Estrogen and prostate cancer: An eclipsed truth in an androgen-dominated scenario

Journal of Cellular Biochemistry

Volumn 102, Issue 4, 2007, Pages 899-911

  Carruba, Giuseppe ^a,b  

^a ARNAS Civico   (Italy)

^b Experimental Oncology   (Italy)

Author keywords

Androgen; Estrogen; Metabolism; Plasma hormones; Prostate cancer; Receptors; Tissue hormones

Indexed keywords

3ALPHA HYDROXYSTEROID DEHYDROGENASE; ANDROGEN; AROMATASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; SEX HORMONE; STEROID 5BETA REDUCTASE; TESTOSTERONE 17BETA DEHYDROGENASE;

CANCER GROWTH; CANCER RISK; CARCINOGENESIS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DIET; ESTROGEN RESPONSIVE ELEMENT; HUMAN; LIFESTYLE; LIGAND BINDING; MALE; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; PROSTATE EPITHELIUM; REVIEW; STEROID METABOLISM;

ANDROGENS; ESTROGENS; HUMANS; MALE; PROSTATIC NEOPLASMS; RECEPTORS, ESTROGEN;

ANIMALIA; RATTUS;

EID: 35648959800     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21529     Document Type: Review

References (88)

1. American Cancer Society. 2007. Cancer facts and figures 2007. Atlanta: American Cancer Society.
2. Bardin A, Boulle N, Lazennec G, Vignon F, Pujol P. 2004. Loss of ERβ expression as a common step in estrogen-dependent tumor progression. Endocr Related Cancer 11:537-551.
3. Barrett-Connor E, Garland C, McPhillips JB, Khaw KT, Wingard DL. 1990. A prospective, population-based study of androstenedione, estrogens, and prostatic cancer. Cancer Res 50:169-173.
4. Bosland MC. 1992. Animal models for the study of prostate carcinogenesis. J Cell Biochem Suppl 16H:89-98.
5. Bosland MC. 2000. The role of steroid hormones in prostate carcinogenesis. J Natl Cancer Inst Monogr 27:39-66.
6. Bosland MC, Ford H, Horton L. 1995. 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-17β or diethylstilbestrol. Carcinogenesis 16:1311-1317.
7. Bradlow HL, Hershcopf RJ, Martucci CP, Fishman J. 1985. Estradiol 16α-hydroxylation in the mouse correlates with mammary tumor incidence and presence of murine mammary tumor virus: A possible model for the hormonal etiology of breast cancer in humans. Proc Natl Acad Sci USA 82:6295-6299.
8. Bradlow H, Telang N, Sepkovic D, Osborne M. 1996. 2-Hydroxyestrone: The "good" estrogen. J Endocrinol 150 (Suppl):S259-S265.
9. Cancel-Tassin G, Cussenot O. 2005. Genetic susceptibility to prostate cancer. Br J Urol Int 96:1380-1385.
10. Carruba G. 2006. Estrogen and mechanisms of prostate cancer progression. Ann NY Acad Sci 1089:201-217.
11. Carruba G, Pfeffer U, Fecarotta E, Coviello D, D'Amato E, Lo Casto M, Vidali G, Castagnetta L. 1994. Estradiol inhibits growth of hormone non responsive PC3 human prostate cancer cells. Cancer Res 54:1190-1193.
12. Carruba G, Adamski J, Calabro M, Miceli MD, Cataliotti A, Bellavia V, Lo Bue A, Polito L, Castagnetta L. 1997. Molecular expression of 17βhydroxysteroid dehydrogenase types in relation to their activity in human prostate cancer cells. Mol Cell Endocrinol 135:51-57.
13. Carruba G, Granata OM, Pala V, Campisi I, Agostara B, Cusimano R, Ravazzolo B, Traina A. 2006. A traditional mediterranean diet decreases endogenous estrogens in healthy postmenopausal women. Nutr Cancer 56:253-259.
14. Castagnetta L, D'Agostino C, Lo Casto M, Traina A, Leake RE. 1981. Breast cancer: A comparison of response to endocrine therapy and oestrogen excretion patterns including unusual metabolites. Br J Cancer 44:670-674.
