Long-term estrogen exposure promotes carcinogen bioactivation, induces persistent changes in gene expression, and enhances the tumorigenicity of MCF-7 human breast cancer cells

Toxicology and Applied Pharmacology

Volumn 240, Issue 3, 2009, Pages 355-366

  Spink, Barbara C ^a   Bennett, James A ^b   Pentecost, Brian T ^a,c   Lostritto, Nicole ^b   Englert, Neal A ^a,c   Benn, Geoffrey K ^a   Goodenough, Angela K ^a   Turesky, Robert J ^a,c   Spink, David C ^a,c  

^a WADSWORTH CENTER   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Benzo(a)pyrene; Breast cancer; DNA adducts; Long term estrogen exposure; MCF 7 cells

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FULVESTRANT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOGENESIS; CARCINOGEN DNA INTERACTION; CARCINOGENICITY; CELL STRAIN MCF 7; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; LONG TERM EXPOSURE; MOUSE; NONHUMAN; PROMOTER REGION; SCID MOUSE; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION; TUMOR GROWTH; TUMOR XENOGRAFT;

ARYL HYDROCARBON HYDROXYLASES; BASE SEQUENCE; BIOTRANSFORMATION; BREAST NEOPLASMS; CARCINOGENS; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; CYTOCHROME P-450 CYP1A1; DNA ADDUCTS; DNA PRIMERS; ESTRADIOL; ESTROGEN RECEPTOR MODULATORS; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

MUS;

EID: 70349759331     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.07.013     Document Type: Article

References (86)

1. Amlal H., Faroqui S., Balasubramaniam A., and Sheriff S. Estrogen up-regulates neuropeptide Y Y1 receptor expression in a human breast cancer cell line. Cancer Res. 66 (2006) 3706-3714
2. Balu N., Padgett W.T., Lambert G.R., Swank A.E., Richard A.M., and Nesnow S. Identification and characterization of novel stable deoxyguanosine and deoxyadenosine adducts of benzo[a]pyrene-7,8-quinone from reactions at physiological pH. Chem. Res. Toxicol. 17 (2004) 827-838
3. Beland F.A., Churchwell M.I., Von Tungeln L.S., Chen S., Fu P.P., Culp S.J., Schoket B., Gyorffy E., Minarovits J., Poirier M.C., Bowman E.D., Weston A., and Doerge D.R. High-performance liquid chromatography electrospray ionization tandem mass spectrometry for the detection and quantitation of benzo[a]pyrene-DNA adducts. Chem. Res. Toxicol. 18 (2005) 1306-1315
4. Bennett J.A., DeFreest L., Anaka I., Saadati H., Balulad S., Jacobson H.I., and Andersen T.T. AFPep: an anti-breast cancer peptide that is orally active. Breast Cancer Res. Treat. 98 (2006) 133-141
5. Bessette E.E., Fasco M.J., Pentecost B.T., and Kaminsky L.S. Mechanisms of arsenite-mediated decreases in benzo[k]fluoranthene-induced human cytochrome P4501A1 levels in HepG2 cells. Drug Metab. Dispos. 33 (2005) 312-320
6. Bourdeau V., Deschenes J., Metivier R., Nagai Y., Nguyen D., Bretschneider N., Gannon F., White J.H., and Mader S. Genome-wide identification of high-affinity estrogen response elements in human and mouse. Mol. Endocrinol. 18 (2004) 1411-1427
7. Brody J.G., Moysich K.B., Humblet O., Attfield K.R., Beehler G.P., and Rudel R.A. Environmental pollutants and breast cancer: epidemiologic studies. Cancer 109 Suppl. 12 (2007) 2667-2711
8. Buzdar A.U., Coombes R.C., Goss P.E., and Winer E.P. Summary of aromatase inhibitor clinical trials in postmenopausal women with early breast cancer. Cancer 112 (2008) 700-709
9. Cavailles V., Augereau P., Garcia M., and Rochefort H. Estrogens and growth factors induce the mRNA of the 52K-pro-cathepsin-D secreted by breast cancer cells. Nucleic Acids Res. 16 (1988) 1903-1919
