The role of estrogen receptor βin prostate cancer

Molecular Medicine

Volumn 20, Issue JULY-DECEMBER 2014, 2014, Pages 427-434

  Christoforou, Paraskevi ^a   Christopoulos, Panagiotis F ^a   Koutsilieris, Michael ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ESTROGEN RECEPTOR AGONIST; ESTROGEN RECEPTOR BETA; PHYTOESTROGEN; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CARCINOGENESIS; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; NONHUMAN; ORGANOGENESIS; OXIDATIVE STRESS; PROSTATE; PROSTATE CANCER; PROSTATE CARCINOGENESIS; PROSTATE DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STEROIDOGENESIS; SWITCHING ROLE THEORY; TREATMENT INDICATION; ANIMAL; DISEASE COURSE; MALE; METABOLISM; PROSTATE TUMOR;

ANIMALS; DISEASE PROGRESSION; ESTROGEN RECEPTOR BETA; HUMANS; MALE; PROSTATE; PROSTATIC NEOPLASMS;

EID: 84921922507     PISSN: 10761551     EISSN: 15283658     Source Type: Journal    
DOI: 10.2119/molmed.2014.00105     Document Type: Article

References (83)

1. Huggins C, Stevens RE Jr, Hodges CV. (1941) Studies on prostatic cancer: Ii. the effects of castration on advanced carcinoma of the prostate gland. Arch. Surg. 43:209–23.
2. Koutsilieris M, Tolis G. (1985) Long-term followup of patients with advanced prostatic carcinoma treated with either buserelin (HOE 766) or orchiectomy: classification of variables associated with disease outcome. Prostate. 7:31–9.
3. Klotz L, McNeill I, Fleshner N. (1999) A phase 1–2 trial of diethylstilbestrol plus low dose warfarin in advanced prostate carcinoma. J. Urol. 161:169–72.
4. Jensen EV. (1960) Fate of steroid estrogens in target tissues. In: Biological Activities of Steroids in Relation to Cancer. Vollmer P.E (ed.) Academic Press, New York, pp. 61–174.
5. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. U. S. A. 93:5925–30.
6. Hartman J, Ström A, Gustafsson JA. (2012) Current concepts and significance of estrogen receptor ® in prostate cancer. Steroids. 77:1262–6.
7. Enmark E, et al. (1997) Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J. Clin. Endocrinol. Metab. 82:4258–65.
8. Fixemer T, Remberger K, Bonkhoff H. (2003) Differential expression of the estrogen receptor beta (ERbeta) in human prostate tissue, premalignant changes, and in primary, metastatic, and recurrent prostatic adenocarcinoma. Prostate. 54:79–87.
9. Royuela M, et al. (2001) Estrogen receptors alpha and beta in the normal, hyperplastic and carcinomatous human prostate. J. Endocrinol. 168:447–54.
10. Heldring N, et al. (2007) Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87:905–31.
11. Powell E, et al. (2012) Identification of estrogen receptor dimer selective ligands reveals growthinhibitory effects on cells that co-express ER〈 and ER®. PLoS ONE. 7:e30993.
12. Chakraborty S, Willett H, Biswas PK. (2012) Insight into estrogen receptor beta–beta and alpha–beta homo- and heterodimerization: A combined molecular dynamics and sequence analysis study. Biophys. Chem. 170:42–50.
13. Walton TJ, et al. (2009) Quantitative RT-PCR analysis of estrogen receptor gene expression in laser microdissected prostate cancer tissue. Prostate. 69:810–9.
14. Hurtado A, et al. (2008) Estrogen receptor beta displays cell cycle-dependent expression and regulates the G1 phase through a non-genomic mechanism in prostate carcinoma cells. Cell. Oncol. 30:349–65.
15. Leav I, et al. (2001) 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. 159:79–92.
16. Leung YK, Mak P, Hassan S, Ho SM. (2006) Estrogen receptor (ER)-beta isoforms: a key to un- derstanding ER-beta signaling. Proc. Natl. Acad. Sci. U.S.A. 103:13162–7.
17. Leung YK, et al. (2010) Estrogen receptor beta2 and beta5 are associated with poor prognosis in prostate cancer, and promote cancer cell migration and invasion. Endocr. Relat. Cancer. 17:675–89.
