The xenoestrogen bisphenol a induces inappropriate androgen receptor activation and mitogenesis in prostatic adenocarcinoma cells

Molecular Cancer Therapeutics

Volumn 1, Issue 7, 2002, Pages 515-524

  Wetherill, Yelena B ^a   Petre, Christin E ^a   Monk, Kelly R ^a   Puga, Alvaro ^a   Knudsen, Karen E ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ANDROGEN RECEPTOR; ANDROSTANOLONE; BROXURIDINE; ESTROGEN; PHENOL DERIVATIVE;

ADENOCARCINOMA; ARTICLE; CELL CULTURE; CELL DIVISION; CELL NUCLEUS; DOSE RESPONSE; FLOW CYTOMETRY; HUMAN; IMMUNOBLOTTING; KINETICS; MALE; METABOLISM; PLASMID; PROSTATE TUMOR; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME;

ADENOCARCINOMA; BROMODEOXYURIDINE; CELL DIVISION; CELL NUCLEUS; DIHYDROTESTOSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGENS, NON-STEROIDAL; FLOW CYTOMETRY; GENES, REPORTER; HUMANS; IMMUNOBLOTTING; KINETICS; MALE; PHENOLS; PLASMIDS; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 0036559993     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Greenlee, R. T., Hill-Harmon, M. B., Murray, T., and Thun, M. Cancer statistics, 2001. CA Cancer J. Clin., 51: 15-36, 2001. (Pubitemid 32166444)
2. Trapman, J., and Brinkmann, A. O. The androgen receptor in prostate cancer. Pathol. Res. Pract., 192: 752-760, 1996. (Pubitemid 26302249)
3. Grossmann, M. E., Huang, H., and Tindall, D. J. Androgen receptor signaling in androgen-refractory prostate cancer. J. Natl. Cancer Inst., 93: 1687-1697, 2001. (Pubitemid 33130257)
4. Denis, L. J., and Griffiths, K. Endocrine treatment in prostate cancer. Semin. Surg. Oncol., 18: 52-74, 2000. (Pubitemid 30036120)
5. Leewansangtong, S., and Soontrapa, S. Hormonal ablation therapy for metastatic prostatic carcinoma: a review. J. Med. Assoc. Thai, 82: 192-205, 1999. (Pubitemid 29173889)
6. Klotz, L. Hormone therapy for patients with prostate carcinoma. Cancer (Phila.), 88: 3009-3014, 2000. (Pubitemid 30413184)
7. Labrie, F. Screening and early hormonal treatment of prostate cancer are accumulating strong evidence and support. Prostate, 43: 215-222, 2000. (Pubitemid 30230457)
8. Jenster, G. The role of the androgen receptor in the development and progression of prostate cancer. Semin. Oncol., 26: 407-421, 1999. (Pubitemid 29411449)
9. Brinkmann, A. O., Blok, L. J., de Ruiter, P. E., Doesburg, P., Steketee, K., Berrevoets, C. A., and Trapman, J. Mechanisms of androgen receptor activation and function. J. Steroid Biochem. Mol. Biol., 69: 307-313, 1999. (Pubitemid 29305551)
10. Marivoet, S., Van Dijck, P., Verhoeven, G., and Heyns, W. Interaction of the 90-kDa heat shock protein with native and in vitro translated androgen receptor and receptor fragments. Mol. Cell. Endocrinol., 88: 165-174, 1992.
11. Russell, D. W., and Wilson, J. D. Steroid 5 α-reductase: two genes/two enzymes. Annu. Rev. Biochem., 63: 25-61, 1994.
12. Jenster, G., Trapman, J., and Brinkmann, A. O. Nuclear import of the human androgen receptor. Biochem. J., 293: 761-768, 1993. (Pubitemid 23244561)
13. Zhou, Z. X., Sar, M., Simental, J. A., Lane, M. V., and Wilson, E. M. A ligand-dependent bipartite nuclear targeting signal in the human androgen receptor. Requirement for the DNA-binding domain and modulation by NH2-terminal and carboxyl-terminal sequences. J. Biol. Chem., 269: 13115-13123, 1994.