10. Cheng A.S., Culhane A.C., Chan M.W., Venkataramu C.R., Ehrich M., Nasir A., Rodriguez B.A., Liu J., Yan P.S., Quackenbush J., Nephew K.P., Yeatman T.J., and Huang T.H. Epithelial progeny of estrogen-exposed breast progenitor cells display a cancer-like methylome. Cancer Res. 68 (2008) 1786-1796
11. Chen L., Devanesan P.D., Higginbotham S., Ariese F., Jankowiak R., Small G.J., Rogan E.G., and Cavalieri E.L. Expanded analysis of benzo[a]pyrene-DNA adducts formed in vitro and in mouse skin: their significance in tumor initiation. Chem. Res. Toxicol. 9 (1996) 897-903
12. Chun Y.J., Kim S., Kim D., Lee S.K., and Guengerich F.P. A new selective and potent inhibitor of human cytochrome P450 1B1 and its application to antimutagenesis. Cancer Res. 61 (2001) 8164-8170
13. Clamp A., Danson S., and Clemons M. Hormonal risk factors for breast cancer: identification, chemoprevention, and other intervention strategies. Lancet Oncol. 3 (2002) 611-619
14. Clemons M., and Goss P. Estrogen and the risk of breast cancer. N. Engl. J. Med. 344 (2001) 276-285
15. Coser K.R., Chesnes J., Hur J., Ray S., Isselbacher K.J., and Shioda T. Global analysis of ligand sensitivity of estrogen inducible and suppressible genes in MCF7/BUS breast cancer cells by DNA microarray. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 13994-13999
16. Cunliffe H.E., Ringner M., Bilke S., Walker R.L., Cheung J.M., Chen Y., and Meltzer P.S. The gene expression response of breast cancer to growth regulators: patterns and correlation with tumor expression profiles. Cancer Res. 63 (2003) 7158-7166
17. Dahlquist K.D., Salomonis N., Vranizan K., Lawlor S.C., and Conklin B.R. GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat. Genet. 31 (2002) 19-20
18. Davarinos N.A., and Pollenz R.S. Aryl hydrocarbon receptor imported into the nucleus following ligand binding is rapidly degraded via the cytosplasmic proteasome following nuclear export. J. Biol. Chem. 274 (1999) 28708-28715
19. Doniger S.W., Salomonis N., Dahlquist K.D., Vranizan K., Lawlor S.C., and Conklin B.R. MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol. 4 (2003) R7
20. Eliassen A.H., Missmer S.A., Tworoger S.S., Spiegelman D., Barbieri R.L., Dowsett M., and Hankinson S.E. Endogenous steroid hormone concentrations and risk of breast cancer among premenopausal women. J. Natl. Cancer Inst. 98 (2006) 1406-1415
21. Fisher B., Costantino J.P., Wickerham D.L., Cecchini R.S., Cronin W.M., Robidoux A., Bevers T.B., Kavanah M.T., Atkins J.N., Margolese R.G., Runowicz C.D., James J.M., Ford L.G., and Wolmark N. Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. J. Natl. Cancer Inst. 97 (2005) 1652-1662
22. Frasor J., Danes J.M., Komm B., Chang K.C., Lyttle C.R., and Katzenellenbogen B.S. Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 144 (2003) 4562-4574
23. Freedman O.C., Verma S., and Clemons M.J. Pre-menopausal breast cancer and aromatase inhibitors: treating a new generation of women. Breast Cancer Res. Treat. 99 (2006) 241-247
24. Ghosh M.G., Thompson D.A., and Weigel R.J. PDZK1 and GREB1 are estrogen-regulated genes expressed in hormone-responsive breast cancer. Cancer Res. 60 (2000) 6367-6375
25. (n) method for the characterization and quantification of 2′-deoxyguanosine adducts of the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by 2-D linear quadrupole ion trap mass spectrometry. Chem. Res. Toxicol. 20 (2007) 263-276
26. Goss P.E., Ingle J.N., Martino S., Robert N.J., Muss H.B., Piccart M.J., Castiglione M., Tu D., Shepherd L.E., Pritchard K.I., Livingston R.B., Davidson N.E., Norton L., Perez E.A., Abrams J.S., Cameron D.A., Palmer M.J., and Pater J.L. Randomized trial of letrozole following tamoxifen as extended adjuvant therapy in receptor-positive breast cancer: updated findings from NCIC CTG MA.17. J. Natl. Cancer Inst. 97 (2005) 1262-1271
