A perspective on the role of estrogen in hormone-induced prostate carcinogenesis

Cancer Letters

Volumn 334, Issue 1, 2013, Pages 28-33

  Bosland, Maarten C ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Androgens; Estrogens; Hormonal carcinogenesis; Prostate cancer

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CARCINOGEN; DNA; ESTROGEN; ESTROGEN RECEPTOR; AR PROTEIN, HUMAN; ESTRADIOL;

ANDROGEN METABOLISM; CARCINOGENESIS; DNA DAMAGE; ESTROGEN ACTIVITY; ESTROGEN METABOLISM; GENOTOXICITY; HORMONAL REGULATION; HUMAN; METABOLITE; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; SHORT SURVEY; ANIMAL; MALE; METABOLISM; PHYSIOLOGY; PROSTATE TUMOR;

ANIMALIA;

ANDROGENS; ANIMALS; CARCINOGENS; ESTRADIOL; ESTROGENS; HUMANS; MALE; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN;

EID: 84891958211     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.08.027     Document Type: Review

References (76)

1. Jemal A., Siegel R., Xu J., Ward E. Cancer statistics, 2010. CA Cancer J. Clin. 2010, 60:277-300.
2. Bosland M.C. The role of steroid hormones in prostate carcinogenesis. J. Natl. Cancer Inst. Monogr. 2000, 39-66.
3. Henderson B.E., Feigelson H.S. Hormonal carcinogenesis. Carcinogenesis 2000, 21:427-433.
4. Tuohimaa P. Control of cell prolifation in male accessory sex glands. Male Accessory Sex Glands 1980, 131-153. Elsevier/North-Holland Biomedical Press, Amsterdam. E. Spring-Mills, E.S.E. Hafez (Eds.).
5. Milman H.A., Bosland M.C., Walden P.D., Heinze J.E. Evaluation of the adequacy of published studies of low-dose effects of bisphenol A on the rodent prostate for use in human risk assessment. Regul. Toxicol. Pharmacol.: RTP 2002, 35:338-346.
6. Morgentaler A., Traish A.M. Shifting the paradigm of testosterone and prostate cancer: the saturation model and the limits of androgen-dependent growth. Eur. Urol. 2009, 55:310-320.
7. Eaton N.E., Reeves G.K., Appleby P.N., Key T.J. Endogenous sex hormones and prostate cancer: a quantitative review of prospective studies. Br. J. Cancer 1999, 80:930-934.
8. Roddam A.W., Allen N.E., Appleby P., Key T.J. Endogenous sex hormones and prostate cancer: a collaborative analysis of 18 prospective studies. J. Natl. Cancer Inst. 2008, 100:170-183.
9. Cunha G.R. Mesenchymal-epithelial interactions: past, present, and future. Differ.; Res. Biolo. Divers. 2008, 76:578-586.
10. Berry P.A., Maitland N.J., Collins A.T. Androgen receptor signalling in prostate: effects of stromal factors on normal and cancer stem cells. Mol. Cell. Endocrinol. 2008, 288:30-37.
11. Setiawan V.W., Schumacher F.R., Haiman C.A., Stram D.O., Albanes D., Altshuler D., Berglund G., Buring J., Calle E.E., Clavel-Chapelon F., Cox D.G., Gaziano J.M., Hankinson S.E., Hayes R.B., Henderson B.E., Hirschhorn J., Hoover R., Hunter D.J., Kaaks R., Kolonel L.N., Kraft P., Ma J., Le Marchand L., Linseisen J., Lund E., Navarro C., Overvad K., Palli D., Peeters P.H., Pike M.C., Riboli E., Stampfer M.J., Thun M.J., Travis R., Trichopoulos D., Yeager M., Ziegler R.G., Spencer Feigelson H., Chanock S.J. CYP17 genetic variation and risk of breast and prostate cancer from the National Cancer Institute Breast and Prostate Cancer Cohort Consortium (BPC3). Cancer Epidemiol. Biomarkers Prev. 2007, 16:2237-2246.
