Rapid, nongenomic signaling effects of several xenoestrogens involved in early- vs. Late-stage prostate cancer cell proliferation

Endocrine Disruptors

Volumn 3, Issue 1, 2015, Pages e995003-1-e995003-11

  Koong, Luke Y ^a   Watson, Cheryl S ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

BPA; Coumestrol; Diet; Genistein; Membrane estrogen receptor; Resveratrol

Indexed keywords

COUMESTROL; CYCLIN D1; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; GENISTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; PROSTATE CANCER CELL LINE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 85013402836     PISSN: None     EISSN: 23273747     Source Type: Journal    
DOI: 10.4161/23273747.2014.995003     Document Type: Article

References (128)

1. Huang CK, Luo J, Lee SO,Chang C. Androgen receptor differential roles in stem/progenitor cells including prostate, embryonic, stromal, and hematopoietic lineages. Stem Cells 2014; 32(9):2299-308; PMID:24740898
2. Bowers JL, Tyulmenkov VV, Jernigan SC, Klinge CM. Resveratrol acts as a mixed agonist/antagonist for estrogen receptors alpha and beta. Endocrinology 2000; 141:3657-67; PMID:11014220
3. McCarty MF. Isoflavones made simple – Genistein’s agonist activity for the beta-type estrogen receptor mediates their health benefits. Medi Hypotheses 2006; 66:1093-114; PMID:16513288; http://dx.doi.org/10.1016/j.mehy.2004.11.046
4. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997; 138:863-70; PMID:9048584
5. Chandsawangbhuwana C, Baker ME. 3D models of human ERa and ERb complexed with coumestrol. Steroids 2014; 80:37-43; PMID:24315835; http://dx.doi.org/10.1016/j.steroids.2013.11.019
6. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998; 139:4252-63; PMID:9751507
7. Prins GS, Hu WY, Shi GB, Hu DP, Majumdar S, Li G, Huang K, Nelles JL, Ho SM, Walker CL, et al. Bisphenol A promotes human prostate stem-progenitor cell self-renewal and increases in vivo carcinogenesis in human prostate epithelium. Endocrinology 2014; 155:805-17; PMID:24424067; http://dx.doi.org/10.1210/en.2013-1955
8. Richter C, Birnbaum L, Farabollini F, Newbold R, Rubin B, Talsness C, Vandenbergh J, Walser-Kuntz D, vom Saal F. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 2007; 24:199-224; PMID:17683900; http://dx.doi.org/10.1016/j.reprotox.2007.06.004
9. Vandenberg L, Colborn T, Hayes T, Heindel J, Jacobs D, Lee D, Shioda T, Soto A, Vom Saal F, Welshons W, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 2012; 33:378-455; PMID:22419778; http://dx.doi.org/10.1210/er.2011-1050
10. Bharathi SP, Raj HM, Jain S, Banerjee BD, Ahmed T, Arora VK. Role of pesticides in the induction of tumor angiogenesis. Anticancer Res 2013; 33:231-40; PMID:23267150
11. De Flora S, Micale RT, La Maestra S, Izzotti A, D’Agostini F, Camoirano A, Davoli SA, Troglio MG, Rizzi F, Davalli P, et al. Upregulation of clusterin in prostate and DNA damage in spermatozoa from bisphenol A-treated rats and formation of DNA adducts in cultured human prostatic cells. Toxicol Sci 2011; 122:45-51; PMID:21536718; http://dx.doi.org/10.1093/toxsci/kfr096
12. Weinhouse C, Anderson OS, Bergin IL, Vandenbergh DJ, Gyekis JP, Dingman MA, Yang J, Dolinoy DC. Dose-dependent incidence of hepatic tumors in adult mice following perinatal exposure to bisphenol A. Environ Health Perspect 2014; 122:485-91; PMID:24487385
13. Giannandrea F, Paoli D, Fig_a-Talamanca I, Lombardo F, Lenzi A, Gandini L. Effect of endogenous and exogenous hormones on testicular cancer: the epidemiological evidence. Int J Dev Biol 2013; 57:255-63; PMID:23784836; http://dx.doi.org/10.1387/ijdb.130015fg
14. Cotter KA, Yershov A, Novillo A, Callard GV. Multiple structurally distinct ERa mRNA variants in zebrafish are differentially expressed by tissue type, stage of development and estrogen exposure. Gen Comp Endocrinol 2013; 194:217-29; PMID:24090614; http://dx.doi.org/10.1016/j.ygcen.2013.09.014