27. Inadera H., Dong H.Y., and Matsushima K. WISP-2 is a secreted protein and can be a marker of estrogen exposure in MCF-7 cells. Biochem. Biophys. Res. Commun. 294 (2002) 602-608
28. Inoue A., Yoshida N., Omoto Y., Oguchi S., Yamori T., Kiyama R., and Hayashi S. Development of cDNA microarray for expression profiling of estrogen-responsive genes. J. Mol. Endocrinol. 29 (2002) 175-192
29. Inoue A., Omoto Y., Yamaguchi Y., Kiyama R., and Hayashi S.I. Transcription factor EGR3 is involved in the estrogen-signaling pathway in breast cancer cells. J. Mol. Endocrinol. 32 (2004) 649-661
30. Jönsson G., Staaf J., Olsson E., Heidenblad M., Vallon-Christersson J., Osoegawa K., de Jong P., Oredsson S., Ringner M., Höglund M., and Borg A. High-resolution genomic profiles of breast cancer cell lines assessed by tiling BAC array comparative genomic hybridization. Genes Chromosomes Cancer 46 (2007) 543-558
31. Jordan V.C. SERMs: meeting the promise of multifunctional medicines. J. Natl. Cancer Inst. 99 (2007) 350-356
32. Jordan V.C., and Brodie A.M. Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer. Steroids 72 (2007) 7-25
33. Kairouz R., Parmar J., Lyons R.J., Swarbrick A., Musgrove E.A., and Daly R.J. Hormonal regulation of the Grb14 signal modulator and its role in cell cycle progression of MCF-7 human breast cancer cells. J. Cell. Physiol. 203 (2005) 85-93
34. Kang S.C., and Lee B.M. Effect of estrogen receptor (ER) on benzo[a]pyrene-DNA adduct formation in human breast cancer cells. J. Toxicol. Environ. Health A 68 (2005) 1833-1840
35. Katzenellenbogen B.S., Kendra K.L., Norman M.J., and Berthois Y. Proliferation, hormonal responsiveness, and estrogen receptor content of MCF-7 human breast cancer cells grown in the short-term and long-term absence of estrogens. Cancer Res. 47 (1987) 4355-4360
36. Kenney N.J., Saeki T., Gottardis M., Kim N., Garcia-Morales P., Martin M.B., Normanno N., Ciardiello F., Day A., Cutler M.L., et al. Expression of transforming growth factor alpha antisense mRNA inhibits the estrogen-induced production of TGF alpha and estrogen-induced proliferation of estrogen-responsive human breast cancer cells. J. Cell. Physiol. 156 (1993) 497-514
37. Kuljukka-Rabb T., Peltonen K., Isotalo S., Mikkonen S., Rantanen L., and Savela K. Time- and dose-dependent DNA binding of PAHs derived from diesel particle extracts, benzo[a]pyrene and 5-methychrysene in a human mammary carcinoma cell line (MCF-7). Mutagenesis 16 (2001) 353-358
38. Labhart P., Karmakar S., Salicru E.M., Egan B.S., Alexiadis V., O'Malley B.W., and Smith C.L. Identification of target genes in breast cancer cells directly regulated by the SRC-3/AIB1 coactivator. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 1339-1344
39. Li S.H., Huang H.L., and Chen Y.H. Ovarian steroid-regulated synthesis and secretion of complement C3 and factor B in mouse endometrium during the natural estrous cycle and pregnancy period. Biol. Reprod. 66 (2002) 322-332
40. Lloyd D.R., and Hanawalt P.C. p53-dependent global genomic repair of benzo[a]pyrene-7,8-diol-9,10-epoxide adducts in human cells. Cancer Res. 60 (2000) 517-521
41. Martinez-Lacaci I., Saceda M., Plowman G.D., Johnson G.R., Normanno N., Salomon D.S., and Dickson R.B. Estrogen and phorbol esters regulate amphiregulin expression by two separate mechanisms in human breast cancer cell lines. Endocrinology 136 (1995) 3983-3992
42. McCoull K.D., Rindgen D., Blair I.A., and Penning T.M. Synthesis and characterization of polycyclic aromatic hydrocarbon o-quinone depurinating N7-guanine adducts. Chem. Res. Toxicol. 12 (1999) 237-246