18. Moore JT, et al. (1998) Cloning and characterization of human estrogen receptor beta isoforms. Biochem. Biophys. Res. Commun. 247:75–8.
19. Younes M, Honma N. (2011) Estrogen receptor ®. Arch. Pathol. Lab. Med. 135:63–6.
20. Peng B, Lu B, Leygue E, Murphy LC. (2003) Putative functional characteristics of human estrogen receptor-beta isoforms. J. Mol. Endocrinol. 30:13–29.
21. Celhay O, et al. (2010) Expression of estrogen related proteins in hormone refractory prostate cancer: association with tumor progression. J. Urol. 184:2172–8.
22. Ghosh D, Griswold J, Erman M, Pangborn W. (2009) Structural basis for androgen specificity and oestrogen synthesis in human aromatase. Nature. 457:219–23.
23. Ellem SJ, Risbridger GP. (2010) Aromatase and regulating the estrogen:androgen ratio in the prostate gland. J. Steroid Biochem. Mol. Biol. 118:246–51.
24. Muthusamy S, et al. (2011) Estrogen receptor ® and 17?® -hydroxysteroid dehydrogenase type 6, a growth regulatory pathway that is lost in prostate cancer. Proc. Natl. Acad. Sci. U.S.A. 108:20090–4.
25. Sugiyama N, Barros RP, Warner M, Gustafsson JA. (2010) ERbeta: recent understanding of estrogen signaling. Trends Endocrinol. Metab. 21:545–52.
26. Berani č N, Stefane B, Brus B, Gobec S, Rižner TL. (2013) New enzymatic assay for the AKR1C enzymes. Chem. Biol. Interact. 202:204–9.
27. Baker ME. (2013) What are the physiological estrogens? Steroids. 78:337–40.
28. Weihua Z. et al. (2001) A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc. Natl. Acad. Sci. U.S.A. 98:6330–5.
29. Grubisha MJ. (2013) Local endocrine, paracrine and redox signaling networks impact estrogen and androgen crosstalk in the prostate cancer microenvironment. Steroids. 78:538–41.
30. Dondi D, et al. (2010) Estrogen receptor beta and the progression of prostate cancer: role of 5alphaandrostane- 3beta,17beta-diol. Endocr. Relat. Cancer. 17:731–42.
31. Dey P, Ström A, Gustafsson JA. (2013) Estrogen receptor ® upregulates FOXO3a and causes induction of apoptosis through PUMA in prostate cancer. Oncogene. 2013, Sept. 30. [Epub ahead of print].
32. Marker PC, Donjacour AA, Dahiya R, Cunha GR. (2003) Hormonal, cellular, and molecular control of prostatic development. Dev. Biol. 253:165–74.
33. Omoto Y, Imamov O, Warner M, Gustafsson JA. (2005) Estrogen receptor alpha and imprinting of the neonatal mouse ventral prostate by estrogen. Proc. Natl. Acad. Sci. U.S.A. 102:1484–9.
34. Prins GS, Huang L, Birch L, Pu Y. (2006) The role of estrogens in normal and abnormal development of the prostate gland. Ann. N. Y. Acad. Sci. 1089:1–13.
35. Shapiro E, et al. (2005) Immunolocalization of estrogen receptor alpha and beta in human fetal prostate. J. Urol. 174:2051–3.
36. Adams JY, Leav I, Lau KM, Ho SM, Pflueger SM. (2002) Expression of estrogen receptor beta in the fetal, neonatal, and prepubertal human prostate. Prostate. 52:69–81
37. Imamov O, et al. (2004) Estrogen receptor beta regulates epithelial cellular differentiation in the mouse ventral prostate. Proc. Natl. Acad. Sci. U.S.A. 101:9375–80.
38. Mak P, et al. (2010) ERbeta impedes prostate cancer EMT by destabilizing HIF-1alpha and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell. 17:319–32.
39. Mak P, Chang C, Pursell B, Mercurio AM. (2013) Estrogen receptor ® sustains epithelial differentiation by regulating prolyl hydroxylase 2 transcription. Proc. Natl. Acad. Sci. U.S.A. 110:4708–13.
40. McPherson SJ, et al. (2007) Essential role for estrogen receptor beta in stromal-epithelial regulation of prostatic hyperplasia. Endocrinology. 148:566–74.
41. Ricke WA, et al. (2008) Prostatic hormonal carcinogenesis is mediated by in situ estrogen production and estrogen receptor alpha signaling. FASEB J. 22:1512–20.