12. Kraft P., Pharoah P., Chanock S.J., Albanes D., Kolonel L.N., Hayes R.B., Altshuler D., Andriole G., Berg C., Boeing H., Burtt N.P., Bueno-de-Mesquita B., Calle E.E., Cann H., Canzian F., Chen Y.C., Crawford D.E., Dunning A.M., Feigelson H.S., Freedman M.L., Gaziano J.M., Giovannucci E., Gonzalez C.A., Haiman C.A., Hallmans G., Henderson B.E., Hirschhorn J.N., Hunter D.J., Kaaks R., Key T., Le Marchand L., Ma J., Overvad K., Palli D., Pike M.C., Riboli E., Rodriguez C., Setiawan W.V., Stampfer M.J., Stram D.O., Thomas G., Thun M.J., Travis R., Trichopoulou A., Virtamo J., Wacholder S. Genetic variation in the HSD17B1 gene and risk of prostate cancer. PLoS Genet. 2005, 1:e68.
13. Pearce C.L., Makridakis N.M., Ross R.K., Pike M.C., Kolonel L.N., Henderson B.E., Reichardt J.K. Steroid 5-alpha reductase type II V89L substitution is not associated with risk of prostate cancer in a multiethnic population study. Cancer Epidemiol. Biomarkers Prev. 2002, 11:417-418.
14. Pearce C.L., Van Den Berg D.J., Makridakis N., Reichardt J.K., Ross R.K., Pike M.C., Kolonel L.N., Henderson B.E. No association between the SRD5A2 gene A49T missense variant and prostate cancer risk: lessons learned. Hum. Mol. Genet. 2008, 17:2456-2461.
15. Chu L.W., Reichardt J.K., Hsing A.W. Androgens and the molecular epidemiology of prostate cancer. Curr. Opin. Endocrinol. Diabetes Obes. 2008, 15:261-270.
16. Chokkalingam A.P., Stanczyk F.Z., Reichardt J.K., Hsing A.W. Molecular epidemiology of prostate cancer: hormone-related genetic loci. Front Biosci. 2007, 12:3436-3460.
17. Li J., Coates R.J., Gwinn M., Khoury M.J. Steroid 5-{alpha}-reductase Type 2 (SRD5a2) gene polymorphisms and risk of prostate cancer: a HuGE review. Am. J. Epidemiol. 2010, 171:1-13.
18. Keshava C., McCanlies E.C., Weston A. CYP3A4 polymorphisms-potential risk factors for breast and prostate cancer: a HuGE review. Am. J. Epidemiol. 2004, 160:825-841.
19. Schleutker J. Polymorphisms in androgen signaling pathway predisposing to prostate cancer. Mol. Cell Endocrinol. 2011.
20. Goodman P.J., Tangen C.M., Crowley J.J., Carlin S.M., Ryan A., Coltman C.A., Ford L.G., Thompson I.M. Implementation of the prostate cancer prevention trial (PCPT). Control. Clin. Trials 2004, 25:203-222.
21. Andriole G., Bostwick D., Brawley O., Gomella L., Marberger M., Tindall D., Breed S., Somerville M., Rittmaster R. Chemoprevention of prostate cancer in men at high risk: rationale and design of the reduction by dutasteride of prostate cancer events (REDUCE) trial. J. Urol. 2004, 172:1314-1317.
22. Thompson I.M., Goodman P.J., Tangen C.M., Lucia M.S., Miller G.J., Ford L.G., Lieber M.M., Cespedes R.D., Atkins J.N., Lippman S.M., Carlin S.M., Ryan A., Szczepanek C.M., Crowley J.J., Coltman C.A. The influence of finasteride on the development of prostate cancer. New Engl. J. Med. 2003, 349:215-224.
23. Andriole G.L., Bostwick D.G., Brawley O.W., Gomella L.G., Marberger M., Montorsi F., Pettaway C.A., Tammela T.L., Teloken C., Tindall D.J., Somerville M.C., Wilson T.H., Fowler I.L., Rittmaster R.S. Effect of dutasteride on the risk of prostate cancer. New Engl. J. Med. 2010, 362:1192-1202.