43. McLachlan J.A., Burow M., Chiang T.C., and Li S.F. Gene imprinting in developmental toxicology: a possible interface between physiology and pathology. Toxicol. Lett. 120 (2001) 161-164
44. Middleton R.B., and Linder M.C. Synthesis and turnover of ceruloplasmin in rats treated with 17β-estradiol. Arch. Biochem. Biophys. 302 (1993) 362-368
45. Moog-Lutz C., Bouillet P., Regnier C.H., Tomasetto C., Mattei M.G., Chenard M.P., Anglard P., Rio M.C., and Basset P. Comparative expression of the psoriasin (S100A7) and S100C genes in breast carcinoma and co-localization to human chromosome 1q21-q22. Int. J. Cancer 63 (1995) 297-303
46. Nakamura T.J., Shinohara K., Funabashi T., and Kimura F. Effect of estrogen on the expression of Cry1 and Cry2 mRNAs in the suprachiasmatic nucleus of female rats. Neurosci. Res. 41 (2001) 251-255
47. Nardulli A.M., Greene G.L., O'Malley B.W., and Katzenellenbogen B.S. Regulation of progesterone receptor messenger ribonucleic acid and protein levels in MCF-7 cells by estradiol: analysis of estrogen's effect on progesterone receptor synthesis and degradation. Endocrinology 122 (1988) 935-944
48. Öberg M., Bergander L., Håkansson H., Rannug U., and Rannug A. Identification of the tryptophan photoproduct 6-formylindolo[3,2-b]carbazole, in cell culture medium, as a factor that controls the background aryl hydrocarbon receptor activity. Toxicol. Sci. 85 (2005) 935-943
49. Ochsner S.A., Steffen D.L., Hilsenbeck S.G., Chen E.S., Watkins C., and McKenna N.J. GEMS (Gene Expression MetaSignatures), a Web resource for querying meta-analysis of expression microarray datasets: 17β-estradiol in MCF-7 cells. Cancer Res. 69 (2009) 23-26
50. Pentecost B.T. Expression and estrogen regulation of the HEM45 MRNA in human tumor lines and in the rat uterus. J. Steroid Biochem. Mol. Biol. 64 (1998) 25-33
51. Petrocelli T., and Lye S.J. Regulation of transcripts encoding the myometrial gap junction protein, connexin-43, by estrogen and progesterone. Endocrinology 133 (1993) 284-290
52. Pulkrabek P., Leffler S., Grunberger D., and Weinstein I.B. Modification of deoxyribonucleic acid by a diol epoxide of benzo[a]pyrene. Relation to deoxyribonucleic acid structure and conformation and effects on transfectional activity. Biochemistry 18 (1979) 5128-5134
53. Quinn A.M., and Penning T.M. Comparisons of (+/-)-benzo[a]pyrene-trans-7,8-dihydrodiol activation by human cytochrome P450 and aldo-keto reductase enzymes: effect of redox state and expression levels. Chem. Res. Toxicol. 21 (2008) 1086-1094
54. Rachner T.D., Schoppet M., Niebergall U., and Hofbauer L.C. 17β-Estradiol inhibits osteoprotegerin production by the estrogen receptor-α-positive human breast cancer cell line MCF-7. Biochem. Biophys. Res. Commun. 368 (2008) 736-741
55. Ramet M., Castren K., Jarvinen K., Pekkala K., Turpeenniemi-Hujanen T., Soini Y., Paakko P., and Vahakangas K. p53 protein expression is correlated with benzo[a]pyrene-DNA adducts in carcinoma cell lines. Carcinogenesis 16 (1995) 2117-2124
56. Rasmussen U.B., Wolf C., Mattei M.G., Chenard M.P., Bellocq J.P., Chambon P., Rio M.C., and Basset P. Identification of a new interferon-alpha-inducible gene (p27) on human chromosome 14q32 and its expression in breast carcinoma. Cancer Res. 53 (1993) 4096-4101
57. Ryan T.J., Seeger J.I., Kumar S.A., and Dickerman H.W. Estradiol preferentially enhances extracellular tissue plasminogen activators of MCF-7 breast cancer cells. J. Biol. Chem. 259 (1984) 14324-14327
58. Sadler A.J., Pugazhendhi D., and Darbre P.D. Use of global gene expression patterns in mechanistic studies of oestrogen action in MCF7 human breast cancer cells. J. Steroid Biochem. Mol. Biol. 114 (2009) 21-32