15. Wong RLY, Walker CL. Molecular Pathways: Environmental estrogens activate nongenomic signaling to developmentally reprogram the epigenome. Clin Cancer Res 2013; 19:3732-7; PMID:23549878; http://dx.doi.org/10.1158/1078-0432.CCR-13-0021
16. Vilahur N, Molina-Molina JM, Bustamante M, Murcia M, Arrebola JP, Ballester F, Mendez MA, Garcia-Esteban R, Guxens M, Marina LS, et al. Male specific association between xenoestrogen levels in placenta and birthweight. Environ Int 2013; 51:174-81; PMID:23262415; http://dx.doi.org/10.1016/j.envint.2012.10.004
17. Ibarluzea Jm J, Fernandez MF, Santa-Marina L, Olea-Serrano MF, Rivas AM, Aurrekoetxea JJ, Exposito J, Lorenzo M, Torne P, Villalobos M, et al. Breast cancer risk and the combined effect of environmental estrogens. Cancer Causes Control 2004; 15:591-600; PMID:15280638; http://dx.doi.org/10.1023/B:CACO.0000036167.51236.86
18. Wetherill YB, Petre CE, Monk KR, Puga A, Knudsen KE. The xenoestrogen bisphenol A induces inappropriate androgen receptor activation and mitogenesis in prostatic adenocarcinoma cells. Mol Cancer Ther 2002; 1:515-24; PMID:12479269
19. Rice S, Whitehead SA. Phytoestrogens and breast cancer– promoters or protectors? Endocr Relat Cancer 2006; 13:995-1015; PMID:17158751; http://dx.doi.org/10.1677/erc.1.01159
20. Jeng Y-J, Watson C. Proliferative and anti-proliferative effects of dietary levels of phytoestrogens in rat pituitary GH3/B6/F10 cells - the involvement of rapidly activated kinases and caspases. BMC Cancer 2009; 9:1-17; PMID:19118499; http://dx.doi.org/10.1186/1471-2407-9-334
21. Zhang Y, Li Q, Zhou D, Chen H. Genistein, a soya isoflavone, prevents azoxymethane-induced up-regulation of WNT/beta-catenin signalling and reduces colon pre-neoplasia in rats. Br J Nutr 2013; 109:33-42; PMID:22716201; http://dx.doi.org/10.1017/S0007114512000876
22. Schleipen B, Hertrampf T, Fritzemeier KH, Kluxen FM, Lorenz A, Molzberger A, VeldersM,Diel P. ERbeta-specific agonists and genistein inhibit proliferation and induce apoptosis in the large and small intestine. Carcinogenesis 2011; 32:1675-83; PMID:21856997; http://dx.doi.org/10.1093/carcin/bgr188
23. Chen J, Zeng J, Xin M, Huang W, Chen X. Formononetin induces cell cycle arrest of human breast cancer cells via IGF1/PI3K/Akt pathways in vitro and in vivo. Horm Metab Res 2011; 43:681-6; PMID:21932171; http://dx.doi.org/10.1055/s-0031-1275703
24. Shanmugam MK, Kannaiyan R, Sethi G. Targeting cell signaling and apoptotic pathways by dietary agents: role in the prevention and treatment of cancer. Nutr Cancer 2011; 63:161-73; PMID:21294053; http://dx.doi.org/10.1080/01635581.2011.523502
25. Alves RC, Almeida IM, Casal S, Oliveira MB. Isoflavones in coffee: influence of species, roast degree, and brewing method. J Agric Food Chem 2010; 58:3002-7;PMID:20131840; http://dx.doi.org/10.1021/jf9039205
26. Adjakly M, Ngollo M, Boiteux JP, Bignon YJ, Guy L, Bernard-Gallon D. Genistein and daidzein: different molecular effects on prostate cancer. Anticancer Res 2013; 33:39-44; PMID:23267126
27. Shenouda NS, Zhou C, Browning JD, Ansell PJ, Sakla MS, Lubahn DB, Macdonald RS. Phytoestrogens in common herbs regulate prostate cancer cell growth in vitro. Nutr Cancer 2004; 49:200-8; PMID:15489213; http://dx.doi.org/10.1207/s15327914nc4902_12
28. Lee YH, Yuk HJ, Park KH, Bae YS. Coumestrol induces senescence through protein kinase CKII inhibition-mediated reactive oxygen species production in human breast cancer and colon cancer cells. Food Chem 2013; 141:381-8; PMID:23768371; http://dx.doi.org/10.1016/j.foodchem.2013.03.053
29. Bommareddy A, Eggleston W, Prelewicz S, Antal A, Witczak Z, McCune DF, Vanwert AL. Chemoprevention of prostate cancer by major dietary phytochemicals. Anticancer Res 2013; 33:4163-74; PMID:24122979