24. Sakr W.A., Grignon D.J., Crissman J.D., Heilbrun L.K., Cassin B.J., Pontes J.J., Haas G.P. High grade prostatic intraepithelial neoplasia (HGPIN) and prostatic adenocarcinoma between the ages of 20-69: an autopsy study of 249 cases. In Vivo 1994, 8:439-443.
25. Morgentaler A. Testosterone and prostate cancer: what are the risks for middle-aged men?. Urol. Clin. NA 2011, 38:119-124.
26. Schultheiss D., Machtens S., Jonas U. Testosterone therapy in the ageing male: what about the prostate?. Andrologia 2004, 36:355-365.
27. Fernandez-Balsells M.M., Murad M.H., Lane M., Lampropulos J.F., Albuquerque F., Mullan R.J., Agrwal N., Elamin M.B., Gallegos-Orozco J.F., Wang A.T., Erwin P.J., Bhasin S., Montori V.M. Clinical review 1: adverse effects of testosterone therapy in adult men: a systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 2010, 95:2560-2575.
28. Calof O.M., Singh A.B., Lee M.L., Kenny A.M., Urban R.J., Tenover J.L., Bhasin S. Adverse events associated with testosterone replacement in middle-aged and older men: a meta-analysis of randomized, placebo-controlled trials. J. Gerontol. Series A, Biol. Sci. Med. Sci. 2005, 60:1451-1457.
29. Tentori L., Graziani G. Doping with growth hormone/IGF-1, anabolic steroids or erythropoietin: is there a cancer risk?. Pharmacol. Res.: Official J. Ital. Pharmacol. Soc. 2007, 55:359-369.
30. Noble R.L. The development of prostatic adenocarcinoma in Nb rats following prolonged sex hormone administration. Cancer Res. 1977, 37:1929-1933.
31. Pollard M., Luckert P.H. Autochthonous prostate adenocarcinomas in Lobund-Wistar rats: a model system. Prostate 1987, 11:219-227.
32. Pollard M., Luckert P.H., Schmidt M.A. Induction of prostate adenocarcinomas in Lobund Wistar rats by testosterone. Prostate 1982, 3:563-568.
33. Hoover D.M., Best K.L., McKenney B.K., Tamura R.N., Neubauer B.L. Experimental induction of neoplasia in the accessory sex organs of male Lobund-Wistar rats. Cancer Res. 1990, 50:142-146.
34. Pollard M., Luckert P.H. Prostate cancer in a Sprague-Dawley rat. Prostate 1985, 6:389-393.
35. Pour P.M., Stepan K. Induction of prostatic carcinomas and lower urinary tract neoplasms by combined treatment of intact and castrated rats with testosterone propionate and N-nitrosobis(2-oxopropyl)amine. Cancer Res. 1987, 47:5699-5706.
36. Bosland M.C., Dreef-Van Der Meulen H.C., Sukumar S., Ofner P., Leav I., Han X., Liehr J.G. Multistage prostate carcinogenesis: the role of hormones. Princess Takamatsu Symp. 1991, 22:109-123.
37. McCormick D.L., Rao K.V., Dooley L., Steele V.E., Lubet R.A., Kelloff G.J., Bosland M.C. Influence of N-methyl-N-nitrosourea, testosterone, and N-(4-hydroxyphenyl)-all-trans-retinamide on prostate cancer induction in Wistar-Unilever rats. Cancer Res. 1998, 58:3282-3288.
38. Shirai T., Tamano S., Kato T., Iwasaki S., Takahashi S., Ito N. Induction of invasive carcinomas in the accessory sex organs other than the ventral prostate of rats given 3,2'-dimethyl-4-aminobiphenyl and testosterone propionate. Cancer Res. 1991, 51:1264-1269.
39. Tsukamoto S., Akaza H., Onozawa M., Shirai T., Ideyama Y. A five-alpha reductase inhibitor or an antiandrogen prevents the progression of microscopic prostate carcinoma to macroscopic carcinoma in rats. Cancer 1998, 82:531-537.
