Differences in metabolite-mediated toxicity of tamoxifen in rodents versus humans elucidated with DNA/microsome electro-optical arrays and nanoreactors

Chemical Research in Toxicology

Volumn 22, Issue 2, 2009, Pages 341-347

  Zhao, Linlin ^a   Krishnan, Sadagopan ^a   Zhang, Yun ^a   Schenkman, John B ^b   Rusling, James F ^a,b  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYTAMOXIFEN; ALPHA HYDROXYTAMOXIFEN; DNA; DRUG METABOLITE; GLUCURONOSYLTRANSFERASE; LIVER ENZYME; NANOPARTICLE; POLYMER; RUTHENIUM; SILICON DIOXIDE; TAMOXIFEN; TAMOXIFEN N OXIDE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCURONIC ACID;

ANIMAL CELL; ARTICLE; CATALYSIS; CHEMOLUMINESCENCE; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DETOXIFICATION; DNA DAMAGE; ENZYME MECHANISM; ENZYME METABOLISM; FILM; GENOTOXICITY; GLUCURONIDATION; HUMAN; HUMAN CELL; LIGHT; LIQUID CHROMATOGRAPHY; LIVER CARCINOMA; LIVER MICROSOME; MICROSOME; NANOREACTOR; NONHUMAN; OXIDATION; RAT; REACTION TIME; REACTOR; RISK; RODENT; TANDEM MASS SPECTROMETRY; TURNOVER TIME;

ANIMALS; ANTINEOPLASTIC AGENTS; CHEMILUMINESCENT MEASUREMENTS; DNA; DNA ADDUCTS; DNA DAMAGE; ELECTROCHEMICAL TECHNIQUES; GLUCURONOSYLTRANSFERASE; HUMANS; MICROSOMES, LIVER; NANOTECHNOLOGY; OPTICS AND PHOTONICS; RATS; SPECIES SPECIFICITY; TAMOXIFEN; TOXICITY TESTS;

RATTUS; RODENTIA;

EID: 62249123949     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx8004295     Document Type: Article

References (38)