30. Chang HT, Chou CT, Chen IL, Liang WZ, Kuo DH, Huang JK, Shieh P, Jan CR. Mechanisms of resveratrol-induced changes in [Ca(2C)]i and cell viability in PC3 human prostate cancer cells. J Recept Signal Transduct Res 2013; 33:298-303; PMID:23898810; http://dx.doi.org/10.3109/10799893.2013.822886
31. Wang TT, Schoene NW, Kim YS, Mizuno CS, Rimando AM. Differential effects of resveratrol and its naturally occurring methylether analogs on cell cycle and apoptosis in human androgen-responsive LNCaP cancer cells. Mol Nutr Food Res 2010; 54:335-44; PMID:20077416; http://dx.doi.org/10.1002/mnfr.200900143
32. Benitez DA, Pozo-Guisado E, Alvarez-Barrientos A, Fernandez-Salguero PM, Castellon EA. Mechanisms involved in resveratrol-induced apoptosis and cell cycle arrest in prostate cancer-derived cell lines. J Androl 2007; 28:282-93; PMID:17050787; http://dx.doi.org/10.2164/jandrol.106.000968
33. Scarlatti F, Sala G, Ricci C, Maioli C, Milani F, Minella M, Botturi M, Ghidoni R. Resveratrol sensitization of DU145 prostate cancer cells to ionizing radiation is associated to ceramide increase. Cancer Lett 2007; 253:124-30; PMID:17321671; http://dx.doi.org/10.1016/j.canlet.2007.01.014
34. Vandenberg L, Chahoud I, Heindel J, Padmanabhan V, Paumgartten F, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 2010; 118:1055-70; PMID:20338858; http://dx.doi.org/10.1289/ehp.0901716
35. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reproduct Toxicol 2007; 24:139-77; PMID:17825522; http://dx.doi.org/10.1016/j.reprotox.2007.07.010
36. Ge LC, Chen ZJ, Liu HY, Zhang KS, Liu H, Huang HB, Zhang G, Wong CK, Giesy JP, Du J, et al. Involvement of activating ERK1/2 through G protein coupled receptor 30 and estrogen receptor alpha/beta in low doses of bisphenol A promoting growth of Sertoli TM4 cells. Toxicol Lett 2014; 226:81-9; PMID:24495410; http://dx.doi.org/10.1016/j.toxlet.2014.01.035
37. Vinas R, Watson CS. Mixtures of xenoestrogens disrupt estradiol-induced non-genomic signaling and downstream functions in pituitary cells. Environ Health 2013; 12:26; PMID:23530988; http://dx.doi.org/10.1186/1476-069X-12-26
38. Bulayeva NN, Watson CS. Xenoestrogen-induced ERK-1 and ERK-2 activation via multiple membraneinitiated signaling pathways. Environ Health Perspect 2004; 112:1481-7; PMID:15531431; http://dx.doi.org/10.1289/ehp.7175
39. Wang W, Wang J, Wang Q, Wu W, Huan F, Xiao H. Bisphenol A modulates calcium currents and intracellular calcium concentration in rat dorsal root ganglion neurons. J Membr Biol 2013; 246:391-7 PMID:23575985; http://dx.doi.org/10.1007/s00232-013-9545-8
40. Wozniak AL, Bulayeva NN, Watson CS. Xenoestrogens at picomolar to nanomolar concentrations trigger membrane estrogen receptor-alpha-mediated Ca2C fluxes and prolactin release in GH3/B6 pituitary tumor cells. Environ Health Perspect 2005; 113:431-9; PMID:15811834; http://dx.doi.org/10.1289/ehp.7505
41. Derouiche S, Warnier M, Mariot P, Gosset P, Mauroy B, Bonnal JL, Slomianny C, Delcourt P, Prevarskaya N, Roudbaraki M. Bisphenol A stimulates human prostate cancer cell migration remodelling of calcium signalling. Springerplus 2013; 2:54; PMID:23450760; http://dx.doi.org/10.1186/2193-1801-2-54
42. Midoro-Horiuti T, Tiwari R, Watson CS, Goldblum RM. Maternal bisphenol a exposure promotes the development of experimental asthma in mouse pups. Environ Health Perspect 2010; 118:273-7; PMID:20123615; http://dx.doi.org/10.1289/ehp.0901259
43. Lamartiniere CA. Protection against breast cancer with genistein: a component of soy. Am J Clin Nutr 2000; 71:1705S-7S; discussion 8S-9S; PMID:10837323
44. Magee PJ, Rowland IR. Phyto-oestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br J Nutr 2004; 91:513-31; PMID:15035679; http://dx.doi.org/10.1079/BJN20031075
45. Adlercreutz H. Phytoestrogens: epidemiology and a possible role in cancer protection. Environ Health Perspect 1995; 103(Suppl 7):103-12; PMID:8593855; http://dx.doi.org/10.1289/ehp.95103s7103