59. Safe S., Wormke M., and Samudio I. Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J. Mammary Gland Biol. Neoplasia 5 (2000) 295-306
60. Santen R.J., Lobenhofer E.K., Afshari C.A., Bao Y., and Song R.X. Adaptation of estrogen-regulated genes in long-term estradiol deprived MCF-7 breast cancer cells. Breast Cancer Res. Treat. 94 (2005) 213-223
61. Sheikh M.S., Shao Z.M., Chen J.C., and Fontana J.A. Differential regulation of matrix Gla protein (MGP) gene expression by retinoic acid and estrogen in human breast carcinoma cells. Mol. Cell. Endocrinol. 92 (1993) 153-160
62. Shimada T., Hayes C.L., Yamazaki H., Amin S., Hecht S.S., Guengerich F.P., and Sutter T.R. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56 (1996) 2979-2984
63. Shimoya K., Zhang Q., Temma K., Kimura T., Tsujie T., Tsutsui T., Wasada K., Kanzaki T., Koyama M., and Murata Y. Secretory leukocyte protease inhibitor levels in cervicovaginal secretion of elderly women. Maturitas 54 (2006) 141-148
64. Sjöblom T., Jones S., Wood L.D., Parsons D.W., Lin J., Barber T.D., Mandelker D., Leary R.J., Ptak J., Silliman N., Szabo S., Buckhaults P., Farrell C., Meeh P., Markowitz S.D., Willis J., Dawson D., Willson J.K., Gazdar A.F., Hartigan J., Wu L., Liu C., Parmigiani G., Park B.H., Bachman K.E., Papadopoulos N., Vogelstein B., Kinzler K.W., and Velculescu V.E. The consensus coding sequences of human breast and colorectal cancers. Science 314 (2006) 268-274
65. Smith L.H., Coats S.R., Qin H., Petrie M.S., Covington J.W., Su M., Eren M., and Vaughan D.E. Differential and opposing regulation of PAI-1 promoter activity by estrogen receptor alpha and estrogen receptor beta in endothelial cells. Circ. Res. 95 (2004) 269-275
66. So A., Sinnemann S., Huntsman D., Fazli L., and Gleave M. Knockdown of the cytoprotective chaperone, clusterin, chemosensitizes human breast cancer cells both in vitro and in vivo. Mol. Cancer Ther. 4 (2005) 1837-1849
67. Soulez M., and Parker M.G. Identification of novel oestrogen receptor target genes in human ZR75-1 breast cancer cells by expression profiling. J. Mol. Endocrinol. 27 (2001) 259-274
68. Spink B.C., Hussain M.M., Katz B.H., Eisele L., and Spink D.C. Transient induction of cytochromes P450 1A1 and 1B1 in MCF-7 human breast cancer cells by indirubin. Biochem. Pharmacol. 66 (2003) 2313-2321
69. Spink D.C., Lincoln II D.W., Dickerman H.W., and Gierthy J.F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin causes an extensive alteration of 17β-estradiol metabolism in MCF-7 breast tumor cells. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 6917-6921
70. Spink D.C., Spink B.C., Cao J.Q., DePasquale J.A., Pentecost B.T., Fasco M.J., Li Y., and Sutter T.R. Differential expression of CYP1A1 and CYP1B1 in human breast epithelial cells and breast tumor cells. Carcinogenesis 19 (1998) 291-298
71. Spink D.C., Katz B.H., Hussain M.M., Pentecost B.T., Cao Z., and Spink B.C. Estrogen regulates Ah responsiveness in MCF-7 breast cancer cells. Carcinogenesis 24 (2003) 1941-1950
72. Spink D.C., Wu S.J., Spink B.C., Hussain M.M., Vakharia D.D., Pentecost B.T., and Kaminsky L.S. Induction of CYP1A1 and CYP1B1 by benzo(k)fluoranthene and benzo(a)pyrene in T-47D human breast cancer cells: roles of PAH interactions and PAH metabolites. Toxicol. Appl. Pharmacol. 226 (2008) 213-224
73. Stuckey R., Aldridge T., Lim F.L., Moore D.J., Tinwell H., Doherty N., Davies R., Smith A.G., Kimber I., Ashby J., Orphanides G., and Moggs J.G. Induction of iron homeostasis genes during estrogen-induced uterine growth and differentiation. Mol. Cell. Endocrinol. 253 (2006) 22-29