15. Castagnetta L, Granata OM, Polito L, Blasi L, Cannella S, Carruba G. 1994. Different conversion metabolic rates of testosterone are associated to hormone-sensitive status and -response of human prostate cancer cells. J Steroid Biochem 49:351-357.
16. Castagnetta L, Miceli MD, Sorci C, Pfeffer U, Farruggio R, Oliveri G, Calabro M, Carruba G. 1995. Growth of LNCaP human prostate cancer cells is stimulated by estradiol via its own receptor. Endocrinology 136:2309-2319.
17. Castagnetta L, Granata OM, Bellavia V, Amodio R, Scaccianoce E, Notarbartolo M, Follari MR, Miceli MD, Carruba G. 1997. Product of aromatase activity in intact LNCaP and MCF7 human cancer cells. J Steroid Biochem Mol Biol 61:287-292.
18. Castagnetta L, Granata OM, Traina A, Ravazzolo B, Amoroso M, Miele M, Bellavia V, Agostara B, Carruba G. 2002. Tissue content of hydroxyestrogens in relation to survival of breast cancer patients. Clin Cancer Res 8:3146-3155.
19. Cavalieri E, Stack D, Devanesan P, Todorovic R, Dwivedy I, Higginbotham S, Johansson S, Patil K, Gross M, Gooden J, Ramanathan R, Cerny R, Rogan E. 1997. Molecular origin of cancer: Catechol estrogen-3, 4-quinones as endogenous tumor initiators. Proc Natl Acad Sci USA 94:10937-10942.
20. Chang BL, Zheng SL, Isaacs SD, Turner A, Hawkins GA, Wiley KE, Bleecker ER, Walsh PC, Meyers DA, Isaacs WB, Xu J. 2003. Polymorphisms in the CYP1A1 gene are associated with prostate cancer risk. Int J Cancer 106:375-378.
21. Coffey DS. 2001. Similarities of prostate and breast cancer: Evolution, diet, and estrogens. Urology 57 (Suppl 4A):31-38.
22. Cook LS, Goldoft M, Schwartz SM, Weiss NS. 1999. Incidence of adenocarcinoma of the prostate in Asian immigrants to the United States and their descendants. J Urol 161:152-155.
23. Cunningham JM, Hebbring SJ, McDonnell SK, Cicek MS, Christensen GB, Wang L, Jacobsen SJ, Cerhan JR, Blute ML, Schaid DJ, Thibodeau SN. 2007. Evaluation of genetic variations in the androgen and estrogen metabolic pathways as risk factors for sporadic and familial prostate cancer. Cancer Epidemiol Biomarkers Prev 16:969-978.
24. Eaton NE, Reeves GK, Appleby PN, Key TJ. 1999. Endogenous sex hormones and prostate cancer: A quantitative review of prospective studies. Br J Cancer 80:930-934.
25. Ellem SJ, Risbridger GP. 2006. Aromatase and prostate cancer. Minerva Endocrinol 31:1-12.
26. Escriva H, Bertrand S, Laudet V. 2004. The evolution of the nuclear receptor superfamily. Essays Biochem 40:11-26.
27. Farnsworth WE, Brown JR. 1976. Androgen of the human prostate. Endocr Res Commun 3:105-117.
28. Friedman AE. 2005. The estradiol-dihydrotestosterone model of prostate cancer. Theor Biol Med Model 2(1):10.
29. Ganmaa D, Li XM, Qin LQ, Wang PY, Takeda M, Sato A. 2003. The experience of Japan as a clue to the etiology of testicular and prostatic cancers. Med Hypotheses 60:724-730.
30. Gann PH, Hennekens CH, Ma J, Longcope C, Stampfer MJ. 1996. Prospective study of sex hormone levels and risk of prostate cancer. J Natl Cancer Inst 88:1118-1126.
31. Ganry O. 2005. Phytoestrogens and prostate cancer risk. Prev Med 41:1-6.
32. Geller J, Albert J, de la Vega D, Loza D, Stoeltzing W. 1978. Dihydrotestosterone concentration in prostate cancer tissue as a predictor of tumor differentiation and hormonal dependency. Cancer Res 38:4349-4352.
