Anterior prostate epithelial AR inactivation modifies estrogen receptor expression and increases estrogen sensitivity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 301, Issue 4, 2011, Pages

  Simanainen, Ulla ^a   McNamara, Keely ^a   Gao, Yan Ru ^a   McPherson, Stephen ^b   Desai, Reena ^a   Jimenez, Mark ^a   Handelsman, David J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

Androgen receptor; Androgen receptor gene targeting; Cre LoxP technology; Estrogen sensitivity; Mouse model; Prostate epithelia

Indexed keywords

ANDROGEN RECEPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CASTRATION; CONTROLLED STUDY; ENZYME INACTIVATION; EPITHELIUM; GENE INACTIVATION; IMMUNOREACTIVITY; KERATINIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE; PROTEIN EXPRESSION; SQUAMOUS CELL METAPLASIA;

ANIMALS; EPITHELIAL CELLS; ESTRADIOL; ESTROGENS; MALE; MICE; MICE, KNOCKOUT; PROSTATE; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN;

EID: 80053242819     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00580.2010     Document Type: Article

References (49)

1. Asano K, Maruyama S, Usui T, Fujimoto N. Regulation of estrogen receptor alpha and beta expression by testosterone in the rat prostate gland. Endocr J 50: 281-287, 2003.
2. Banerjee PP, Banerjee S, Lai JM, Strandberg JD, Zirkin BR, Brown TR. Age-dependent and lobe-specific spontaneous hyperplasia in the brown Norway rat prostate. Biol Reprod 59: 1163-1170, 1998.
3. Benbrahim-Tallaa L, Liu J, Webber MM, Waalkes MP. Estrogen signaling and disruption of androgen metabolism in acquired androgenindependence during cadmium carcinogenesis in human prostate epithelial cells. Prostate 67: 135-145, 2007.
4. Bianco JJ, Handelsman DJ, Pedersen JS, Risbridger GP. Direct response of the murine prostate gland and seminal vesicles to estradiol. Endocrinology 143: 4922-4933, 2002.
5. Bianco JJ, McPherson SJ, Wang H, Prins GS, Risbridger GP. Transient neonatal estrogen exposure to estrogen-deficient mice (aromatase knockout) reduces prostate weight and induces inflammation in late life. Am J Pathol 168: 1869-1878, 2006.
6. Bonkhoff H, Fixemer T, Hunsicker I, Remberger K. Estrogen receptor expression in prostate cancer and premalignant prostatic lesions. Am J Pathol 155: 641-647, 1999.
7. Bosland MC. The role of steroid hormones in prostate carcinogenesis. J Natl Cancer Inst Monogr 39-66, 2000.
8. Cunha GR, Donjacour AA, Cooke PS, Mee S, Bigsby RM, Higgins SJ, Sugimura Y. The endocrinology and developmental biology of the prostate. Endocr Rev 8: 338-362, 1987.
9. Harkonen PL, Makela SI. Role of estrogens in development of prostate cancer. J Steroid Biochem Mol Biol 92: 297-305, 2004.
10. Harwood DT, Handelsman DJ. Development and validation of a sensitive liquid chromatography-tandem mass spectrometry assay to simultaneously measure androgens and estrogens in serum without derivatization. Clin Chim Acta 409: 78-84, 2009.
11. Hayward SW, Baskin LS, Haughney PC, Cunha AR, Foster BA, Dahiya R, Prins GS, Cunha GR. Epithelial development in the rat ventral prostate, anterior prostate and seminal vesicle. Acta Anat (Basel) 155: 81-93, 1996.
12. Henshall SM, Quinn DI, Lee CS, Head DR, Golovsky D, Brenner PC, Delprado W, Stricker PD, Grygiel JJ, Sutherland RL. Altered expression of androgen receptor in the malignant epithelium and adjacent stroma is associated with early relapse in prostate cancer. Cancer Res 61: 423-427, 2001.