74. Sundstrom S.A., Komm B.S., Ponce-de-Leon H., Yi Z., Teuscher C., and Lyttle C.R. Estrogen regulation of tissue-specific expression of complement C3. J. Biol. Chem. 264 (1989) 16941-16947
75. Tamimi R.M., Byrne C., Colditz G.A., and Hankinson S.E. Endogenous hormone levels, mammographic density, and subsequent risk of breast cancer in postmenopausal women. J. Natl. Cancer Inst. 99 (2007) 1178-1187
76. The Adjuvant Breast Cancer Trials Collaborative Group. Ovarian ablation or suppression in premenopausal early breast cancer: results from the international adjuvant breast cancer ovarian ablation or suppression randomized trial. J. Natl. Cancer Inst. 99 (2007) 516-525
77. Turesky R.J., Rossi S.C., Welti D.H., Lay Jr. J.O., and Kadlubar F.F. Characterization of DNA adducts formed in vitro by reaction of N-hydroxy-2-amino-3-methylimidazo[4,5-f]quinoline and N-hydroxy-2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline at the C-8 and N2 atoms of guanine. Chem. Res. Toxicol. 5 (1992) 479-490
78. Vendrell J.A., Magnino F., Danis E., Duchesne M.J., Pinloche S., Pons M., Birnbaum D., Nguyen C., Theillet C., and Cohen P.A. Estrogen regulation in human breast cancer cells of new downstream gene targets involved in estrogen metabolism, cell proliferation and cell transformation. J. Mol. Endocrinol. 32 (2004) 397-414
79. Vogel V.G., Costantino J.P., Wickerham D.L., Cronin W.M., Cecchini R.S., Atkins J.N., Bevers T.B., Fehrenbacher L., Pajon Jr. E.R., Wade III J.L., Robidoux A., Margolese R.G., James J., Lippman S.M., Runowicz C.D., Ganz P.A., Reis S.E., McCaskill-Stevens W., Ford L.G., Jordan V.C., and Wolmark N. Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: the NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 trial. Jama 295 (2006) 2727-2741
80. Wen X., and Walle T. Cytochrome P450 1B1, a novel chemopreventive target for benzo[a]pyrene-initiated human esophageal cancer. Cancer Lett. 246 (2007) 109-114
81. Wittmann B.M., Sherk A., and McDonnell D.P. Definition of functionally important mechanistic differences among selective estrogen receptor down-regulators. Cancer Res. 67 (2007) 9549-9560
82. Wood L.D., Parsons D.W., Jones S., Lin J., Sjoblom T., Leary R.J., Shen D., Boca S.M., Barber T., Ptak J., Silliman N., Szabo S., Dezso Z., Ustyanksky V., Nikolskaya T., Nikolsky Y., Karchin R., Wilson P.A., Kaminker J.S., Zhang Z., Croshaw R., Willis J., Dawson D., Shipitsin M., Willson J.K., Sukumar S., Polyak K., Park B.H., Pethiyagoda C.L., Pant P.V., Ballinger D.G., Sparks A.B., Hartigan J., Smith D.R., Suh E., Papadopoulos N., Buckhaults P., Markowitz S.D., Parmigiani G., Kinzler K.W., Velculescu V.E., and Vogelstein B. The genomic landscapes of human breast and colorectal cancers. Science 318 (2007) 1108-1113
83. Yager J.D., and Davidson N.E. Estrogen carcinogenesis in breast cancer. N. Engl. J. Med. 354 (2006) 270-282
84. Yamamura J., Miyoshi Y., Tamaki Y., Taguchi T., Iwao K., Monden M., Kato K., and Noguchi S. mRNA expression level of estrogen-inducible gene, alpha 1-antichymotrypsin, is a predictor of early tumor recurrence in patients with invasive breast cancers. Cancer Sci. 95 (2004) 887-892
85. Zou E., and Matsumura F. Long-term exposure to beta-hexachlorocyclohexane (beta-HCH) promotes transformation and invasiveness of MCF-7 human breast cancer cells. Biochem. Pharmacol. 66 (2003) 831-840
86. Zschocke J., Manthey D., Bayatti N., van der Burg B., Goodenough S., and Behl C. Estrogen receptor alpha-mediated silencing of caveolin gene expression in neuronal cells. J. Biol. Chem. 277 (2002) 38772-38780