46. Abd Elmageed ZY, Moroz K, Srivastav SK, Fang Z, Crawford BE, Moparty K, Thomas R, Abdel-Mageed AB. High circulating estrogens and selective expression of ERbeta in prostate tumors of Americans: implications for racial disparity of prostate cancer. Carcinogenesis 2013; 34:2017-23; PMID:23658372; http://dx.doi.org/10.1093/carcin/bgt156
47. Kunisue T, Tanabe S, Isobe T, Aldous KM, Kannan K. Profiles of phytoestrogens in human urine from several Asian countries. J Agric Food Chem 2010; 58:9838-46; PMID:20707345; http://dx.doi.org/10.1021/jf102253j
48. Vergne S, Sauvant P, Lamothe V, Chantre P, Asselineau J, Perez P, Durand M, Moore N, Bennetau-Pelissero C. Influence of ethnic origin (Asian v. Caucasian) and background diet on the bioavailability of dietary isoflavones. Br J Nutr 2009; 102:1642-53; PMID:19622188; http://dx.doi.org/10.1017/S0007114509990833
49. Renouf M, Hendrich S. Bacteroides uniformis is a putative bacterial species associated with the degradation of the isoflavone genistein in human feces. J Nutr 2011; 141:1120-6; PMID:21525249; http://dx.doi.org/10.3945/jn.111.140988
50. Gaido KW, Leonard LS, Lovell S, Gould JC, Babai D, Portier CJ, McDonnell DP. Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormone receptor gene transcription assay. Toxicol Appl Pharmacol 1997; 143:205-12; PMID:9073609; http://dx.doi.org/10.1006/taap.1996.8069
51. Singleton DW, Feng Y, Chen Y, Busch SJ, Lee AV, Puga A, Khan SA. Bisphenol-A and estradiol exert novel gene regulation in human MCF-7 derived breast cancer cells. Mol Cell Endocrinol 2004; 221:47-55; PMID:15223131; http://dx.doi.org/10.1016/j.mce.2004.04.010
52. Sheeler CQ, Dudley MW, Khan SA. Environmental estrogens induce transcriptionally active estrogen receptor dimers in yeast: activity potentiated by the coactivator RIP140. Environ Health Perspect 2000; 108:97-103; PMID:10656848; http://dx.doi.org/10.1289/ehp.0010897
53. Gutendorf B, Westendorf J. Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phytoestrogens and xenoestrogens. Toxicology 2001; 166:79-89; PMID:11518614; http://dx.doi.org/10.1016/S0300-483X(01)00437-1
54. Kochukov M, Jeng Y-J, Watson C. Alkylphenol xenoestrogens with varying carbon chain lengths differentially and potently activate signaling and functional responses in GH3/B6/F10 somatomammotropes. Environ Health Perspect 2009; 117:723-30; PMID:19479013; http://dx.doi.org/10.1289/ehp.0800182
55. Vinas R, Watson C. Bisphenol s disrupts estradiolinduced nongenomic signaling in a rat pituitary cell line: effects on cell functions. Environ Health Perspect 2013; 121:352-8;
56. PMID:23458715; http://dx.doi.org/10.1289/ehp.1205826
57. Watson CS, Alyea RA, Jeng YJ, Kochukov MY. Nongenomic actions of low concentration estrogens and xenoestrogens on multiple tissues. Mol Cell Endocrinol 2007; 274:1-7; PMID:17601655; http://dx.doi.org/10.1016/j.mce.2007.05.011
58. Zsarnovszky A, Le HH, Wang HS, Belcher SM. Ontogeny of rapid estrogen-mediated extracellular signal-regulated kinase signaling in the rat cerebellar cortex: potent nongenomic agonist and endocrine disrupting activity of the xenoestrogen bisphenol A. Endocrinology 2005; 146:5388-96; PMID:16123166; http://dx.doi.org/10.1210/en.2005-0565
59. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B. Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc Natl Acad Sci U S A 2000; 97:11603-8; PMID:11027358; http://dx.doi.org/10.1073/pnas.97.21.11603
60. Sicotte NL, Liva SM, Klutch R, Pfeiffer P, Bouvier S, Odesa S, Wu TC, Voskuhl RR. Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann Neurol 2002; 52:421-8; PMID:12325070; http://dx.doi.org/10.1002/ana.10301
61. Voskuhl R, Wang H, Jackson Wu T, Sicotte N, Bates A, Beaver G, Corboy J, Cross A, Dhib-Jalbut S, Ford C, et al. A combination trial of estriol plus glatimer acetate in relapsing-remitting multiple sclerosis. Abstract from the American Academy of Neurology 2014 Annual Meeting 2014.