40. Ellem S.J., Schmitt J.F., Pedersen J.S., Frydenberg M., Risbridger G.P. Local aromatase expression in human prostate is altered in malignancy. J. Clin. Endocrinol. Metab. 2004, 89:2434-2441.
41. Bosland M.C., Ford H., Horton L. Induction at high incidence of ductal prostate adenocarcinomas in NBL/Cr and Sprague-Dawley Hsd:SD rats treated with a combination of testosterone and estradiol-17 beta or diethylstilbestrol. Carcinogenesis 1995, 16:1311-1317.
42. Ozten N., Horton L., Lasano S., Bosland M.C. Selenomethionine and alpha-tocopherol do not inhibit prostate carcinogenesis in the testosterone plus estradiol-treated NBL rat model. Cancer Prev. Res. (Phila) 2010, 3:371-380.
43. Ricke W.A., Ishii K., Ricke E.A., Simko J., Wang Y., Hayward S.W., Cunha G.R. Steroid hormones stimulate human prostate cancer progression and metastasis. Int. J. Cancer 2006, 118:2123-2131.
44. Hayward S.W., Wang Y., Cao M., Hom Y.K., Zhang B., Grossfeld G.D., Sudilovsky D., Cunha G.R. Malignant transformation in a nontumorigenic human prostatic epithelial cell line. Cancer Res. 2001, 61:8135-8142.
45. Hayward S.W., Dahiya R., Cunha G.R., Bartek J., Deshpande N., Narayan P. Establishment and characterization of an immortalized but non-transformed human prostate epithelial cell line: BPH-1. In Vitro Cell. Dev. Biol. Anim. 1995, 31:14-24.
46. McPherson S.J., Wang H., Jones M.E., Pedersen J., Iismaa T.P., Wreford N., Simpson E.R., Risbridger G.P. Elevated androgens and prolactin in aromatase-deficient mice cause enlargement, but not malignancy, of the prostate gland. Endocrinology 2001, 142:2458-2467.
47. Fowler K.A., Gill K., Kirma N., Dillehay D.L., Tekmal R.R. Overexpression of aromatase leads to development of testicular leydig cell tumors: an in vivo model for hormone-mediated TesticularCancer. Am. J. Pathol. 2000, 156:347-353.
48. Li X., Nokkala E., Yan W., Streng T., Saarinen N., Warri A., Huhtaniemi I., Santti R., Makela S., Poutanen M. Altered structure and function of reproductive organs in transgenic male mice overexpressing human aromatase. Endocrinology 2001, 142:2435-2442.
49. Jarred R.A., McPherson S.J., Bianco J.J., Couse J.F., Korach K.S., Risbridger G.P. Prostate phenotypes in estrogen-modulated transgenic mice. Trends Endocrinol. Metabol.: TEM 2002, 13:163-168.
50. Setlur S.R., Chen C.X., Hossain R.R., Ha J.S., Van Doren V.E., Stenzel B., Steiner E., Oldridge D., Kitabayashi N., Banerjee S., Chen J.Y., Schafer G., Horninger W., Lee C., Rubin M.A., Klocker H., Demichelis F. Genetic variation of genes involved in dihydrotestosterone metabolism and the risk of prostate cancer. Cancer Epidemiol. Biomarkers Prev. 2010, 19:229-239.
51. Yao S., Till C., Kristal A.R., Goodman P.J., Hsing A.W., Tangen C.M., Platz E.A., Stanczyk F.Z., Reichardt J.K., Tang L., Neuhouser M.L., Santella R.M., Figg W.D., Price D.K., Parnes H.L., Lippman S.M., Thompson I.M., Ambrosone C.B., Hoque A. Serum estrogen levels and prostate cancer risk in the prostate cancer prevention trial: a nested case-control study. Cancer Causes Control: CCC 2011, 22:1121-1131.