14. Cleutjens, K. B., van Eekelen, C. C., van der Korput, H. A., Brinkmann, A. O., and Trapman, J. Two androgen response regions cooperate in steroid hormone regulated activity of the prostate-specific antigen promoter. J. Biol. Chem., 271: 6379-6388, 1996. (Pubitemid 26095448)
15. Cleutjens, K. B., van der Korput, H. A., van Eekelen, C. C., van Rooij, H. C., Faber, P. W., and Trapman, J. An androgen response element in a far upstream enhancer region is essential for high, androgen-regulated activity of the prostate-specific antigen promoter. Mol. Endocrinol., 11: 148-161, 1997. (Pubitemid 27057428)
16. Stephan, C., Jung, K., Diamandis, E. P., Rittenhouse, H. G., Lein, M., and Loening, S. A. Prostate-specific antigen, its molecular forms, and other kallikrein markers for detection of prostate cancer. Urology, 59: 2-8, 2002. (Pubitemid 34059296)
17. Montgomery, J. S., Price, D. K., and Figg, W. D. The androgen receptor gene and its influence on the development and progression of prostate cancer. J. Pathol., 195: 138-146, 2001. (Pubitemid 32899021)
18. Reid, P., Kantoff, P., and Oh, W. Antiandrogens in prostate cancer. Investig. New Drugs, 17: 271-284, 1999. (Pubitemid 30037959)
19. Petrylak, D. P. Chemotherapy for advanced hormone refractory prostate cancer. Urology, 54: 30-35, 1999.
20. Visakorpi, T., Hyytinen, E., Koivisto, P., Tanner, M., Keinanen, R., Palmberg, C., Palotie, A., Tammela, T., Isola, J., and Kallioniemi, O. P. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat. Genet., 9: 401-406, 1995.
21. Zegarra-Moro, O. L., Schmidt, L. J., Huang, H., and Tindall, D. J. Disruption of androgen receptor function inhibits proliferation of androgen-refractory prostate cancer cells. Cancer Res., 62: 1008-1013, 2002. (Pubitemid 34160279)
22. Koivisto, P., Kononen, J., Palmberg, C., Tammela, T., Hyytinen, E., Isola, J., Trapman, J., Cleutjens, K., Noordzij, A., Visakorpi, T., and Kallioniemi, O. P. Androgen receptor gene amplification: a possible molecular mechanism for androgen deprivation therapy failure in prostate cancer. Cancer Res., 57: 314-319, 1997. (Pubitemid 27036612)
23. Culig, Z., Hobisch, A., Cronauer, M. V., Cato, A. C., Hittmair, A., Radmayr, C., Eberle, J., Bartsch, G., and Klocker, H. Mutant androgen receptor detected in an advanced-stage prostatic carcinoma is activated by adrenal androgens and progesterone. Mol. Endocrinol., 7: 1541-1550, 1993. (Pubitemid 24034236)
24. Suzuki, H., Sato, N., Watabe, Y., Masai, M., Seino, S., and Shimazaki, J. Androgen receptor gene mutations in human prostate cancer. J. Steroid Biochem. Mol. Biol., 46: 759-765, 1993. (Pubitemid 24045142)
25. Taplin, M. E., Bubley, G. J., Ko, Y. J., Small, E. J., Upton, M., Rajeshkumar, B., and Balk, S. P. Selection for androgen receptor mutations in prostate cancers treated with androgen antagonist. Cancer Res., 59: 2511-2515, 1999. (Pubitemid 29269089)
26. Taplin, M. E., Bubley, G. J., Shuster, T. D., Frantz, M. E., Spooner, A. E., Ogata, G. K., Keer, H. N., and Balk, S. P. Mutation of the androgen-receptor gene in metastatic androgen-independent prostate cancer. N. Engl. J. Med., 332: 1393-1398, 1995.