13. Ho SM, Leav I, Merk FB, Yu M, Kwan PW, Ziar J. Induction of atypical hyperplasia, apoptosis, and type II estrogen-binding sites in the ventral prostates of Noble rats treated with testosterone and pharmacologic doses of estradiol-17 beta. Lab Invest 73: 356-365, 1995.
14. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 66: 5624-5632, 2006.
15. Jin C, Wang F, Wu X, Yu C, Luo Y, McKeehan WL. Directionally specific paracrine communication mediated by epithelial FGF9 to stromal FGFR3 in two-compartment premalignant prostate tumors. Cancer Res 64: 4555-4562, 2004.
16. Krieg M, Nass R, Tunn S. Effect of aging on endogenous level of 5 alpha-dihydrotestosterone, testosterone, estradiol, and estrone in epithelium and stroma of normal and hyperplastic human prostate. J Clin Endocrinol Metab 77: 375-381, 1993.
17. Krongrad A, Wilson CM, Wilson JD, Allman DR, McPhaul MJ. Androgen increases androgen receptor protein while decreasing receptor mRNA in LNCaP cells. Mol Cell Endocrinol 76: 79-88, 1991.
18. Kruithof-Dekker IG, Tetu B, Janssen PJ, Van der Kwast TH. Elevated estrogen receptor expression in human prostatic stromal cells by androgen ablation therapy. J Urol 156: 1194-1197, 1996.
19. Kyprianou N, Isaacs JT. Activation of programmed cell death in the rat ventral prostate after castration. Endocrinology 122: 552-562, 1988.
20. Leav I, Merk FB, Kwan PWL, Ho SM. Androgen-supported estrogenenhanced epithelial proliferation in the prostates of intact noble rats. Prostate 15: 23-40, 1989.
21. McNamara KM, Harwood DT, Simanainen U, Walters KA, Jimenez M, Handelsman DJ. Measurement of sex steroids in murine blood and reproductive tissues by liquid chromatography-tandem mass spectrometry. J Steroid Biochem Mol Biol 121: 611-618, 2010.
22. McPherson SJ, Ellem SJ, Risbridger GP. Estrogen-regulated development and differentiation of the prostate. Differentiation 76: 660-670, 2008.
23. McPherson SJ, Ellem SJ, Simpson ER, Patchev V, Fritzemeier KH, Risbridger GP. Essential role for estrogen receptor beta in stromalepithelial regulation of prostatic hyperplasia. Endocrinology 148: 566-574, 2007.
24. Noble RL. Prostate carcinoma of the Nb rat in relation to hormones. Int Rev Exp Pathol 23: 113-159, 1982.
25. O'Shaughnessy PJ, Sheffield JW. Effect of temperature and the role of testicular descent on post-natal testicular androgen production in the mouse. J Reprod Fertil 91: 357-364, 1991.
26. Omoto Y. Estrogen receptor-alpha signaling in growth of the ventral prostate: comparison of neonatal growth and postcastration regrowth. Endocrinology 149: 4421-4427, 2008.
27. Omoto Y, Imamov O, Warner M, Gustafsson JÅ. Estrogen receptor alpha and imprinting of the neonatal mouse ventral prostate by estrogen. Proc Natl Acad Sci USA 105: 1484-1489, 2005.
28. Omoto Y, Imamov O, Warner M, Gustafsson JA. Estrogen receptor alpha and imprinting of the neonatal mouse ventral prostate by estrogen. Proc Natl Acad Sci USA 102: 1484-1489, 2005.
29. Pelletier G. Expression of steroidogenic enzymes and sex-steroid receptors in human prostate. Best Pract Res Clin Endocrinol Metab 22: 223-228, 2008.
30. Prins GS. Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression. Endocrinology 130: 3703-3714, 1992.
31. Prins GS, Birch L, Couse JF, Choi I, Katzenellenbogen B, Korach KS. Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor alpha: studies with alphaERKO and betaERKO mice. Cancer Res 61: 6089-6097, 2001.