1. Jordan, V. C. (2003) Tamoxifen: A most unlikely pioneering medicine. Nat. Rev. Drug Discovery 2, 205-213.
2. White, I. N. H. (2003) Tamoxifen: Is it safe? Comparison of activation and detoxication mechanisms in rodents and in humans. Curr. Drug Metab. 4, 223-239.
3. Fisher, B., Costantino, J. P., Wickerham, D. L., Redmond, C. K., Kavanah, M., Cronin, W. M., Vogel, V., Robidoux, A., Dimitrov, N., Atkins, J., Daly, M., Wieand, S., Tan-Chiu, E., Ford, L., and Wolmark, N. (1998) Tamoxifen for prevention of breast cancer Report of the National Surgical Adjuvant Breast and Bowel Project P-1 study. J. Natl. Cancer Inst. 90, 1371-1388.
4. Greaves, P., Goonetilleke, R., Nunn, G., Topham, J., and Orton, T. (1993) 2-Year carcinogenicity study of tamoxifen in Alderley-Park Wistar-derived rats. Cancer Res. 53, 3919-3924.
5. Fisher, B., Costantino, J. P., Redmond, C. K., Fisher, E. R., Wickerham, D. L., Cronin, W. M., Bowman, D., Couture, J., Dimitrov, N. V., Evans, J., Farrar, W., Kavanah, M., Lickley, H. L., Margolese, R., Paterson, A. H. G., Robidoux, A., Shibata, H., and Terz, J. (1994) Endometrial cancer in tamoxifen-treated breast-cancer patients: Findings from the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-14. J. Natl. Cancer Inst. 86, 527-537.
6. Rutqvist, L. E., Johansson, H., Signomklao, T., Johansson, U., Fornander, T., and Wilking, N. (1995) Adjuvant tamoxifen therapy for early-stage breast-cancer and 2nd primary malignancies. J. Natl. Cancer Inst. 87, 645-651.
7. Carmichael, P. L., Ugwumadu, A. H. N., Neven, P., Hewer, A. J., Poon, G. K., and Phillips, D. H. (1996) Lack of genotoxicity of tamoxifen in human endometrium. Cancer Res. 56, 1475-1479.
8. Carmichael, P. L., Sardar, S., Crooks, N., Neven, P., Van Hoof, I., Ugwumadu, A., Bourne, T., Tomas, E., Hellberg, P., Hewer, A. J., and Phillips, D. H. (1999) Lack of evidence from HPLC P-32-post-labelling for tamoxifen-DNA adducts in the human endometrium. Carcinogenesis 20, 339-342.
9. Beland, F. A., Churchwell, M. I., Doerge, D. R., Parkin, D. R., Malejka-Giganti, D., Hewer, A., Phillips, D. H., Carmichael, P. L., da Costa, G. G., and Marques, M. M. (2004) Electrospray ionization-tandem mass spectrometry and P-32-postlabeling analyses of tamoxifen-DNA adducts in humans. J. Natl. Cancer Inst. 96, 1099-1104.
10. Shibutani, S., Ravindernath, A., Suzuki, N., Terashima, I., Sugarman, S. M., Grollman, A. P., and Pearl, M. L. (2000) Identification of tamoxifen-DNA adducts in the endometrium of women treated with tamoxifen. Carcinogenesis 21, 1461-1467.
11. Hemminki, K., Rajaniemi, H., Lindahl, B., and Moberger, B. (1996) Tamoxifen-induced DNA adducts in endometrial samples from breast cancer patients. Cancer Res. 56, 4374-4377.
12. Shibutani, S., Suzuki, N., Terashima, I., Sugarman, S. M., Grollman, A. P., and Pearl, M. L. (1999) Tamoxifen-DNA adducts detected in the endometrium of women treated with tamoxifen. Chem. Res. Toxicol. 12, 646-653.
13. Martin, E. A., Brown, K., Gaskell, M., Al-Azzawi, F., Garner, R. C., Boocock, D. J., Mattock, E., Pring, D. W., Dingley, K., Turteltaub, K. W., Smith, L. L., and White, I. N. H. (2003) Tamoxifen DNA damage detected in human endometrium using accelerator mass spectrometry. Cancer Res. 63, 8461-8465.
14. Poon, G. K., Cui, Y. C., McCague, R., Lonning, P. E., Feng, R., Rowlands, M. G., and Jarman, M. (1993) Analysis of phase I and phase II metabolites of tamoxifen in breast cancer patients. Drug Metab. Dispos. 21, 1119-1124.
15. Poon, G. K., Walter, B., Lonning, P. E., Horton, M. N., and McCague, R. (1995) Identification of tamoxifen metabolites in human Hep G2 cell-line, human liver homogenate, and patients on long-term therapy for breast-cancer. Drug Metab. Dispos. 23, 377-382.
16. Davis, W., Venitt, S., and Phillips, D. H. (1998) The metabolic activation of tamoxifen and alpha-hydroxytamoxifen to DNA-binding species in rat hepatocytes proceeds via sulphation. Carcinogenesis 19, 861-866.
17. Shibutani, S., Shaw, P. M., Suzuki, N., Dasaradhi, L., Duffel, M. W., and Terashima, I. (1998) Sulfation of alpha-hydroxytamoxifen catalyzed by human hydroxysteroid sulfotransferase results in tamoxifen-DNA adducts. Carcinogenesis 19, 2007-2011.
18. Osborne, M. R., Hewer, A., Hardcastle, I. R., Carmichael, P. L., and Phillips, D. H. (1996) Identification of the major tamoxifen-deoxyguanosine adduct formed in the liver DNA of rats treated with tamoxifen. Cancer Res. 56, 66-71.