27. Shi, X. B., Ma, A. H., Xia, L., Kung, H. J., and de Vere White, R. W. Functional analysis of 44 mutant androgen receptors from human prostate cancer. Cancer Res., 62: 1496-1502, 2002. (Pubitemid 34407813)
28. Zhao, X. Y., Malloy, P. J., Krishnan, A. V., Swami, S., Navone, N. M., Peehl, D. M., and Feldman, D. Glucocorticoids can promote androgen-independent growth of prostate cancer cells through a mutated androgen receptor. Nat. Med., 6: 703-706, 2000. (Pubitemid 30398797)
29. Schafer, T. E., Lapp, C. A., Hanes, C. M., Lewis, J. B., Wataha, J. C., and Schuster, G. S. Estrogenicity of bisphenol A and bisphenol A dimethacrylate in vitro. J. Biomed. Mater. Res., 45: 192-197, 1999. (Pubitemid 29165933)
30. Krishnan, A. V., Stathis, P., Permuth, S. F., Tokes, L., and Feldman, D. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology, 132: 2279-2286, 1993. (Pubitemid 23156872)
31. Sonnenschein, C., and Soto, A. M. An updated review of environmental estrogen and androgen mimics and antagonists. J. Steroid Biochem. Mol. Biol., 65: 143-150, 1998. (Pubitemid 28335600)
32. Diel, P., Schulz, T., Smolnikar, K., Strunck, E., Vollmer, G., and Michna, H. Ability of xeno- and phytoestrogens to modulate expression of estrogen-sensitive genes in rat uterus: estrogenicity profiles and uterotropic activity. J. Steroid Biochem. Mol. Biol., 73: 1-10, 2000. (Pubitemid 30261468)
33. Laws, S. C., Carey, S. A., Ferrell, J. M., Bodman, G. J., and Cooper, R. L. Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol. Sci., 54: 154-167, 2000. (Pubitemid 30152466)
34. Markey, C. M., Michaelson, C. L., Veson, E. C., Sonnenschein, C., and Soto, A. M. The mouse uterotrophic assay: a reevaluation of its validity in assessing the estrogenicity of bisphenol A. Environ. Health Perspect., 109: 55-60, 2001. (Pubitemid 32118026)
35. Howdeshell, K. L., Hotchkiss, A. K., Thayer, K. A., Vandenbergh, J. G., and vom Saal, F. S. Exposure to bisphenol A advances puberty. Nature (Lond.), 401: 763-764, 1999. (Pubitemid 129515829)
36. Papaconstantinou, A. D., Umbreit, T. H., Fisher, B. R., Goering, P. L., Lappas, N. T., and Brown, K. M. Bisphenol A-induced increase in uterine weight and alterations in uterine morphology in ovariectomized B6C3F1 mice: role of the estrogen receptor. Toxicol. Sci., 56: 332-339, 2000. (Pubitemid 30497502)
37. Brotons, J. A., Olea-Serrano, M. F., Villalobos, M., Pedraza, V., and Olea, N. Xenoestrogens released from lacquer coatings in food cans. Environ. Health Perspect., 103: 608-612, 1995.