52. Rohrmann S., Nelson W.G., Rifai N., Brown T.R., Dobs A., Kanarek N., Yager J.D., Platz E.A. Serum estrogen, but not testosterone, levels differ between black and white men in a nationally representative sample of Americans. J. Clin. Endocrinol. Metab. 2007, 92:2519-2525.
53. Travis R.C., Schumacher F., Hirschhorn J.N., Kraft P., Allen N.E., Albanes D., Berglund G., Berndt S.I., Boeing H., Bueno-de-Mesquita H.B., Calle E.E., Chanock S., Dunning A.M., Hayes R., Feigelson H.S., Gaziano J.M., Giovannucci E., Haiman C.A., Henderson B.E., Kaaks R., Kolonel L.N., Ma J., Rodriguez L., Riboli E., Stampfer M., Stram D.O., Thun M.J., Tjonneland A., Trichopoulos D., Vineis P., Virtamo J., Le Marchand L., Hunter D.J. CYP19A1 genetic variation in relation to prostate cancer risk and circulating sex hormone concentrations in men from the Breast and Prostate Cancer Cohort Consortium. Cancer Epidemiol. Biomarkers Prev. 2009, 18:2734-2744.
54. Vermeulen A., Kaufman J.M., Goemaere S., van Pottelberg I. Estradiol in elderly men. The aging male. Official J. Int. Soc. Study Aging Male 2002, 5:98-102.
55. Latil A., Bieche I., Vidaud D., Lidereau R., Berthon P., Cussenot O., Vidaud M. Evaluation of androgen, estrogen (ER alpha and ER beta), and progesterone receptor expression in human prostate cancer by real-time quantitative reverse transcription-polymerase chain reaction assays. Cancer Res. 2001, 61:1919-1926.
56. Lau K.M., Leav I., Ho S.M. Rat estrogen receptor-alpha and -beta, and progesterone receptor mRNA expression in various prostatic lobes and microdissected normal and dysplastic epithelial tissues of the Noble rats. Endocrinology 1998, 139:424-427.
57. Leav I., Lau K.M., Adams J.Y., McNeal J.E., Taplin M.E., Wang J., Singh H., Ho S.M. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am. J. Pathol. 2001, 159:79-92.
58. Thompson C.J., Tam N.N., Joyce J.M., Leav I., Ho S.M. Gene expression profiling of testosterone and estradiol-17 beta-induced prostatic dysplasia in Noble rats and response to the antiestrogen ICI 182,780. Endocrinology 2002, 143:2093-2105.
59. McCormick D.L., Johnson W.D., Lubet R.A., Steele V.E., Bosland M.C. Differential chemopreventive activity of the antiandrogen, flutamide, and the antiestrogen, tamoxifen, in the rat prostate. Proc. Am. Assoc. Cancer Res. 2002, 43:640.
60. Krege J.H., Hodgin J.B., Couse J.F., Enmark E., Warner M., Mahler J.F., Sar M., Korach K.S., Gustafsson J.A., Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc. Natl. Acad. Sci. USA 1998, 95:15677-15682.
61. Weihua Z., Makela S., Andersson L.C., Salmi S., Saji S., Webster J.I., Jensen E.V., Nilsson S., Warner M., Gustafsson J.A. A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc. Natl. Acad. Sci. USA 2001, 98:6330-6335.
62. Couse J.F., Curtis Hewitt S., Korach K.S. Receptor null mice reveal contrasting roles for estrogen receptor alpha and beta in reproductive tissues. J. Steroid Biochem. Mol. Biol. 2000, 74:287-296.
63. Dupont S., Krust A., Gansmuller A., Dierich A., Chambon P., Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000, 127:4277-4291.
64. Horvath L.G., Henshall S.M., Lee C.S., Head D.R., Quinn D.I., Makela S., Delprado W., Golovsky D., Brenner P.C., O'Neill G., Kooner R., Stricker P.D., Grygiel J.J., Gustafsson J.A., Sutherland R.L. Frequent loss of estrogen receptor-beta expression in prostate cancer. Cancer Res. 2001, 61:5331-5335.