19. Beland, F. A., McDaniel, L. P., and Marques, M. M. (1999) Comparison of the DNA adducts formed by tamoxifen and 4-hydroxytamoxifen in vivo. Carcinogenesis 20, 471-477.
20. Kaku, T., Ogura, K., Nishiyama, T., Ohnuma, T., Muro, K., and Hiratsuka, A. (2004) Quaternary ammonium-linked glucuronidation of tamoxifen by human liver microsomes and UDP-glucuronosyl-transferase 1A4. Biochem. Pharmacol. 67, 2093-2102.
21. Boocock, D. J., Maggs, J. L., Brown, K., White, I. N. H., and Park, B. K. (1999) Glucuronylation of alpha-hydroxytamoxifen: a deactivation pathway in humans? Br. J. Clin. Pharmacol. 47, 578-579.
22. Sun, D. X., Chen, G., Dellinger, R. W., Duncan, K., Fang, J. L., and Lazarus, P. (2006) Characterization of tamoxifen and 4-hydroxytamoxifen glucuronidation by human UGT1A4 variants. Breast Cancer Res. 8, R50.
23. Phillips, D. H. (2001) Understanding the genotoxicity of tamoxifen? Carcinogenesis 22, 839-849.
24. Umemoto, A., Komaki, K., Monden, Y., Suwa, M., Kanno, Y., Kitagawa, M., Suzuki, M., Lin, C. X., Ueyama, Y., Momen, M. A., Ravindemath, A., and Shibutani, S. (2001) Identification and quantification of tamoxifen-DNA adducts in the liver of rats and mice. Chem. Res. Toxicol. 14, 1006-1013.
25. Boocock, D. J., Maggs, J. L., White, I. N. H., and Park, B. K. (1999) Alpha-hydroxytamoxifen, a genotoxic metabolite of tamoxifen in the rat: identification and quantification in vivo and in vitro. Carcinogenesis 20, 153-160.
26. Boocock, D. J., Maggs, J. L., Brown, K., White, I. N. H., and Park, B. K. (2000) Major inter-species differences in the rates of O-sulphonation and O-glucuronylation of alpha-hydroxytamoxifen in vitro: a metabolic disparity protecting human liver from the formation of tamoxifen-DNA adducts. Carcinogenesis 21, 1851-1858.
27. (a) Hvastkovs, E. G., So, M., Krishnan, S., Bajrami, B., Tarun, M., Jansson, I., Schenkman, J. B., and Rusling, J. F. (2007) Electrochemiluminescent arrays for cytochrome P450-activated genotoxicity screening. DNA damage from benzo[a]pyrene metabolites. Anal. Chem. 79, 1897-1906.
28. (b) Yang, J., Wang, B., and Rusling, J. F. (2005) Genotoxicity sensor response correlated with DNA nucleobase damage rates. Mol. BioSyst. 1, 251-259.
29. Krishnan, S., Hvastkovs, E. G., Bajrami, B., Choudhary, D., Schenkman, J. B., and Rusling, J. F. (2008) Synergistic metabolic toxicity screening using microsome/DNA electrochemiluminescent arrays and nanoreactors. Anal. Chem. 80, 5279-5285.
30. Krishnan, S., Hvastkovs, E. G., Bajrami, B., Jansson, I., Schenkman, J. B., and Rusling, J. F. (2007) Genotoxicity screening for N-nitroso compounds. Electrochemical and electrochemiluminescent detection of human enzyme-generated DNA damage from N-nitrosopyrrolidine. Chem. Commun. 1713-1715.
31. Rusling, J. F., Hvastkovs, E. G., Hull, D. O., and Schenkman, J. B. (2008) Biochemical applications of ultrathin films of enzymes, polyions and DNA. Chem. Commun. 141-154.
32. Dennany, L., Forster, R. J., and Rusling, J. F. (2003) Simultaneous direct electrochemiluminescence and catalytic voltammetry detection of DNA in ultrathin films. J. Am. Chem. Soc. 125, 5213-5218.
33. Kim, S. Y., Laxmi, Y. R. S., Suzuki, N., Ogura, K., Watabe, T., Duffel, M. W., and Shibutani, S. (2005) Formation of tamoxifen-DNA adducts via O-sulfonation, not O-acetylation, of alpha-hydroxytamoxifen in rat and human livers. Drug Metab. Dispos. 33, 1673-1678.
34. Rajaniemi, H., Rasanen, I., Koivisto, P., Peltonen, K., and Hemminki, K. (1999) Identification of the major tamoxifen-DNA adducts in rat liver by mass spectroscopy. Carcinogenesis 20, 305-309.
35. da Costa, G. G., Marques, M. M., Beland, F. A., Freeman, J. P., Churchwell, M. I., and Doerge, D. R. (2003) Quantification of tamoxifen DNA adducts using on-line sample preparation and HPLC-electrospray ionization tandem mass spectrometry. Chem. Res. Toxicol. 16, 357-366.
36. Pathak, D. N., Pongracz, K., and Bodell, W. J. (1995) Microsomal and peroxidase activation of 4-hydroxy-tamoxifen to form DNA-adducts - comparison with DNA-adducts formed in Sprague-Dawley rats treated with tamoxifen. Carcinogenesis 16, 11-15.
37. Lim, C. K., Yuan, Z. X., Lamb, J. H., White, I. N. H., Dematteis, F., and Smith, L. L. (1994) A comparative study of tamoxifen metabolism in female rat, mouse and human liver-microsomes. Carcinogenesis 15, 589-593.
38. Bajrami, B., Krishnan, S., and Rusling, J. F. (2008) Microsome biocolloids for rapid drug metabolism and inhibition assessment by LC-MS. Drug Metab. Lett. 2, 158-162.