38. Olea, N., Pulgar, R., Perez, P., Olea-Serrano, F., Rivas, A., Novillo-Fertrell, A., Pedraza, V., Soto, A. M., and Sonnenschein, C. Estrogenicity of resin-based composites and sealants used in dentistry. Environ. Health Perspect., 104: 298-305, 1996. (Pubitemid 26123084)
39. Ramos, J. G., Varayoud, J., Sonnenschein, C., Soto, A. M., Muno Zde Toro, M., and Luque, E. H. Prenatal exposure to low doses of bisphenol A alters the periductal stroma and glandular cell function in the rat ventral prostate. Biol. Reprod., 65: 1271-1277, 2001. (Pubitemid 32927597)
40. Gupta, C. Reproductive malformation of the male offspring following maternal exposure to estrogenic chemicals. Proc. Soc. Exp. Biol. Med., 224: 61-68, 2000. (Pubitemid 30314397)
41. Knudsen, E. S., Pazzagli, C., Born, T. L., Bertolaet, B. L., Knudsen, K. E., Arden, K. C., Henry, R. R., and Feramisco, J. R. Elevated cyclins and cyclin-dependent kinase activity in the rhabdomyosarcoma cell line RD. Cancer Res., 58: 2042-2049, 1998. (Pubitemid 28217485)
42. Knudsen, K. E., Arden, K. C., and Cavenee, W. K. Multiple G1 regulatory elements control the androgen-dependent proliferation of prostatic carcinoma cells. J. Biol. Chem., 273: 20213-20222, 1998. (Pubitemid 28377582)
43. Schreiber, E., Matthias, P., Muller, M. M., and Schaffner, W. Rapid detection of octamer binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res., 17: 6419, 1989. (Pubitemid 19198635)
44. Zhang, J., Zhang, S., Murtha, P. E., Zhu, W., Hou, S. S., and Young, C. Y. Identification of two novel cis-elements in the promoter of the prostate-specific antigen gene that are required to enhance androgen receptor-mediated transactivation. Nucleic Acids Res., 25: 3143-3150, 1997. (Pubitemid 27331411)
45. Sadar, M. D., and Gleave, M. E. Ligand-independent activation of the androgen receptor by the differentiation agent butyrate in human prostate cancer cells. Cancer Res., 60: 5825-5831, 2000.
46. Chen, C., and Okayama, H. High efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol., 7: 2745-2752, 1987.
47. Knudsen, K. E., Booth, D., Naderi, S., Sever-Chroneos, Z., Fribourg, A. F., Hunton, I. C., Feramisco, J. R., Wang, J. Y., and Knudsen, E. S. RB-dependent S-phase response to DNA damage. Mol. Cell. Biol., 20: 7751-7763, 2000.
48. Horoszewicz, J. S., Leong, S. S., Chu, T. M., Wajsman, Z. L., Friedman, M., Papsidero, L., Kim, U., Chai, L. S., Kakati, S., Arya, S. K., and Sandberg, A. A. The LNCaP cell line - a new model for studies on human prostatic carcinoma. Prog. Clin. Biol. Res., 37: 115-132, 1980.
49. Horoszewicz, J. S., Leong, S. S., Kawinski, E., Karr, J. P., Rosenthal, H., Chu, T. M., Mirand, E. A., and Murphy, G. P. LNCaP model of human prostatic carcinoma. Cancer Res., 43: 1809-1818, 1983. (Pubitemid 13122588)
50. Sonnenschein, C., Olea, N., Pasanen, M. E., and Soto, A. M. Negative controls of cell proliferation: human prostate cancer cells and androgens. Cancer Res., 49: 3474-3481, 1989. (Pubitemid 19178161)
51. Kim, I. Y., Kim, J. H., Zelner, D. J., Ahn, H. J., Sensibar, J. A., and Lee, C. Transforming growth factor-β1 is a mediator of androgen-regulated growth arrest in an androgen-responsive prostatic cancer cell line. LNCaP. Endocrinology, 137: 991-999, 1996.
52. Fribourg, A. F., Knudsen, K. E., Strobeck, M. W., Lindhorst, C. M., and Knudsen, E. S. Differential requirements for ras and the retinoblastoma tumor suppressor protein in the androgen dependence of prostatic adenocarcinoma cells. Cell Growth Differ., 11: 361-372, 2000. (Pubitemid 30619564)
53. Sherr, C. J. Cancer cell cycles. Science (Wash. DC), 274: 1672-1677, 1996.
54. Knudsen, K. E., Fribourg, A. F., Strobeck, M. W., Blanchard, J. M., and Knudsen, E. S. Cyclin A is a functional target of retinoblastoma tumor suppressor protein-mediated cell cycle arrest. J. Biol. Chem., 274: 27632-27641, 1999.
