Mechanisms enforcing the estrogen receptor β selectivity of botanical estrogens

FASEB Journal

Volumn 27, Issue 11, 2013, Pages 4406-4418

  Jiang, Yan ^a   Gong, Ping ^a   Madak Erdogan, Zeynep ^a   Martin, Teresa ^b   Jeyakumar, Muthu ^b   Carlson, Kathryn ^b   Khan, Ikhlas ^c   Smillie, Troy J ^c   Chittiboyina, Amar G ^c   Rotte, Sateesh C K ^c   Helferich, William G ^b   Katzenellenbogen, John A ^b   Katzenellenbogen, Benita S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Breast cancer cells; Chromatin binding; Gene regulation; Proliferation

Indexed keywords

BIOCHANIN A; BOTANICAL ESTROGEN; DAIDZEIN; EQUOL; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FORMONONETIN; GENISTEIN; LIQUIRITIGENIN; PROGESTERONE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING ASSAY; BINDING SITE; BREAST CANCER; CANCER CELL; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; DRUG SELECTIVITY; ENANTIOMER; ESTROGEN ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IC 50; LIGAND BINDING; PRIORITY JOURNAL; TARGET CELL;

BREAST CANCER CELLS; CHROMATIN BINDING; GENE REGULATION; PROLIFERATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BINDING SITES; CELL PROLIFERATION; CHROMATIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HUMANS; MCF-7 CELLS; NUCLEAR PROTEINS; NUCLEAR RECEPTOR COACTIVATOR 3; PHYTOESTROGENS; TRANSCRIPTION, GENETIC;

EID: 84887088487     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-234617     Document Type: Article

References (60)

1. Manson, J. E., Hsia, J., Johnson, K C, Rossouw, J. E., Assaf, A. R., Lasser, N. L., Trevisan, M., Black, H. R., Heckbert, S. R., Detrano, R., Strickland, O. L., Wong, N. D., Crouse, J. R., Stein, E., and Cushman, M. (2003) Estrogen plus progestin and the risk of coronary heart disease. N. Engl J. Med. 349, 523-534 (Pubitemid 36951364)
2. Wassertheil-Smoller, S., Hendrix, S. L., Limacher, M., Heiss, G., Kooperberg, C, Baird, A, Kotchen, T., Curb, J. D., Black, H., and Rossouw., J. E., Aragaki, A, Safford, M., Stein, E., Laowattana, S., and Mysiw, W. J. (2003) Effect of estrogen plus progestin on stroke in postmenopausal women: the Women's Health Initiative: a randomized trial. JAMA 289, 2673-2684 (Pubitemid 37430138)
3. Chlebowski, R. T., and Hendrix., S. L., Langer, R. D., Stefanick, M. L., Gass, M., Lane, D., Rodabough, R.J., Gilligan, M. A, Cyr, M. G., Thomson, C. A, Khandekar, J., Petrovitch, H., and McTiernan, A. (2003) Influence of estrogen plus progestin on breast cancer and mammography in healthy postmenopausal women: the Women's Health Initiative Randomized Trial. JAMA 289, 3243-3253 (Pubitemid 37430077)
4. Shumaker, S. A, Legault, C., and Rapp., S. R., Thal, L., Wallace, R B., Ockene, J. K, Hendrix, S. L., Jones, B. N., 3rd, Assaf, A. R., Jackson, R. D., Kotchen, J. M., Wassertheil-Smoller, S., and Wactawski-Wende, J. (2003) Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289, 2651-2662 (Pubitemid 37430136)
5. Shumaker, S. A, Legault, C., Kuller, L., Rapp, S. R., Thal, L., and Lane., D. S., Fillit, H., Stefanick, M. L., Hendrix, S. L., Lewis, C. E., Masaki, K, and Coker, L. H. (2004) Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291, 2947-2958 (Pubitemid 38802684)
6. Kuiper, G. G., and Lemmen., J. G., Carlsson, B., Corton, J. C, Safe, S. H., van der Saag, P. T., van der Burg, B., and Gustafsson, J. A (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139, 4252-4263 (Pubitemid 28513713)
7. Allred, C. D., Allred, K. F., Ju, Y. H., Virant, S. M., and Helferich, W. G. (2001) Soy diets containing varying amounts of genistein stimulate growth of estrogen-dependent (MCF-7) tumors in a dose-dependent manner. Cancer Res. 61, 5045-5050 (Pubitemid 32681533)
8. Hsieh, C. Y., and Santell., R. C., Haslam, S. Z., and Helferich, W. G. (1998) Estrogenic effects of genistein on the growth of estrogen receptor-positive human breast cancer (MCF-7) cells in vitro and in vivo. Cancer Res. 58, 3833-3838 (Pubitemid 28405638)
9. Huntley, A. L., and Ernst, E. (2004) Soy for the treatment of perimenopausal symptoms: a systematic review. Maturitas 47, 1-9 (Pubitemid 38050010)
10. Taku, K, Melby, M. K, Kronenberg, F., and Kurzer., M. S., and Messina, M. (2012) Extracted or synthesized soybean isoflavones reduce menopausal hot flash frequency and severity: systematic review and meta-analysis of randomized controlled trials. Menopause 19, 776-790
11. Siow, R. C., and Li., F. Y., Rowlands, D.J., de Winter, P., and Mann, G. E. (2007) Cardiovascular targets for estrogens and phytoestrogens: transcriptional regulation of nitric oxide synthase and antioxidant defense genes. Free Radic. Biol. Med. 42, 909-925 (Pubitemid 46356896)
12. Butler, L. M., and Wu., A. H., Wang, R., Koh, W. P., and Yuan., J. M., and Yu, M. C. (2010) A vegetable-fruit-soy dietary pattern protects against breast cancer among postmenopausal Singapore Chinese women. Am. J. Clin. Nutr. 91, 1013-1019
13. Levis, S., