Investigating DNA adduct-targeted mutagenicity of tamoxifen: Preferential formation of tamoxifen-DNA adducts in the human p53 gene in SV40 immortalized hepatocytes but not endometrial carcinoma cells

Biochemistry

Volumn 44, Issue 23, 2005, Pages 8418-8427

  Besaratinia, Ahmad ^a   Pfeifer, Gerd P ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; BLOOD; CELLS; CHEMOTHERAPY; GENES; METABOLISM; MUTAGENESIS; TUMORS;

BREAST CANCER; CARCINOGENICITY; ENDOMETRIAL CANCER; TAMOXIFEN THERAPY;

DNA;

NUCLEOTIDE; PROTEIN P53; TAMOXIFEN;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CARCINOGENICITY; CELL IMMORTALIZATION; CIRCULATION; CODON; DETOXIFICATION; DNA ADDUCT; DOSE RESPONSE; ENDOMETRIUM CARCINOMA; ESTROGEN ACTIVITY; EXON; FIBROBLAST; HUMAN; HUMAN CELL; LIVER CELL; MITOSIS; MOUSE; MUTAGENICITY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TRANSGENE; TUMOR SUPPRESSOR GENE;

ANIMALS; BACTERIOPHAGE LAMBDA; BASE SEQUENCE; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; DNA ADDUCTS; DNA MUTATIONAL ANALYSIS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOMETRIAL NEOPLASMS; FEMALE; GENE FREQUENCY; GENES, P53; HEPATOCYTES; HUMANS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS; SIMIAN VIRUS 40; TAMOXIFEN; TRANSCRIPTION FACTORS; TRANSGENES; VIRAL PROTEINS;

EID: 20444370676     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0503753     Document Type: Article

References (86)

1. White, I. N. (1999) The tamoxifen dilemma, Carcinogenesis 20, 1153-1160.
2. Phillips, D. H. (2001) Understanding the genotoxicity of tamoxifen? Carcinogenesis 22, 839-849.
3. White, I. N. (2003) Tamoxifen: Is it safe? Comparison of activation and detoxication mechanisms in rodents and in humans, Curr. Drug Metab. 4, 223-239.
4. Greaves, P., Goonetilleke, R., Nunn, G., Topham, J., and Orton, T. (1993) Two-year carcinogenicity study of tamoxifen in Alderley Park Wistar-derived rats, Cancer Res. 53, 3919-3924.
5. Carthew, P., Martin, E. A., White, I. N., De Matteis, F., Edwards, R. E., Dorman, B. M., Heydon, R. T., and Smith, L. L. (1995) Tamoxifen induces short-term cumulative DNA damage and liver tumors in rats: Promotion by phenobarbital, Cancer Res. 55, 544-547.
6. 32P-postlabelling in three rat strains exposed to dietary tamoxifen: The relationship between cell proliferation and liver tumour formation, Carcinogenesis 16, 1299-1304.
7. Davies, R., Oreffo, V. I., Martin, E. A., Festing, M. F., White, I. N., Smith, L. L., and Styles, J. A. (1997) Tamoxifen causes gene mutations in the livers of λ/lacI transgenic rats, Cancer Res. 57, 1288-1293.
8. Chen, T., Gamboa da Costa, G., Marques, M. M., Shelton, S. D., Beland, F. A., and Manjanatha, M. G. (2002) Mutations induced by α-hydroxytamoxifen in the lacI and cII genes of Big Blue transgenic rats, Carcinogenesis 23, 1751-1757.
9. White, I. N., de Matteis, F., Davies, A., Smith, L. L., Crofton-Sleigh, C., Venitt, S., Hewer, A., and Phillips, D. H. (1992) Genotoxic potential of tamoxifen and analogues in female Fischer F344/n rats, DBA/2 and C57BL/6 mice, and in human MCL-5 cells, Carcinogenesis 13, 2197-2203.
10. Martin, E. A., Carthew, P., White, I. N., Heydon, R. T., Gaskell, M., Mauthe, R. J., Turteltaub, K. W., and Smith, L. L. (1997) Investigation of the formation and accumulation of liver DNA adducts in mice chronically exposed to tamoxifen, Carcinogenesis 18, 2209-2215.
11. Newbold, R. R., Jefferson, W. N., Padilla-Burgos, E., and Bullock, B. C. (1997) Uterine carcinoma in mice treated neonatally with tamoxifen, Carcinogenesis 18, 2293-2298.
12. Carthew, P., Edwards, R. E., Nolan, B. M., Martin, E. A., Heydon, R. T., White, I. N., and Tucker, M. J. (2000) Tamoxifen induces endometrial and vaginal cancer in rats in the absence of endometrial hyperplasia, Carcinogenesis 21, 793-797.
13. Poirier, M. C. (2004) Chemical-induced DNA damage and human cancer risk, Nat. Rev. Cancer 4, 630-637.
14. Hussain, S. P., and Harris, C. C. (1998) Molecular epidemiology of human cancer: Contribution of mutation spectra studies of tumor suppressor genes, Cancer Res. 58, 4023-4037.
15. Besaratinia, A., and Pfeifer, G. P. (2005) DNA damage and mutagenesis induced by polycyclic aromatic hydrocarbons, in The Carcinogenic Effects of Polycyclic Aromatic Hydrocarbons (Luch, A., Ed.) pp 171-210, Imperial College Press, London, U.K.
16. Carmichael, P. L., Ugwumadu, A. H., 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.
17. 32P-post-labelling for tamoxifen-DNA adducts in the human endometrium, Carcinogenesis 20, 339-342.
18. 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.
19. Hemminki, K., Widlak, P., and Hou, S. M. (1995) DNA adducts caused by tamoxifen and toremifene in human microsomal system and lymphocytes in vitro, Carcinogenesis 16, 1661-1664.
20. Hemminki, K., Rajaniemi, H., Koskinen, M., and Hansson, J. (1997) Tamoxifen-induced DNA adducts in leucocytes of breast cancer patients, Carcinogenesis 18, 9-13.
21. 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.
22. 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.
23. 2-deoxyguanosinyl)tamoxifen lesions, the major DNA adducts detected in endometrial tissues of patients treated with tamoxifen, Cancer Res. 59, 2091-2095.
24. 32P-postlabelled DNA adducts in liver obtained from women treated with tamoxifen, Carcinogenesis 16, 1651-1654.
25. 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. (2003) Tamoxifen DNA damage detected in human endometrium using accelerator mass spectrometry, Cancer Res. 63, 8461-8465.