62. Watson C, Jeng Y-J, Kochukov M. Nongenomic actions of estradiol compared with estrone and estriol in pituitary tumor cell signaling and proliferation. FASEB J 2008; 22:3328-36; PMID:18541692; http://dx.doi.org/10.1096/fj.08-107672
63. vom Saal FS, Welshons WV. Large effects from small exposures. II. The importance of positive controls in low-dose research on bisphenol A. Environ Res 2006; 100:50-76; PMID:16256977; http://dx.doi.org/10.1016/j.envres.2005.09.001
64. Zhong L, Xiang X, Lu W, Zhou P, Wang L. Interference of xenoestrogen o,p0-DDT on the action of endogenous estrogens at environmentally realistic concentrations. Bull Environ Contam Toxicol 2013; 90:591-5; PMID:23478948; http://dx.doi.org/10.1007/s00128-013-0976-9
65. Jeng Y-J, Kochukov M, Watson C. Membrane estrogen receptor-alpha-mediated nongenomic actions of phytoestrogens in GH3/B6/F10 pituitary tumor cells. J Mol Signal 2009; 4:1-11; PMID:19320971; http://dx.doi.org/10.1186/1750-2187-4-2
66. Watson CS, Bulayeva NN, Wozniak AL, Alyea RA. Xenoestrogens are potent activators of nongenomic estrogenic responses. Steroids 2007; 72:124-34; PMID:17174995; http://dx.doi.org/10.1016/j.steroids.2006.11.002
67. Watson CS, Hu G, Paulucci-Holthauzen AA. Rapid actions of xenoestrogens disrupt normal estrogenic signaling. Steroids 2013; PMID:24269739
68. Jeng Y, Kochukov M, Watson C. Combinations of physiologic estrogens with xenoestrogens alter calcium and kinase responses, prolactin release, and membrane estrogen receptor trafficking in rat pituitary cells. Environ Health 2010; 9:61; PMID:20950447; http://dx.doi.org/10.1186/1476-069X-9-61
69. Watson CS, Bulayeva NN, Wozniak AL, Finnerty CC. Signaling from the membrane via membrane estrogen receptor-a: Estrogens, xenoestrogens, and phytoestrogens. Steroids 2005; 70:364-71; PMID:15862819; http://dx.doi.org/10.1016/j.steroids.2005.03.002
70. Koong LY, Watson CS. Direct estradiol and diethylstilbestrol actions on early- versus late-stage prostate cancer cells http://dx.doi.org/10.1002/pros.22875. Prostate 2014; 74(16):1589-603; PMID: 25213831; http://dx.doi.org/10.1002/pros.22875
71. Cagnol S, Chambard JC. ERK and cell death: Mechanisms of ERK-induced cell death - apoptosis, autophagy and senescence. FEBS J 2010; 277:2-21; PMID:19843174; http://dx.doi.org/10.1111/j.1742-4658.2009.07366.x
72. Klein KA, Reiter RE, Redula J, Moradi H, Zhu XL, Brothman AR, Lamb DJ, Marcelli M, Belldegrun A, Witte ON, et al. Progression of metastatic human prostate cancer to androgen independence in immunodeficient SCID mice. Nat Med 1997; 3:402-8; PMID:9095173; http://dx.doi.org/10.1038/nm0497-402
73. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 1979; 17:16-23; PMID:447482
74. Bulayeva NN, Gametchu B, Watson CS. Quantitative measurement of estrogen-induced ERK 1 and 2 activation via multiple membrane-initiated signaling pathways. Steroids 2004; 69:181-92; PMID:15072920; http://dx.doi.org/10.1016/j.steroids.2003.12.003
75. Viñas R, Goldblum RM, Watson CS. Rapid estrogenic signaling activities of the modified (chlorinated, sulfonated, and glucuronidated) endocrine disruptor bisphenol A. Endocrine Disruptors 2013; 1:0-9.