33. Giovannucci E, Leitzman M, Speigelman D, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. 1998. A prospective study of physical activity and prostate cancer in male health professionals. Cancer Res 58:5117-5122.
34. Gustafsson JA. 2003. What pharmacologists can learn from recent advances in estrogen signalling. Trends Pharmacol Sci 24:479-495.
35. Herynk MH, Fuqua SAW. 2004. Estrogen receptor mutations in human disease. Endocr Rev 25:869-898.
36. Ho SM. 2004. Estrogens and antiestrogens: Key mediators of prostate carcinogenesis and new therapeutic candidates. J Cell Biochem 91:491-503.
37. Hsing AW, Chokkalingam AP. 2006. Prostate cancer epidemiology. Front Biosci 11:1388-1413.
38. Iguchi T, Fukazawa Y, Tani N, Sato T, Ozawa S, Takasugi N, Shuin T, Kubotal Y, Petrov V. 1990. Effect of some hormonally active steroids upon the growth of LNCaP human prostate tumour cells in vitro. Cancer J 3:184-191.
39. Jarred RA, Cancilla B, Prins GS, Thayer KA, Cunha GR, Risbridger GP. 2000. Evidence that estrogens directly alter androgen-regulated prostate development. Endocrinology 141:3471-3477.
40. Kolonel LN. 1996. Nutrition and prostate cancer. Cancer Causes Control 7:83-94.
41. Kolonel LN, Nomura AM, Cooney RV. 1999. Dietary fat and prostate cancer: Current status. J Natl Cancer Inst 91:414-428.
42. Kolonel LN, Altshuler D, Henderson BE. 2004. The multiethnic cohort study: Exploring genes, lifestyle and cancer risk. Nat Rev Cancer 4:519-527.
43. Kuiper GGJM, Carlquist M, Gustafsson JA. 1998. Estrogen is a male and female hormone. Sci Med 5:36-45.
44. Labrie F, Luu-The V, Labrie C, Belanger A, Simard J, Lin SX, Pellitier G. 2003. Endocrine and intracrine sources of androgens in women: Inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone. Endocr Rev 24:152-182.
45. Leader JE, Wang C, Popov VM, Fu M, Pestell RG. 2006. Epigenetics and the estrogen receptor. Ann NY Acad Sci 1089:73-87.
46. Leav I, Merk FB, Kwan PW, Ho SM. 1989. Androgen supported estrogen-enhanced epithelial proliferation in the prostates of intact Noble rats. Prostate 15:23-40.
47. Levin ER. 2001. Cell Localization, physiology and non-genomic actions of estrogen receptors. J Appl Physiol 91:1860-1867.
48. Li LC, Okino ST, Dahiya R. 2004. DNA methylation in prostate cancer. Biochim Biophys Acta 1704:87-102.
49. Maffini MV, Rubin BS, Sonnenschein C, Soto AM. 2006. Endocrine disruptors and reproductive health: The case of bisphenol-A. Mol Cell Endocrinol 254-255:179-186.
50. McLachlan JA. 2001. Environmental signaling: What embryos and evolution teach us about endocrine disrupting chemicals. Endocr Rev 22:319-341.
51. McPherson SJ, Wang H, Jones ME, Pedersen J, Iismaa TP, Wreford N, Simpson ER, Risbridger GP. 2001. Elevated androgens and prolactin in aromatase-deficient mice cause enlargement, but not malignancy, of the prostate gland. Endocrinology 142:2458-2467.
52. Mentor-Marcel R, Lamartiniere CA, Eltoum IE, Greenberg NM, Elgavish A. 2001. Genistein in the diet reduces the incidence of poorly differentiated prostatic adenocarcinoma in transgenic mice (TRAMP). Cancer Res 61:6777-6782.
53. Merk FB, Warhol MJ, Kwan PW, Leav I, Alroy J, Ofner P, Pinkus GS. 1986. Multiple phenotypes of prostatic glandular cells in castrated dogs after individual or combined treatment with androgen and estrogen. Morphometric, ultrastructural, and cytochemical distinctions. Lab Invest 54:442-456.