26. 32P-postlabeling, Biochem. Biophys. Res. Commun. 320, 297-302.
27. 32P-postlabeling analyses of tamoxifen-DNA adducts in humans, J. Natl. Cancer Inst. 96, 1099-1104.
28. Hainaut, P., and Hollstein, M. (2000) p53 and human cancer: The first ten thousand mutations, Adv. Cancer Res. 77, 81-137.
29. Vogelstein, B., and Kinzler, K. W. (2004) Cancer genes and the pathways they control, Nat. Med. 10, 789-799.
30. Olivier, M., Hussain, S. P., Caron de Fromentel, C., Hainaut, P., and Harris, C. C. (2004) TP53 mutation spectra and load: A tool for generating hypotheses on the etiology of cancer, IARC Sci. Publ. 247-270.
31. Besaratinia, A., and Pfeifer, G. P. (2003) Weak yet distinct mutagenicity of acrylamide in mammalian cells, J. Natl. Cancer Inst. 95, 889-896.
32. Lim, C. K., Yuan, Z. X., Lamb, J. H., White, I. N., De Matteis. F., and Smith, L. L. (1994) A comparative study of tamoxifen metabolism in female rat, mouse, and human liver microsomes, Carcinogenesis 15, 589-593.
33. Boocock, D. J., Maggs, J. L., White, I. N., and Park, B. K. (1999) α-Hydroxytamoxifen, a genotoxic metabolite of tamoxifen in the rat: Identification and quantification in vivo and in vitro, Carcinogenesis 20, 153-160.
34. Pfeifer, G. P., Chen, H. H., Komura, J., and Riggs, A. D. (1999) Chromatin structure analysis by ligation-mediated and terminal transferase-mediated polymerase chain reaction, Methods Enzymol. 304, 548-571.
35. Besaratinia, A., and Pfeifer, G. P. (2004) Genotoxicity of acrylamide and glycidamide, J. Natl. Cancer Inst. 96, 1023-1029.
36. Chen, H. H., Kontaraki, J., Bonifer, C., and Riggs, A. D. (2001) Terminal transferase-dependent PCR (TDPCR) for in vivo UV photofootprinting of vertebrate cells, Sci. STKE. PL1 (1-17).
37. Jakubczak, J. L., Merlino, G., French, J. E., Muller, W. J., Paul, B., Adhya, S., and Garges, S. (1996) Analysis of genetic instability during mammary tumor progression using a novel selection-based assay for in vivo mutations in a bacteriophage λ transgene target, Proc. Natl. Acad. Sci. U.S.A. 93, 9073-9078.
38. Herskowitz, I., and Hagen, D. (1980) The lysis-lysogeny decision of phage λ: Explicit programming and responsiveness, Annu. Rev. Genet. 14, 399-445.
39. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.
40. Adams, W. T., and Skopek, T. R. (1987) Statistical test for the comparison of samples from mutational spectra, J. Mol. Biol. 194, 391-396.
41. Besaratinia, A., Synold, T. W., Xi, B., and Pfeifer, G. P. (2004) G → T transversions and small tandem base deletions are the hallmark of mutations induced by ultraviolet A radiation in mammalian cells, Biochemistry 43, 8169-8177.
42. Harbach, P. R., Zimmer, D. M., Filipunas, A. L., Mattes, W. B., and Aaron, C. S. (1999) Spontaneous mutation spectrum at the λ cII locus in liver, lung, and spleen tissue of Big Blue transgenic mice, Environ. Mol. Mutagen. 33, 132-143.
43. Davies, R., Gant, T. W., Smith, L. L., and Styles, J. A. (1999) Tamoxifen induces G:C → T:A mutations in the cII gene in the liver of λ/lacI transgenic rats but not at 5′-CpG-3′ dinucleotide sequences as found in the lacI transgene, Carcinogenesis 20, 1351-1356.
44. Heddle, J. A., Martus, H. J., and Douglas, G. R. (2003) Treatment and sampling protocols for transgenic mutation assays, Environ. Mol. Mutagen. 41, 1-6.
45. Thybaud, V., Dean, S., Nohmi, T., de Boer, J., Douglas, G. R., Glickman, B. W., Gorelick, N. J., Heddle, J. A., Heflich, R. H., Lambert, I., Martus, H. J., Mirsalis, J. C., Suzuki, T., and Yajima, N. (2003) In vivo transgenic mutation assays, Mutat. Res. 540, 141-151.
46. Mellon, I., Spivak, G., and Hanawalt, P. C. (1987) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene, Cell 51, 241-249.
47. Hanawalt, P. C. (1994) Transcription-coupled repair and human disease, Science 266, 1957-1958.
48. Yoon, J. H., Smith, L. E., Feng, Z., Tang, M., Lee, C. S., and Pfeifer, G. P. (2001) Methylated CpG dinucleotides are the preferential targets for G → T transversion mutations induced by benzo[a]pyrene diol epoxide in mammalian cells: Similarities with the p53 mutation spectrum in smoking-associated lung cancers, Cancer Res. 61, 7110-7117.
