Formation of tamoxifen-DNA adducts via O-sulfonation, not O-acetylation, of α-hydroxytamoxifen in rat and human livers

Drug Metabolism and Disposition

Volumn 33, Issue 11, 2005, Pages 1673-1678

  Sung, Yeon Kim ^a   Santosh Laxmi, Y R ^a   Suzuki, Naomi ^a   Ogura, Kenichiro ^b   Watabe, Tadashi ^b   Duffel, Michael W ^c   Shibutani, Shinya ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; ACYLTRANSFERASE; ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; ALPHA HYDROXYTAMOXIFEN; ARYLAMINE ACETYLTRANSFERASE; DNA; HYDROXYSTEROID SULFOTRANSFERASE; TAMOXIFEN; TAMOXIFEN DERIVATIVE; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA ADDUCT; ENZYME MECHANISM; HUMAN; LIVER CYTOSOL; NONHUMAN; PRIORITY JOURNAL; RAT; SULFONATION; TOXICOKINETICS;

ACETYLATION; ACETYLTRANSFERASES; ANIMALS; CYTOSOL; DNA ADDUCTS; FEMALE; HUMANS; LIVER; RATS; RATS, INBRED F344; SULFONES; SULFOTRANSFERASES; TAMOXIFEN;

ANIMALIA;

EID: 27544464442     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.105.005330     Document Type: Article

References (40)