65. Chen Y.C., Kraft P., Bretsky P., Ketkar S., Hunter D.J., Albanes D., Altshuler D., Andriole G., Berg C.D., Boeing H., Burtt N., Bueno-de-Mesquita B., Cann H., Canzian F., Chanock S., Dunning A., Feigelson H.S., Freedman M., Gaziano J.M., Giovannucci E., Sanchez M.J., Haiman C.A., Hallmans G., Hayes R.B., Henderson B.E., Hirschhorn J., Kaaks R., Key T.J., Kolonel L.N., LeMarchand L., Ma J., Overvad K., Palli D., Pharaoh P., Pike M., Riboli E., Rodriguez C., Setiawan V.W., Stampfer M., Stram D.O., Thomas G., Thun M.J., Travis R.C., Virtamo J., Trichopoulou A., Wacholder S., Weinstein S.J. Sequence variants of estrogen receptor beta and risk of prostate cancer in the National Cancer Institute Breast and Prostate Cancer Cohort Consortium. Cancer Epidemiol. Biomarkers Prev. 2007, 16:1973-1981.
66. Cavalieri E.L., Devanesan P., Bosland M.C., Badawi A.F., Rogan E.G. Catechol estrogen metabolites and conjugates in different regions of the prostate of Noble rats treated with 4-hydroxyestradiol: implications for estrogen-induced initiation of prostate cancer. Carcinogenesis 2002, 23:329-333.
67. Yang L., Gaikwad N.W., Meza J., Cavalieri E.L., Muti P., Trock B., Rogan E.G. Novel biomarkers for risk of prostate cancer: results from a case-control study. Prostate 2009, 69:41-48.
68. Cavalieri E., Frenkel K., Liehr J.G., Rogan E., Roy D. Estrogens as endogenous genotoxic agents-DNA adducts and mutations. J. Natl. Cancer Inst. Monogr. 2000, 75-93.
69. Mailander P.C., Meza J.L., Higginbotham S., Chakravarti D. Induction of A.T to G.C mutations by erroneous repair of depurinated DNA following estrogen treatment of the mammary gland of ACI rats. J. Steroid Biochem. Mol. Biol. 2006, 101:204-215.
70. Bolton J.L., Thatcher G.R. Potential mechanisms of estrogen quinone carcinogenesis. Chem. Res. Toxicol. 2008, 21:93-101.
71. Liehr J.G. Role of DNA adducts in hormonal carcinogenesis. Regul. Toxicol. Pharmacol.: RTP 2000, 32:276-282.
72. Li K.M., Todorovic R., Devanesan P., Higginbotham S., Kofeler H., Ramanathan R., Gross M.L., Rogan E.G., Cavalieri E.L. Metabolism and DNA binding studies of 4-hydroxyestradiol and estradiol-3,4-quinone in vitro and in female ACI rat mammary gland in vivo. Carcinogenesis 2004, 25:289-297.
73. Saeed M., Rogan E., Fernandez S.V., Sheriff F., Russo J., Cavalieri E. Formation of depurinating N3Adenine and N7Guanine adducts by MCF-10F cells cultured in the presence of 4-hydroxyestradiol. Int. J. Cancer 2007, 120:1821-1824.
74. Zhang F., Swanson S.M., van Breemen R.B., Liu X., Yang Y., Gu C., Bolton J.L. Equine estrogen metabolite 4-hydroxyequilenin induces DNA damage in the rat mammary tissues: formation of single-strand breaks, apurinic sites, stable adducts, and oxidized bases. Chem. Res. Toxicol. 2001, 14:1654-1659.
75. Han X., Liehr J.G., Bosland M.C. Induction of a DNA adduct detectable by 32P-postlabeling in the dorsolateral prostate of NBL/Cr rats treated with estradiol-17 beta and testosterone. Carcinogenesis 1995, 16:951-954.
76. Ho S.M., Roy D. Sex hormone-induced nuclear DNA damage and lipid peroxidation in the dorsolateral prostates of Noble rats. Cancer Lett. 1994, 84:155-162.