49. 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.
50. Tornaletti, S., and Pfeifer, G. P. (1995) Complete and tissue-independent methylation of CpG sites in the p53 gene: Implications for mutations in human cancers, Oncogene 10, 1493-1499.
51. Davies, R., Oreffo, V. I., Bayliss, S., Dinh, P. A., Lilley, K. S., White, I. N., Smith, L. L., and Styles, J. A. (1996) Mutational spectra of tamoxifen-induced mutations in the livers of lacI transgenic rats, Environ. Mol. Mutagen. 28, 430-433.
52. Lowes, D. A., Brown, K., Heydon, R. T., Martin, E. A., and Gant, T. W. (1999) Site-specific tamoxifen-DNA adduct formation: Lack of correlation with mutational ability in Escherichia coli, Biochemistry 38, 10989-10996.
53. Styles, J. A., Davies, R., Fenwick, S., Walker, J., White, I. N., and Smith, L. L. (2001) Tamoxifen mutagenesis and carcinogenesis in livers of λ/lacI transgenic rats: Selective influence of phenobarbital promotion. Cancer Lett. 162, 117-122.
54. Yadollahi-Farsani, M., Davies, D. S., and Boobis, A. R. (2002) The mutational signature of α-hydroxytamoxifen at Hprt locus in Chinese hamster cells, Carcinogenesis 23, 1947-1952.
55. Vancutsem, P. M., Lazarus, P., and Williams, G. M. (1994) Frequent and specific mutations of the rat p53 gene in hepatocarcinomas induced by tamoxifen, Cancer Res. 54, 3864-3867.
56. 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.
57. Shibutani, S., Suzuki, N., Laxmi, Y. R., Schild, L. J., Divi, R. L., Grollman, A. P., and Poirier, M. C. (2003) Identification of tamoxifen-DNA adducts in monkeys treated with tamoxifen, Cancer Res. 63, 4402-4406.
58. 32P-postlabeling, Cancer Res. 59, 4829-4833.
59. Brown, K., Brown, J. E., Martin, E. A., Smith, L. L., and White, I. N. (1998) Determination of DNA damage in F344 rats induced by geometric isomers of tamoxifen and analogues, Chem. Res. Toxicol. 11, 521-534.
60. 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.
61. 2-Deoxyguanosinyl)tamoxifen, Biochemistry 36, 13010-13017.
62. 6-(2-hydroxyestron-6-yl)-2′-deoxyadenosine, Biochemistry 37, 13807-13815.
63. Dasaradhi, L., and Shibutani, S. (1997) Identification of tamoxifen-DNA adducts formed by α-sulfate tamoxifen and α-acetoxy-tamoxifen, Chem. Res. Toxicol. 10, 189-196.
64. Terashima, I., Suzuki, N., Itoh, S., Yoshizawa, I., and Shibutani, S. (1998) Mutagenic specificity of model estrogen-DNA adducts in mammalian cells, Biochemistry 37, 8803-8807.
65. Okubo, T., Nagai, F., Ushiyama, K., Yokoyama, Y., Ozawa, S., Kano, K., Tomita, S., Kubo, H., and Kano, I. (1998) DNA cleavage and 8- hydroxydeoxyguanosine formation caused by tamoxifen derivatives in vitro, Cancer Lett. 122, 9-15.
66. Wood, M. L., Dizdaroglu, M., Gajewski, E., and Essigmann, J. M. (1990) Mechanistic studies of ionizing radiation and oxidative mutagenesis: Genetic effects of a single 8-hydroxyguanine (7-hydro-8-oxoguanine) residue inserted at a unique site in a viral genome, Biochemistry 29, 7024-7032.
67. Shibutani, S., Takeshita, M., and Grollman, A. P. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG, Nature 349, 431-434.
68. Barbier, O., Albert, C., Martineau, I., Vallee, M., High, K., Labrie, F., Hum, D. W., Labrie, C., and Belanger, A. (2001) Glucuronidation of the nonsteroidal antiestrogen EM-652 (SCH 57068), by human and monkey steroid conjugating UDP-glucuronosyltransferase enzymes, Mol. Pharmacol. 59, 636-645.
69. Lepine, J., Bernard, O., Plante, M., Tetu, B., Pelletier, G., Labrie, F., Belanger, A., and Guillemette, C. (2004) Specificity and regioselectivity of the conjugation of estradiol, estrone, and their catecholestrogen and methoxyestrogen metabolites by human uridine diphospho-glucuronosyltransferases expressed in endometrium, J. Clin. Endocrinol. Metab. 89, 5222-5232.
70. Mulder, G. J. (1992) Glucuronidation and its role in regulation of biological activity of drugs, Annu. Rev. Pharmacol. Toxicol. 32, 25-49.