1. Apak TI and Duffel MW (2004) Interactions of the stereoisomers of alpha-hydroxytamoxifen with human hydroxysteroid sulfotransferase SULT2A1 and rat hydroxysteroid sulfotransferase STa. Drug Metab Dispos 32:1501-1508.
2. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
3. Dasaradhi L and Shibutani S (1997) Identification of tamoxifen-DNA adducts formed by α-sulfate tamoxifen and α-acetoxytamoxifen. Chem Res Toxicol 10:189-196.
4. Davis W, Venitt S, and Phillips DH (1998) The metabolic activation of tamoxifen and alphahydroxytamoxifen to DNA-binding species in rat hepatocytes proceeds via sulphation. Carcinogenesis 19:861-866.
5. Etienne MC, Milano G, Fischel JL, Frenay M, Francois E, Formento JL, Gioanni J, and Namer M (1989) Tamoxifen metabolism: pharmacokinetic and in vitro study. Br J Cancer 60:30-35.
6. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, Vogel V, Robidoux A, Dimitrov N, Atkins J, et al. (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.
7. Gamboa da Costa G, Hamilton LP, Beland FA, and Marques MM (2000) Characterization of the major DNA adduct formed by α-hydroxy-N- desmethyltamoxifen in vitro and in vivo. Chem Res Toxicol 13:200-207.
8. Geese WJ and Blanchard R (2001) Biochemical characterization and tissue distribution of human SULT2B1. Biochem Biophys Res Commun 288:280-289.
9. Glatt H, Davis W, Meinl W, Hermersdorfer H, Venitt S, and Phillips D (1998) Rat, but not human, sulfotransferase activates a tamoxifen metabolite to produce DNA adducts and gene mutations in bacteria and mammalian cells in culture. Carcinogenesis 19:1709-1713.
10. Han X and Liehr JG (1992) Induction of covalent DNA adducts in rodents by tamoxifen. Cancer Res 52:1360-1363.
11. Hard GC, Iatropoulos MJ, Jordan K, Radi L, Kaltenberg OP, Imondi AR, and Williams GM (1993) Major difference in the hepatocarcinogenicity and DNA adduct forming ability between toremifene and tamoxifen in female Crl:CD(BR) rats. Cancer Res 53:4534-4541.
12. IARC (1996) Monographs on the Evaluation of Carcinogenic Risks to Humans: Some Pharmaceutical Drugs, vol 66, International Agency for Research on Cancer, Lyon, France.
13. Jacolot F, Simon I, Dreano Y, Beaune P, Riche C, and Berthou F (1991) Identification of the cytochrome P-450 IIIA family as the enzymes involved in the N-demethylation of tamoxifen in human liver microsomes. Biochem Pharmacol 41:1911-1919.
14. Kim SY, Suzuki N, Laxmi YR, McGarrigle BP, Olson JR, Sharma M, Sharma M, and Shibutani S (2005) Formation of tamoxifen-DNA adducts in human endometrial explants exposed to α-hydroxytamoxifen. Chem Res Toxicol 18:889-895.
15. Kim SY, Suzuki N, Laxmi YRS, and Shibutani S (2004) Genotoxic mechanism of tamoxifen in developing endometrial cancer. Drug Metab Rev 36:199-218.
16. Kitagawa M, Ravindernath A, Suzuki N, Rieger R, Terashima I, Umemoto A, and Shibutani S (2000) Identification of tamoxifen-DNA adducts induced by α-acetoxy-N-desmethyltamoxifen. Chem Res Toxicol 13:761-769.
17. Land SJ, Zukowski K, Lee MS, Debiec-Rychter M, King CM, and Wang CY (1989) Metabolism of aromatic amines: relationships of N-acetylation, O-acetylation, N,O-acetyltransfer and deacetylation in human liver and urinary bladder. Carcinogenesis 10:727-731.
18. Lien EA, Solheim E, and Ueland PM (1991) Distribution of tamoxifen and its metabolites in rat and human tissues during steady-state treatment. Cancer Res 51:4837-4844.
19. Maiti S and Chen G (2003) Tamoxifen induction of aryl sulfotransferase and hydroxysteroid sulfotransferase in male and female rat liver and intestine. Drug Metab Dispos 31:637-644.
20. Martin EA, Brown K, Gaskell M, Al-Azzawi F, Garner RC, Boocock DJ, Mattock E, Pring DW, Dingley K, Turteltaub KW, et al. (2003) Tamoxifen DNA damage detected in human endometrium using accelerator mass spectrometry. Cancer Res 63:8461-8465.
21. 32P-Postlabelled DNA adducts in liver obtained from women treated with tamoxifen. Carcinogenesis 16:1651-1654.
22. Ogura K, Sohtome T, Sugiyama A, Okuda H, Hiratsuka A, and Watabe T (1990) Rat liver cytosolic hydroxysteroid sulfotransferase (sulfotransferase a) catalyzing the formation of reactive sulfate esters from carcinogenic polycyclic hydroxymethylarenes. Mol Pharmacol 37:848-854.
23. Osborne CK (1998) Tamoxifen in the treatment of breast cancer. N Engl J Med 339:1609-1617.
24. Osborne MR, Hewer A, Hardcastle IR, Carmichael PL, and Phillips DH (1996) Identification of the major tamoxifen-deoxyguanosine adduct formed in the liver DNA of rats treated with tamoxifen. Cancer Res 56:66-71.
25. Phillips DH, Carmichael PL, Hewer A, Cole KJ, and Poon GK (1994) α-Hydroxytamoxifen, a metabolite of tamoxifen with exceptionally high DNA-binding activity in rat hepatocytes. Cancer Res 54:5518-5522.
26. 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.
27. Rubin GL, Harrold AJ, Mills JA, Falany CN, and Coughtrie MW (1999) Regulation of sulphotransferase expression in the endometrium during the menstrual cycle, by oral contraceptives and during early pregnancy. Mol Hum Reprod 5:995-1002.
28. Schild LJ, Divi RL, Beland FA, Churchwell MI, Doerge DR, Gamboa da Costa G, Marques MM, and Poirier MC (2003) Formation of tamoxifen-DNA adducts in multiple organs of adult female cynomolgus monkeys dosed with tamoxifen for 30 days. Cancer Res 63:5999-6003.
29. Sheng JJ and Duffel MW (2001) Bacterial expression, purification and characterization of rat hydroxysteroid sulfotransferase STa. Protein Expr Purif 21:235-242.
30. Shibutani S, Dasaradhi L, Terashima I, Banoglu E, and Duffel MW (1998a) α-Hydroxytamoxifen is a substrate of hydroxysteroid (alcohol) sulfotransferase, resulting in tamoxifen DNA adducts. Cancer Res 58:647-653.
31. 32P-postlabeling analysis. Proc Am Assoc Cancer Res 43:1042.
32. Shibutani S, Ravindernath A, Suzuki N, Terashima I, Sugarman SM, Grollman AP, and Pearl ML (2000) Identification of tamoxifen-DNA adducts in the endometrium of women treated with tamoxifen. Carcinogenesis 21:1461-1467.
33. Shibutani S, Ravindernath A, Terashima I, Suzuki N, Laxmi YR, Kanno Y, Suzuki M, Apak TI, Sheng JJ, and Duffel MW (2001) Mechanism of lower genotoxicity of toremifene compared with tamoxifen. Cancer Res 61:3925-3931.
34. Shibutani S, Shaw P, Suzuki N, Dasaradhi L, Duffel MW, and Terashima I (1998b) Sulfation of α-hydroxytamoxifen catalyzed by human hydroxysteroid sulfotransferase results in tamoxifen DNA adducts. Carcinogenesis 19:2007-2011.
35. Shibutani S, Suzuki N, Laxmi YR, Schild LJ, Divi LJ, Divi RL, Grollman AP, and Poirier MC (2003) Identification of tamoxifen-DNA adducts in monkeys treated with tamoxifen. Cancer Res 63:4402-4406.
36. 32P- Postlabeling/polyacrylamide gel electrophoresis analysis: application to the detection of DNA adducts. Chem Res Toxicol 15:305-311.
37. Umemoto A, Kajikawa A, Tanaka M, Hamada K, Seraj MJ, Kubota A, Nakayama M, Kinouchi T, Ohnishi Y, Yamashita K, and Monden Y (1994) Presence of mucosa-specific DNA adduct in human colon: possible implication for colorectal cancer. Carcinogenesis 15:901-905.
38. Umemoto A, Komaki K, Monden Y, Suwa M, Kanno Y, Kitagawa M, Suzuki M, Lin CX, Ueyama Y, Momen MA, et al. (2001) Identification and quantification of tamoxifen-DNA adducts in the liver of rats and mice. Chem Res Toxicol 14:1006-1013.
39. Umemoto A, Monden Y, Komaki K, Suwa M, Kanno Y, Suzuki M, Lin CX, Ueyama Y, Momen MA, Ravindernath A, and Shibutani S (1999) Tamoxifen-DNA adducts formed by α-acetoxytamoxifen N-oxide. Chem Res Toxicol 12:1083-1089.
40. van Leeuwen FE, Benraadt J, Coebergh JW, Kiemeney LA, Gimbrere CH, Otter R, Schouten LJ, Damhuis RA, Bontenbal M, Diepenhorst FW, et al. (1994) Risk of endometrial cancer after tamoxifen treatment of breast cancer. Lancet 343:448-452.