Pharmacol Sci 2009; 109: 380-387.
30. Johnson AM, O'Connell MJ, Miyamoto H, et al. Androgenic dependence of exophytic tumor growth in a transgenic mouse model of bladder cancer: A role for thrombospondin-1. BMC Urol 2008; 8: 7.
31. Wu J-T, Han B-M, Yu S-Q, Wang H-P, Xia S-J. Androgen receptor is a potential therapeutic target for bladder cancer. Urology 2010; 75: 820-827.
32. Ito M, Yamamoto K, Maruo Y, Sato H, Fujiyama Y, Bamba T. Effect of a conserved mutation in uridine diphosphate glucuronosyltransferase 1A1 and 1A6 on glucuronidation of a metabolite of flutamide. Eur J Clin Pharmacol 2002; 58: 11-14.
33. Coe KJ, Nelson SD, Ulrich RG, et al. Profiling the hepatic effects of flutamide in rats: A microarray comparison with classical aryl hydrocarbon receptor ligands and atypical CYP1A inducers. Drug Metab Dispos 2006; 34: 1266-1275.
34. Tuygun C, Kankaya D, Imamoglu A, et al. Sex-specific hormone receptors in urothelial carcinomas of the human urinary bladder: A comparative analysis of clinicopathological features and survival outcomes according to receptor expression. Urol Oncol 2011; 29: 43-51.
35. Mir C, Shariat SF, van der Kwast TH, et al. Loss of androgen receptor expression is not associated with pathological stage, grade, gender or outcome in bladder cancer: A large multi-institutional study. BJU Int 2011; 108: 24-30.
36. Miyamoto H, Yao JL, Chaux AM, et al. Expression of androgen and oestrogen receptors and its prognostic significance in urothelial neoplasm of the urinary bladder. BJU Int 2011; In press.
37. Chen H, Yang K, Choi S, Fischer JH, Jeong H. Up-regulation of UDP-glucuronosyltransferase (UGT) 1A4 by 17β-estradiol: A potential mechanism of increased lamotrigine elimination in pregnancy. Drug Metab Dispos 2009; 37: 1841-1847.
38. Hu DG, Mackenzie PI. Estrogen receptor α, fos-related antigen-2, and c-Jun coordinately regulate human UDP glucuronosyltransferase 2B15 and 2B17 expression in response to 17β-estradiol in MCF-7cells. Mol Pharmacol 2009; 76: 425-439.
39. Scosyrev E, Noyes K, Feng C, Messing E. Sex and racial differences in bladder cancer presentation and mortality in the US. Cancer 2009; 115: 68-74.