42. Gabal SM, Habib FM, Helmy DO, Ibrahim MF. (2007) Expression of estrogen receptor-B (ER-B) in benign and malignant prostatic epithelial cells and its correlation with the clinico-pathological features. J. Egypt Natl. Canc. Inst. 19:239–48.
43. Gallardo F, et al. (2007) Expression of androgen, oestrogen alpha and beta, and progesterone receptors in the canine prostate: differences between normal, inflamed, hyperplastic and neoplastic glands. J. Comp. Pathol. 136:1–8.
44. Bardin A, Boulle N, Lazennec G, Vignon F, Pujol P. (2004) Loss of ERbeta expression as a common step in estrogen-dependent tumor progression. Endocr. Relat. Cancer. 11:537–51.
45. Li LC, Yeh CC, Nojima D, Dahiya R. (2000) Cloning and characterization of human estrogen receptor beta promoter. Biochem. Biophys. Res. Commun. 275:682–9.
46. Zhang X, Leung YK, Ho SM. (2007) AP-2 regulates the transcription of estrogen receptor (ER)-beta by acting through a methylation hotspot of the 0N promoter in prostate cancer cells. Oncogene. 26:7346–54
47. Cotrim CZ, Fabris V, Doria ML, Lindberg K, Gustafsson J. (2013) Estrogen receptor beta growthinhibitory effects are repressed through activation of MAPK and PI3K signalling in mammary epithelial and breast cancer cells. Oncogene. 32:2390–402.
48. Lee MT, Ouyang B, Ho SM, Leung YK. (2013) Differential expression of estrogen receptor beta isoforms in prostate cancer through interplay between transcriptional and translational regulation. Mol. Cell. Endocrinol. 376:125–35.
49. Gupta-Elera G, Garrett AR, Robison RA, O’Neill KL. (2012) The role of oxidative stress in prostate cancer. Eur. J. Cancer Prev. 21:155–62.
50. Kumar B, Koul S, Khandrika L, Meacham RB, Koul HK. (2008) Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res. 68:1777–85.
51. Thapa D, Ghosh R. (2012) Antioxidants for prostate cancer chemoprevention: challenges and opportunities. Biochem. Pharmacol. 83:1319–30.
52. Miró AM, et al. (2011b) 17®-estradiol regulates oxidative stress in prostate cancer cell lines according to ERalpha/ERbeta ratio. J. Steroid Biochem. Mol. Biol. 123:133–9.
53. Rebillard A, Lefeuvre-Orfila L, Gueritat J, Cillard J. (2013) Prostate cancer and physical activity: adaptive response to oxidative stress. Free Radic. Biol. Med. 60:115–24.
54. Grubisha MJ, Cifuentes ME, Hammes SR, Defranco DB. (2012) A local paracrine and endocrine network involving TGF®, Cox-2, ROS, and estrogen receptor ® influences reactive stromal cell regulation of prostate cancer cell motility. Mol. Endocrinol. 26:940–54.
55. Whittal RM, et al. (2000) Preferential oxidation of zinc finger 2 in estrogen receptor DNA-binding domain prevents dimerization and, hence, DNA binding. Biochemistry. 39:8406–17.
56. Zellweger T, et al. (2013) Estrogen receptor ® expression and androgen receptor phosphorylation correlate with a poor clinical outcome in hormone-naive prostate cancer and are elevated in castration- resistant disease. Endocr. Relat. Cancer. 20:403–13.
57. Savoy RM, Ghosh PM. (2013) The changing roles of steroid nuclear receptors with prostate cancer progression. Endocr. Relat. Cancer. 20:C9–11.
58. Dey P, et al. (2012) Estrogen receptors ®1 and ®2 have opposing roles in regulating proliferation and bone metastasis genes in the prostate cancer cell line PC3. Mol. Endocrinol. 26:1991–2003.
59. Alonso-Magdalena P, et al. (2009) A role for epithelial- mesenchymal transition in the etiology of benign prostatic hyperplasia. PNAS. 106:2859–63.
60. Nagasaki S, et al. (2012) Immunohistochemical analysis of gastrin-releasing peptide receptor (GRPR) and possible regulation by estrogen receptor ®cx in human prostate carcinoma. Neoplasma. 59:224–32.
61. Huber MA, Kraut N, Beug H. (2005) Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17:548–58.