76. Gallagher RP, Kutynec CL. Diet, micronutrients and prostate cancer: a review of the evidence. Can J Urol 1997; 4:22-7; PMID:12735830
77. Hedelin M, Balter KA, Chang ET, Bellocco R, Klint A, Johansson JE, Wiklund F, Thellenberg-Karlsson C, Adami HO, Gronberg H. Dietary intake of phytoestrogens, estrogen receptor-beta polymorphisms and the risk of prostate cancer. Prostate 2006; 66:1512-20; PMID:16921512; http://dx.doi.org/10.1002/pros.20487
78. Nakamura H, Wang Y, Kurita T, Adomat H, Cunha GR. Genistein increases epidermal growth factor receptor signaling and promotes tumor progression in advanced human prostate cancer. PLoS One 2011; 6:e20034; PMID:21603581; http://dx.doi.org/10.1371/journal.pone.0020034
79. El Touny LH, Banerjee PP. Identification of a biphasic role for genistein in the regulation of prostate cancer growth and metastasis. Cancer Res 2009; 69:3695-703; PMID:19351854; http://dx.doi.org/10.1158/0008-5472.CAN-08-2958
80. Wang X, Clubbs EA, Bomser JA. Genistein modulates prostate epithelial cell proliferation via estrogen- and extracellular signal-regulated kinase-dependent pathways. J Nutr Biochem 2006; 17:204-10; PMID:16198100; http://dx.doi.org/10.1016/j.jnutbio.2005.07.005
81. Watson C, Gametchu B. Membrane-initiated steroid actions and the proteins that mediate them. Proc Soc Exp Biol Med 1999; 220:9-19; PMID:9893163; http://dx.doi.org/10.3181/00379727-220-44338
82. Zivadinovic D, Gametchu B, Watson CS. Membrane estrogen receptor-alpha levels in MCF-7 breast cancer cells predict cAMP and proliferation responses. Breast Cancer Res 2005; 7:R101-12; PMID:15642158; http://dx.doi.org/10.1186/bcr958
83. Hess KR, Pusztai L, Buzdar AU, Hortobagyi GN. Estrogen receptors and distinct patterns of breast cancer relapse. Breast Cancer Res Treat 2003; 78:105-18; PMID:12611463; http://dx.doi.org/10.1023/A:1022166517963
84. Bianchini G, Pusztai L, Karn T, Iwamoto T, Rody A, Kelly C, Muller V, Schmidt S, Qi Y, Holtrich U, et al. Proliferation and estrogen signaling can distinguish patients at risk for early versus late relapse among estrogen receptor positive breast cancers. Breast Cancer Res 2013; 15:R86; PMID:24060333
85. Signoretti S, Loda M. Estrogen receptor beta in prostate cancer: brake pedal or accelerator? Am J Pathol 2001; 159:13-6; PMID:11438447; http://dx.doi.org/10.1016/S0002-9440(10)61666-5
86. Campbell CH, Watson CS. A comparison of membrane vs. intracellular estrogen receptor-alpha in GH (3)/B6 pituitary tumor cells using a quantitative plate immunoassay. Steroids 2001; 66:727-36; PMID:11522334; http://dx.doi.org/10.1016/S0039-128X(01)00106-4
87. Watson CS, Campbell CH, Gametchu B. Membrane oestrogen receptors on rat pituitary tumour cells: immuno-identification and responses to oestradiol and xenoestrogens. Exp Physiol 1999; 84:1013-22 PMID:10564698; http://dx.doi.org/10.1111/j.1469-445X.1999.01903.x
88. Alyea R, Laurence S, Kim S, Katzenellenbogen B, Katzenellenbogen J, Watson C. The roles of membrane estrogen receptor subtypes in modulating dopamine transporters in PC-12 cells. J Neurochem 2008; 106:1525-33; PMID:18489713; http://dx.doi.org/10.1111/j.1471-4159.2008.05491.x
89. Gametchu B, Watson CS. Plasma membrane-associated glucocorticoid hormone receptor in human leukemic patients: clinical implications. In: Glucocorticoid Receptor Structure and Leukemic Cell Responses. B Gametchu, ed. Austin: R.G. Landes Company, 1995:163-76.
90. Hartman J, Str€om A, Gustafsson J-A. Current concepts and significance of estrogen receptor b in prostate cancer. Steroids 2012; 77:1262-6; PMID:22824289; http://dx.doi.org/10.1016/j.steroids.2012.07.002
91. Lai JS, Brown LG, True LD, Hawley SJ, Etzioni RB, Higano CS, Ho SM, Vessella RL, Corey E. Metastases of prostate cancer express estrogen receptor-beta. Urology 2004; 64:814-20; PMID:15491740; http://dx.doi.org/10.1016/j.urology.2004.05.036
92. Chan QK, Lam HM, Ng CF, Lee AY, Chan ES, Ng HK, Ho SM, Lau KM. Activation of GPR30 inhibits the growth of prostate cancer cells through sustained activation of Erk1/2, c-jun/c-fos-dependent upregulation of p21, and induction of G(2) cell-cycle arrest. Cell Death Differ 2010; 17:1511-23; PMID:20203690; http://dx.doi.org/10.1038/cdd.2010.20