54. Mononen N, Seppala EH, Duggal P, Autio V, Ikonen T, Ellonen P, Saharinen J, Saarela J, Vihinen M, Tammela TL, Kallioniemi O, Bailey-Wilson JE, Schleutker J. 2006. Profiling genetic variation along the androgen biosynthesis and metabolism pathways implicates several single nucleotide polymorphisms and their combinations as prostate cancer risk factors. Cancer Res 66:743-747.
55. Mueller SO, Korach SK. 2001. Estrogen receptors and endocrine diseases: Lessons from estrogen receptor knockout mice. Curr Opin Pharmacol 1:613-619.
56. Murata M, Watanabe M, Yamanaka M, Kubota Y, Ito H, Nagao M, Katoh T, Kamataki T, Kawamura J, Yatani R, Shiraishi T. 2001. Genetic polymorphisms in cytochrome P450 (CYP) 1A1. CYP1A2, CYP2E1, glutathione S-transferase (GST) M1 and GSTT1 and susceptibility to prostate cancer in the Japanese population. Cancer Lett 165:171-177.
57. Muti P, Westerlind K, Wu T, Grimaldi T, De Berry J III, Schunemann H, Freudenheim JL, Hill H, Carruba G, Bradlow L. 2002. Urinary estrogen metabolites and prostate cancer: A case-control study in the United States. Cancer Causes Control 13:947-955.
58. Noble RL. 1982. Prostate carcinoma of the Nb rat in relation to hormones. Int Rev Exp Pathol 23:113-159.
59. Nock NL, Cicek MS, Li L, Liu X, Rybicki BA, Moreira A, Plummer SJ, Casey G, Witte JS. 2006. Polymorphisms in estrogen bioactivation, detoxification and oxidative DNA base excision repair genes and prostate cancer risk. Carcinogenesis 27:1842-1848.
60. Ockrim J, Lalani E-N, Aubel P. 2006. Therapy insight: Parenteral estrogen treatment for prostate cancer - A new dawn for an old therapy. Nat Clin Pract Oncol 3:552-563.
61. Ofner P, Bosland MC, Vena RL. 1992. Differential effects of diethylstilbestrol and estradiol-17β in combination with testosterone on rat prostate lobes. Toxicol Appl Pharmacol 112:300-309.
62. Parkin DM, Bray F, Ferlay J, Pisani P. 2005. Global cancer statistics, 2002. CA Cancer J Clin 55:74-108.
63. Peng B, Lu B, Leygue E, Murphy LC. 2003. Putative functional characteristics of human estrogen receptor-beta isoforms. J Mol Endocrinol 30:13-29.
64. Penot G, Le Péron C, Mérot Y, Grimaud-Fanouillère E, Ferriere F, Boujrad N, Kah O, Saligaut C, Ducouret B, Métivier R, Flouriot G. 2005. The human estrogen receptor-α isoform hERα46 antagonizes the proliferative influence of hERα66 in MCF7 breast cancer cells. Endocrinology 146:5474-5484.
65. Platz EA, Leitzmann MF, Rifai N, Kantoff PW, Chen YC, Stampfer MJ, Willett WC, Giovannucci E. 2005. Sex steroid hormones and the androgen receptor gene CAG repeat and subsequent risk of prostate cancer in the prostate-specific antigen era. Cancer Epidemiol Biomarkers Prev 14:1262-1269.
66. Pollard M, Luckert PH, Schmidt MA. 1982. Induction of prostate adenocarcinomas in Lobund Wistar rats by testosterone. Prostate 3:563-568.
67. Popov VM, Wang C, Shirley LA, Rosenberg A, Li S, Nevalainen M, Fu M, Pestell RG. 2007. The functional significance of nuclear receptor acetylation. Steroids 72:221-230.
68. Prins GS, Huang L, Birch L, Pu Y. 2006. The role of estrogens in normal and abnormal development of the prostate gland. Ann NY Acad Sci 2006. 1089:1-13.
69. Prins GS, Birch L, Tang WY, Ho SM. 2007. Developmental estrogen exposures predispose to prostate carcinogenesis with aging. Reprod Toxicol 23:374-382.
70. Raghow S, Hooshdaran MZ, Katiyar S, Steiner MS. 2002. Toremifene prevents prostate cancer in the transgenic adenocarcinoma of mouse prostate model. Cancer Res 62:1370-1376.
71. Rohrmann S, Roberts WW, Walsh PC, Platz EA. 2003. Family history of prostate cancer and obesity in relation to high-grade disease and extraprostatic extension in young men with prostate cancer. Prostate 55:140-146.
72. Schatzl G, Madersbacher S, Thurridl T, Waldmuller J, Kramer G, Haitel A, Marberger M. 2001. High-grade prostate cancer is associated with low serum testosterone levels. Prostate 47:52-58.
73. Sim HG, Cheng CW. 2005. Changing demography of prostate cancer in Asia. Eur J Cancer 41:834-845.
74. Simpson ER, Misso M, Hewitt KN, Hill RA, Boon WC, Jones ME, Kovacic A, Zhou J, Clyne CD. 2005. Estrogen - The good, the bad, and the unexpected. Endocr Rev 26:322-330.
75. Sonnenschein C, Olea N, Pasanen ME, Soto AM. 1989. Negative controls of cell proliferation: Human prostate cancer cells and androgens. Cancer Res 49:3474-3481.
76. Takahashi M, Shimomoto T, Miyajima K, Yoshida M, Katashima S, Uematsu F, Maekawa A, Naka D. 2004. Effects of estrogens and metabolites on endometrial carcinogenesis in young adult mice initiated with N-ethyl-N0- nitro-N-nitrosoguanidine. Cancer Lett 211:1-9.
77. Thompson CJ, Tam NN, Joyce JM, Leav I, Ho SM. 2002. Gene expression profiling of testosterone and estradiol-17 beta-induced prostatic dysplasia in Noble rats and response to the antiestrogen ICI 182,780. Endocrinology 143:2093-2105.
78. Thompson IM, Goodman PJ, Tangen CM, Lucia MS, Miller GJ, Ford LG, Lieber MM, Cespedes RD, Atkins JN, Lippman SM, Carlin SM, Ryan A, Szczepanek CM, Crowley JJ, Coltman CA, Jr. 2003. The influence of finasteride on the development of prostate cancer. N Engl J Med 349:215-224.
79. Trosko JE. 2007. Stem cells and cell-cell communication in the understanding of the role of diet and nutrients in human diseases. J Fd Hyg Safety 22:1-14.
80. van Landeghem AAJ, Poortman J, Nabuurs M, Thijssen JHH. 1985. Endogenous concentration and subcellular distribution of estrogens in normal and malignant human breast tissue. Cancer Res 45:2900-2906.
81. Vermeulen A, Kaufman JM, Goemaere S, van Pottelberg I. 2002. Estradiol in elderly men. Aging Male 5:98-102.
82. Vihko P, Herrala A, Harkonen P, Isomaa V, Kaija H, Kurkela R, Pulkka A. 2006. Control of cell proliferation by steroids: The role of 17HSDs. Mol Cell Endocrinol 248:141-148.
83. Wang Y, Hayward SW, Donjacour AA, Young P, Jacks T, Sage J, Dahiya R, Cardiff RD, Day ML, Cunha GR. 2000. Sex hormone-induced carcinogenesis in Rb-deficient prostate tissue. Cancer Res 60:6008-6017.
84. Wang ZY, Zhang XT, Shen P, Loggie BW, Chang YC, Deuel TF. 2006. A variant of estrogen receptor-α, hER-α36: Transduction of estrogen- and antiestrogen-dependent membrane-initiated mitogenic signalling. Proc Natl Acad Sci USA 103:9063-9068.
85. Weihua Z, Makela S, Andersson LC, Salmi S, Saji S, Webster JI, Jensen EV, Nilsson S, Warner M, Gustafsson JA. 2001. A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc Natl Acad Sci USA 98:6330-6335.
86. Wirén S, Stocks T, Rinaldi S, Hallmans G, Bergh A, Stenman UH, Kaaks R, Stattin P. 2007. Androgens and prostate cancer risk: A prospective study. Prostate 67:1230-1237.
87. Wynder EL, Fujita Y, Harris RE, Hirayama T, Hiyama T. 1991. Comparative epidemiology of cancer between the United States and Japan. A second look. Cancer 67:746-763.
88. Yager JD, Davidson NE. 2006. Estrogen carcinogenesis in breast cancer. N Engl J Med 354:270-282.