55. Philips, A., Huet, X., Plet, A., Le Cam, L., Vie, A., and Blanchard, J. M. The retinoblastoma protein is essential for cyclin A repression in quiescent cells. Oncogene, 16: 1373-1381, 1998. (Pubitemid 28151844)
56. Kipreos, E. T., and Wang, J. Y. Cell cycle-regulated binding of c-Abl tyrosine kinase to DNA. Science (Wash. DC), 256: 382-385, 1992.
57. Sever-Chroneos, Z., Angus, S. P., Fribourg, A. F., Wan, H., Todorov, I., Knudsen, K. E., and Knudsen, E. S. Retinoblastoma tumor suppressor protein signals through inhibition of cyclin-dependent kinase 2 activity to disrupt PCNA function in S phase. Mol. Cell. Biol., 21: 4032-4045, 2001. (Pubitemid 32476464)
58. Zippelius, A., Lutterbuse, R., Riethmuller, G., and Pantel, K. Analytical variables of reverse transcription-polymerase chain reaction-based detection of disseminated prostate cancer cells. Clin. Cancer Res., 6: 2741-2750, 2000. (Pubitemid 30482113)
59. Kuil, C. W., and Mulder, E. Mechanism of antiandrogen action: conformational changes of the receptor. Mol. Cell. Endocrinol., 102: R1-R5, 1994. (Pubitemid 24177469)
60. Avila, D. M., Zoppi, S., and McPhaul, M. J. The androgen receptor (AR) in syndromes of androgen insensitivity and in prostate cancer. J. Steroid Biochem. Mol. Biol., 76: 135-142, 2001. (Pubitemid 32510675)
61. Kuiper, G. G., Lemmen, J. G., Carlsson, B., Corton, J. C., Safe, S. H., van der Saag, P. T., van der Burg, B., and Gustafsson, J. A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology, 139: 4252-4263, 1998. (Pubitemid 28513713)
62. Migliaccio, A., Castoria, G., Di Domenico, M., de Falco, A., Bilancio, A., Lombardi, M., Barone, M. V., Ametrano, D., Zannini, M. S., Abbondanza, C., and Auricchio, F. Steroid-induced androgen receptor-oestradiol receptor β-Src complex triggers prostate cancer cell proliferation. EMBO J., 19: 5406-5417, 2000.
63. Ashby, J., Tinwell, H., and Haseman, J. Lack of effects for low dose levels of bisphenol A and diethylstilbestrol on the prostate gland of CF1 mice exposed in utero. Regul. Toxicol. Pharmacol., 30: 156-166, 1999.
64. Cagen, S. Z., Waechter, J. M., Jr., Dimond, S. S., Breslin, W. J., Butala, J. H., Jekat, F. W., Joiner, R. L., Shiotsuka, R. N., Veenstra, G. E., and Harris, L. R. Normal reproductive organ development in CF-1 mice following prenatal exposure to bisphenol A. Toxicol. Sci., 50: 36-44, 1999. (Pubitemid 29344509)
65. Welshons, W. V., Nagel, S. C., Thayer, K. A., Judy, B. M., and Vom Saal, F. S. Low-dose bioactivity of xenoestrogens in animals: fetal exposure to low doses of methoxychlor and other xenoestrogens increases adult prostate size in mice. Toxicol. Ind. Health, 15: 12-25, 1999. (Pubitemid 30484114)
66. Sheehan, D. M. Activity of environmentally relevant low doses of endocrine disruptors and the bisphenol A controversy: initial results confirmed. Proc. Soc. Exp. Biol. Med., 224: 57-60, 2000. (Pubitemid 30314396)
67. Takeuchi, T., and Tsutsumi, O. Serum bisphenol a concentrations showed gender differences, possibly linked to androgen levels. Biochem. Biophys. Res. Commun., 291: 76-78, 2002. (Pubitemid 34681140)
68. Inoue, K., Kato, K., Yoshimura, Y., Makino, T., and Nakazawa, H. Determination of bisphenol A in human serum by high-performance liquid chromatography with multi-electrode electrochemical detection. J. Chromatogr. B Biomed. Sci. Appl., 749: 17-23, 2000.