93. Comeglio P, Morelli A, Cellai I, Vignozzi L, Sarchielli E, Filippi S, Maneschi E, Corcetto F, Corno C, Gacci M, et al. Opposite effects of tamoxifen on metabolic syndrome-induced bladder and prostate alterations: a role for GPR30/GPER? Prostate 2014; 74:10-28; PMID:24037776; http://dx.doi.org/10.1002/pros.22723
94. Zhang Z, Duan L, Du X, Ma H, Park I, Lee C, Zhang J, Shi J. The proliferative effect of estradiol on human prostate stromal cells is mediated through activation of ERK. Prostate 2008; 68:508-16; PMID:18213633; http://dx.doi.org/10.1002/pros.20722
95. Revankar CM, Mitchell HD, Field AS, Burai R, Corona C, Ramesh C, Sklar LA, Arterburn JB, Prossnitz ER. Synthetic estrogen derivatives demonstrate the functionality of intracellular GPR30. ACS Chem Biol 2007; 2:536-44; PMID:17655271; http://dx.doi.org/10.1021/cb700072n
96. Yu X, Filardo EJ, Shaikh ZA. The membrane estrogen receptor GPR30 mediates cadmium-induced proliferation of breast cancer cells. Toxicol Appl Pharmacol 2010; 245:83-90; PMID:20153348; http://dx.doi.org/10.1016/j.taap.2010.02.005
97. Deschenes-Simard X, Kottakis F, Meloche S, Ferbeyre G. ERKs in cancer: friends or foes? Cancer Res 2014; 74:412-9; PMID:24408923; http://dx.doi.org/10.1158/0008-5472.CAN-13-2381
98. Roskoski Jr R. ERK1/2 MAP kinases: Structure, function, and regulation. Pharmacol Res 2012; 66:105-43; PMID:22569528; http://dx.doi.org/10.1016/j.phrs.2012.04.005
99. Chang F, Steelman LS, Shelton JG, Lee JT, Navolanic PM, Blalock WL, Franklin R, McCubrey JA. Regulation of cell cycle progression and apoptosis by Ras/Raf/MEK/ERK pathway. Int J Oncol 2003; 22:469-80; PMID:12579299
100. Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D. Estrogens as endogenous genotoxic agents–DNA adducts and mutations. J Natl Cancer Inst Monogr 2000; (27):75-93; PMID:10963621; http://dx.doi.org/10.1093/oxfordjournals.jncimonographs.a024247
101. Yuan L, Dietrich AK, Nardulli AM. 17beta-Estradiol alters oxidative stress response protein expression and oxidative damage in the uterus. Mol Cell Endocrinol 2014; 382:218-26; PMID:24103313; http://dx.doi.org/10.1016/j.mce.2013.09.023
102. Spencer WA, Vadhanam MV, Jeyabalan J, Gupta RC. Oxidative DNA damage following microsome/Cu(II)- mediated activation of the estrogens, 17beta-estradiol, equilenin, and equilin: role of reactive oxygen species. Chem Res Toxicol 2012; 25:305-14; PMID:22126130; http://dx.doi.org/10.1021/tx200356v
103. Alao JP. The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Mol Cancer 2007; 6:1-16; PMID:17199893; http://dx.doi.org/10.1186/1476-4598-6-24
104. Terada Y, Nakashima O, Inoshita S, Kuwahara M, Sasaki S, Marumo F. Mitogen-activated protein kinase cascade and transcription factors: the opposite role of MKK3/6-p38K and MKK1-MAPK. Nephrol Dial Transplant 1999; 14:45-7; PMID:10048449; http://dx.doi.org/10.1093/ndt/14.suppl_1.45
105. Zheng J, Li H, Zhu H, Xiao X, Ma Y. Genistein inhibits estradiol- and environmental endocrine disruptor- induced growth effects on neuroblastoma cells. Oncol Lett 2013; 5:1583-6; PMID:23761822
106. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998; 12:3499-511; PMID:9832503; http://dx.doi.org/10.1101/gad.12.22.3499
107. Yang K, Guo Y, Stacey WC, Harwalkar J, Fretthold J, Hitomi M, Stacey DW. Glycogen synthase kinase 3 has a limited role in cell cycle regulation of cyclin D1 levels. BMC Cell Biol 2006; 7:33; PMID:16942622; http://dx.doi.org/10.1186/1471-2121-7-33
108. Alao JP, Gamble SC, Stavropoulou AV, Pomeranz KM, Lam EW, Coombes RC, Vigushin DM. The cyclin D1 proto-oncogene is sequestered in the cytoplasm of mammalian cancer cell lines. Mol Cancer 2006; 5:7; PMID:16503970; http://dx.doi.org/10.1186/1476-4598-5-7
109. Casanovas O, Miro F, Estanyol JM, Itarte E, Agell N, Bachs O. Osmotic stress regulates the stability of cyclin D1 in a p38SAPK2-dependent manner. J Biol Chem 2000; 275:35091-7; PMID:10952989; http://dx.doi.org/10.1074/jbc.M006324200
110. Mikhailov A, Shinohara M, Rieder CL. Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the p38 MAPK checkpoint pathway. J Cell Biol 2004; 166:517-26; PMID:15302851; http://dx.doi.org/10.1083/jcb.200405167