71. Pfeifer, A. M., Cole, K. E., Smoot, D. T., Weston, A., Groopman, J. D., Shields, P. G., Vignaud, J. M., Juillerat, M., Lipsky, M. M., Trump, B. F., et al. (1993) Simian virus 40 large tumor antigen-immortalized normal human liver epithelial cells express hepatocyte characteristics and metabolize chemical carcinogens, Proc. Natl. Acad. Sci. U.S.A. 90, 5123-5127.
72. Coller, J. K., Krebsfaenger, N., Klein, K., Endrizzi, K., Wolbold, R., Lang, T., Nussler, A., Neuhaus, P., Zanger, U. M., Eichelbaum, M., and Murdter, T. E. (2002) The influence of CYP2B6, CYP2C9, and CYP2D6 genotypes on the formation of the potent antioestrogen Z-4-hydroxy-tamoxifen in human liver, Br. J. Clin. Pharmacol. 54, 157-167.
73. Way, D. L., Grosso, D. S., Davis, J. R., Surwit, E. A., and Christian, C. D. (1983) Characterization of a new human endometrial carcinoma (RL95-2) established in tissue culture, In Vitro 19, 147-158.
74. Hendricks, D. T., Taylor, R., Reed, M., and Birrer, M. J. (1997) FHIT gene expression in human ovarian, endometrial, and cervical cancer cell lines. Cancer Res. 57, 2112-2115.
75. Klinge, C. M., Jernigan, S. C., and Risinger, K. E. (2002) The agonist activity of tamoxifen is inhibited by the short heterodimer partner orphan nuclear receptor in human endometrial cancer cells, Endocrinology 143, 853-867.
76. Grosso, D. S., and Way, D. L. (1984) Characterization of cytosolic estrogen sulfotransferase from RL95-2 endometrial cancer cells, J. Clin. Endocrinol. Metab. 59, 829-834.
77. Grese, T. A., Pennington, L. D., Sluka, J. P., Adrian, M. D., Cole, H. W., Fuson, T. R., Magee, D. E., Phillips, D. L., Rowley, E. R., Shetler, P. K., Short, L. L., Venugopalan, M., Yang, N. N., Sato, M., Glasebrook, A. L., and Bryant, H. U. (1998) Synthesis and pharmacology of conformationally restricted raloxifene analogues: Highly potent selective estrogen receptor modulators, J. Med. Chem. 41, 1272-1283.
78. Jana, N. R., Sarkar, S., Ishizuka, M., Yonemoto, J., Tohyama, C., and Sone, H. (1999) Role of estradiol receptor-α in differential expression of 2,3,7,8-tetrachlorodibenzo-p-dioxin-inducible genes in the RL95-2 and KLE human endometrial cancer cell lines, Arch. Biochem. Biophys. 368, 31-39.
79. Bao, H., Vepakomma, M., and Sarkar, M. A. (2002) Benzo[a]-pyrene exposure induces CYP1A1 activity and expression in human endometrial cells, J. Steroid Biochem. Mol. Biol. 81, 37-45.
80. Levesque, E., Beaulieu, M., Hum, D. W., and Belanger, A. (1999) Characterization and substrate specificity of UGT2B4 (E458): A UDP-glucuronosyltransferase encoded by a polymorphic gene, Pharmacogenetics 9, 207-216.
81. Feigelson, H. S., and Henderson, B. E. (2000) Future possibilities in the prevention of breast cancer: Role of genetic variation in breast cancer prevention, Breast Cancer Res. 2, 277-282.
82. Nowell, S., Sweeney, C., Winters, M., Stone, A., Lang, N. P., Hutchins, L. F., Kadlubar, F. F., and Ambrosone, C. B. (2002) Association between sulfotransferase 1A1 genotype and survival of breast cancer patients receiving tamoxifen therapy, J. Natl. Cancer Inst. 94, 1635-1640.
83. Miyoshi, Y., Ando, A., Hasegawa, S., Ishitobi, M., Yamamura, J., Irahara, N., Tanji, Y., Taguchi, T., Tamaki, Y., and Noguchi, S. (2003) Association of genetic polymorphisms in CYP19 and CYP1A1 with the oestrogen receptor-positive breast cancer risk, Eur. J. Cancer 39, 2531-2537.
84. Duguay, Y., McGrath, M., Lepine, J., Gagne, J. F., Hankinson, S. E., Colditz, G. A., Hunter, D. J., Plante, M., Tetu, B., Belanger, A., Guillemette, C., and De Vivo, I. (2004) The functional UGT1A1 promoter polymorphism decreases endometrial cancer risk, Cancer Res. 64, 1202-1207.
85. Phillips, D. H., Carmichael, P. L., Hewer, A., Cole, K. J., Hardcastle, I. R., Poon, G. K., Keogh, A., and Strain, A. J. (1996) Activation of tamoxifen and its metabolite α-hydroxytamoxifen to DNA-binding products: Comparisons between human, rat, and mouse hepatocytes, Carcinogenesis 17, 89-94.
86. Pathak, D. N., and Bodell, W. J. (1994) DNA adduct formation by tamoxifen with rat and human liver microsomal activation systems, Carcinogenesis 15, 529-532.