62. Cavallaro U, Christofori G. (2004) Multitasking in tumor progression: signaling functions of cell adhesion molecules. Ann. N. Y. Acad. Sci. 1014:58–66.
63. Pez F, et al. (2011) The HIF-1–inducible lysyl oxidase activates HIF-1 via the Akt pathway in a positive regulation loop and synergizes with HIF-1 in promoting tumor cell growth. Cancer Res. 71:1647–57.
64. Yang MH, et al. (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 10:295–305.
65. Walton TJ, et al. (2008) DNA demethylation and histone deacetylation inhibition co-operate to re- express estrogen receptor beta and induce apoptosis in prostate cancer cell-lines. Prostate. 68:210–22.
66. Cheng J, Lee EJ, Madison LD, Lazennec G. (2004) Expression of estrogen receptor beta in prostate carcinoma cells inhibits invasion and proliferation and triggers apoptosis. FEBS Lett. 566:169–72.
67. Nakamura Y, et al. (2013) Cyclin D1 (CCND1) expression is involved in estrogen receptor beta (ER®) in human prostate cancer. Prostate. 73:590–5.
68. Lai JS, et al. (2004) Metastases of prostate cancer express estrogen receptor-beta. Urology. 64:814–20.
69. Hofland J, et al. (2010) Evidence of limited contributions for intratumoral steroidogenesis in prostate cancer. Cancer Res. 70:1256–64.
70. Gross M, et al. (2009) Expression of androgen and estrogen related proteins in normal weight and obese prostate cancer patients. Prostate. 69:520–7.
71. Meyers MJ, et al. (2001) Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 44:4230–51.
72. McPherson SJ, et al. (2010) Estrogen receptor-beta activated apoptosis in benign hyperplasia and cancer of the prostate is androgen independent and TNFalpha mediated. Proc. Natl. Acad. Sci. U.S.A. 107:3123–8.
73. Lau KM, LaSpina M, Long J, Ho SM. (2000) Expression of estrogen receptor (ER)-alpha and ERbeta in normal and malignant prostatic epithelial cells: regulation by methylation and involvement in growth regulation. Cancer Res. 60:3175–82.
74. Rossi V, et al. (2011) Raloxifene induces cell death and inhibits proliferation through multiple signaling pathways in prostate cancer cells expressing different levels of estrogen receptor 〈 and ®. J. Cell. Physiol. 226:1334–9.
75. Kim IY, et al. (2002) Raloxifene, a selective estrogen receptor modulator, induces apoptosis in androgen- responsive human prostate cancer cell line LNCaP through an androgen-independent pathway. Cancer Res. 62:3649–53.
76. Nelson AW, Tilley WD, Neal DE, Carroll J. (2014) Estrogen receptor beta in prostate cancer: friend or foe? Endocr. Relat. Cancer. 2014, Jan. 8 [Epub ahead of print].
77. Patisaul HB, Jefferson W. (2010) The pros and cons of phytoestrogens. Front. Neuroendocrinol. 31:400–19.
78. Slusarz A, et al. (2012) Aggressive prostate cancer is prevented in ER〈KO mice and stimulated in ER®KO TRAMP mice. Endocrinology. 153:4160–70.
79. Thelen P, Wuttke W, Seidlová-Wuttke D. (2014) Phytoestrogens selective for the estrogen receptor beta exert anti-androgenic effects in castration resistant prostate cancer. J. Steroid Biochem. Mol. Biol. 139:290–3.
80. Matsumura K, Tanaka T, Kawashima H, Nakatani T. (2008) Involvement of the estrogen receptor beta in genistein-induced expression of p21(waf1/cip1) in PC-3 prostate cancer cells. Anticancer Res. 28:709–14.
81. Atawia, RT, Tadros MG, Khalifa AE, Mosli HA, Abdel-Naim AB. (2013) Role of the phytoestrogenic, pro-apoptotic and anti-oxidative properties of silymarin in inhibiting experimental benign prostatic hyperplasia in rats. Toxicol. Lett. 219:160–9
82. Yan L, Spitznagel EL. (2009) Soy consumption and prostate cancer risk in men: a revisit of a meta-analysis. Am. J. Clin. Nutr. 89:1155–63.
83. Koutsilieris M. (1992) Pathophysiology of uterine leiomyomas. Biochem. Cell. Biol. 70:273–8.