32. Prins GS, Korach KS. The role of estrogens and estrogen receptors in normal prostate growth and disease. Steroids 73: 233-244, 2008.
33. Prins GS, Tang WY, Belmonte J, Ho SM. Perinatal exposure to oestradiol and bisphenol A alters the prostate epigenome and increases susceptibility to carcinogenesis. Basic Clin Pharmacol 102: 134-138, 2008.
34. Ricke WA, McPherson SJ, Bianco JJ, Cunha GR, Wang Y, Risbridger GP. Prostatic hormonal carcinogenesis is mediated by in situ estrogen production and estrogen receptor alpha signaling. FASEB J 22: 1512-1520, 2008.
35. Risbridger GP, Bianco JJ, Ellem SJ, McPherson SJ. Oestrogens and prostate cancer. Endocr Relat Cancer 10: 187-191, 2003.
36. Risbridger GP, Wang H, Frydenberg M, Cunha G. The metaplastic effects of estrogen on mouse prostate epithelium: proliferation of cells with basal cell phenotype. Endocrinology 142: 2443-2450, 2001.
37. Savolainen S, Pakarainen T, Huhtaniemi I, Poutanen M, Makela S. Delay of postnatal maturation sensitizes the mouse prostate to testosterone-induced pronounced hyperplasia: protective role of estrogen receptorbeta. Am J Pathol 171: 1013-1022, 2007.
38. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, Humphrey PA, Sundberg JP, Rozengurt N, Barrios R, Ward JM, Cardiff RD. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res 64: 2270-2305, 2004.
39. Simanainen U, Allan CM, Lim P, McPherson S, Jimenez M, Zajac JD, Davey RA, Handelsman DJ. Disruption of prostate epithelial androgen receptor impedes prostate lobe-specific growth and function. Endocrinology 148: 2264-2272, 2007.
40. Simanainen U, McNamara K, Gao YR, Handelsman DJ. Androgen sensitivity of prostate epithelium is enhanced by postnatal androgen receptor inactivation. Am J Physiol Endocrinol Metab 296: E1335-E1343, 2009.
41. Singh J, Handelsman DJ. Morphometric studies of neonatal estrogen imprinting in the mature mouse prostate. J Endocrinol 162: 39-48, 1999.
42. Singh J, Zhu Q, Handelsman DJ. Stereological evaluation of mouse prostate development. J Androl 20: 251-258, 1999.
43. Stanbrough M, Leav I, Kwan PW, Bubley GJ, Balk SP. Prostatic intraepithelial neoplasia in mice expressing an androgen receptor transgene in prostate epithelium. Proc Natl Acad Sci USA 98: 10823-10828, 2001.
44. Tsurusaki T, Aoki D, Kanetake H, Inoue S, Muramatsu M, Hishikawa Y, Koji T. Zone-dependent expression of estrogen receptors alpha and beta in human benign prostatic hyperplasia. J Clin Endocrinol Metab 88: 1333-1340, 2003.
45. Waters KM, Safe S, Gaido KW. Differential gene expression in response to methoxychlor and estradiol through ERalpha, ERbeta, and AR in reproductive tissues of female mice. Toxicol Sci 63: 47-56, 2001.
46. Wu CT, Altuwaijri S, Ricke WA, Huang SP, Yeh S, Zhang C, Niu Y, Tsai MY, Chang C. Increased prostate cell proliferation and loss of cell differentiation in mice lacking prostate epithelial androgen receptor. Proc Natl Acad Sci USA 104: 12679-12684, 2007.
47. Yamashita S. Localization of estrogen and androgen receptors in male reproductive tissues of mice and rats. Anat Rec A Discov Mol Cell Evol Biol 279: 768-778, 2004.
48. Yatkin E, Bernoulli J, Talvitie EM, Santti R. Inflammation and epithelial alterations in rat prostate: impact of the androgen to oestrogen ratio. Int J Androl 32: 399-410, 2009.
49. Zhang FP, Poutanen M, Wilbertz J, Huhtaniemi I. Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol Endocrinol 15: 172-183, 2001.