111. Zou Y, Ewton DZ, Deng X, Mercer SE, Friedman E. Mirk/dyrk1B kinase destabilizes cyclin D1 by phosphorylation at threonine 288. J Biol Chem 2004; 279:27790-8; PMID:15075324; http://dx.doi.org/10.1074/jbc.M403042200
112. Pettersson K, Delaunay F, Gustafsson JA. Estrogen receptor beta acts as a dominant regulator of estrogen signaling. Oncogene 2000; 19:4970-8; PMID:11042684; http://dx.doi.org/10.1038/sj.onc.1203828
113. van Lipzig MM, ter Laak AM, Jongejan A, Vermeulen NP, Wamelink M, Geerke D, Meerman JH. Prediction of ligand binding affinity and orientation of xenoestrogens to the estrogen receptor bymolecular dynamics simulations and the linear interaction energy method. JMed Chem 2004; 47:1018-30; PMID:14761204; http://dx.doi.org/10.1021/jm0309607
114. Harris DM, Besselink E, Henning SM, Go VLW, Heber D. Phytoestrogens induce differential estrogen receptor alpha- or beta-mediated responses in transfected breast cancer cells. Exp Biol Med 2005; 230:558-68; PMID:16118406
115. Schreihofer DA. Transcriptional regulation by phytoestrogens in neuronal cell lines. Mol Cell Endocrinol 2005; 231:13-22; PMID:15713532; http://dx.doi.org/10.1016/j.mce.2004.12.006
116. Matthews JB, Twomey K, Zacharewski TR. In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors alpha and beta. Chem Res Toxicol 2001; 14:149-57; PMID:11258963
117. Jeng YJ, Watson CS. Proliferative and anti-proliferative effects of dietary levels of phytoestrogens in rat pituitary GH3/B6/F10 cells - the involvement of rapidly activated kinases and caspases. BMC Cancer 2009; 9:334; PMID:19765307; http://dx.doi.org/10.1186/1471-2407-9-334
118. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 1987; 262:5592-5; PMID:3106339
119. Yan GR, Xiao CL, He GW, Yin XF, Chen NP, Cao Y, He QY. Global phosphoproteomic effects of natural tyrosine kinase inhibitor, genistein, on signaling pathways. Proteomics 2010; 10:976-86; PMID:20049867
120. Daibata M, Mellinghoff I, Takagi S, Humphreys RE, Sairenji T. Effect of genistein, a tyrosine kinase inhibitor, on latent EBV activation induced by cross-linkage of membrane IgG in Akata B cells. J Immunol 1991; 147:292-7; PMID:1711079
121. Golden GA, Mason RP, Tulenko TN, Zubenko GS, Rubin RT. Rapid and opposite effects of cortisol and estradiol on human erythrocyte NaC,KC-ATPase activity: relationship to steroid intercalation into the cell membrane. Life Sci 1999; 65:1247-55; PMID:10503940; http://dx.doi.org/10.1016/S0024-3205(99)00360-4
122. Whiting KP, Restall CJ, Brain PF. Steroid hormoneinduced effects on membrane fluidity and their potential roles in non-genomic mechanisms. Life Sci 2000; 67:743-57; PMID:10968404; http://dx.doi.org/10.1016/S0024-3205(00)00669-X
123. Routledge EJ, White R, Parker MG, Sumpter JP. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J Biol Chem 2000; 275:35986-93; PMID:10964929; http://dx.doi.org/10.1074/jbc.M006777200
124. Leclercq G, Jacquot Y. Interactions of isoflavones and other plant derived estrogens with estrogen receptors for prevention and treatment of breast cancer-considerations concerning related efficacy and safety. J Steroid Biochem Mol Biol 2014; 139:237-44; PMID:23274118; http://dx.doi.org/10.1016/j.jsbmb.2012.12.010
125. van Bokhoven A, Varella-Garcia M, Korch C, Johannes WU, Smith EE, Miller HL, Nordeen SK, Miller GJ, Lucia MS. Molecular characterization of human prostate carcinoma cell lines. Prostate 2003; 57:205-25; PMID:14518029; http://dx.doi.org/10.1002/pros.10290
126. Maggiolini M, Vivacqua A, Carpino A, Bonofiglio D, Fasanella G, Salerno M, Picard D, Ando S. The mutant androgen receptor T877A mediates the proliferative but not the cytotoxic dose-dependent effects of genistein and quercetin on human LNCaP prostate cancer cells. Mol Pharmacol 2002; 62:1027-35; PMID:12391264; http://dx.doi.org/10.1124/mol.62.5.1027
127. Jeng Y, Watson C. Combinations of physiologic estrogens with xenoestrogens alter ERK phosphorylation profiles in rat pituitary cells. Environ Health Perspect 2011; 119:104-12; PMID:20870566; http://dx.doi.org/10.1289/ehp.1002512
128. Watson CS, Jeng Y-J, Guptarak J. Endocrine disruption via estrogen receptors that participate in nongenomic signaling pathways. J Steroid Biochem Mol Biol 2011; 127:44-50; PMID:21300151; http://dx.doi.org/10.1016/j.jsbmb.2011.01.015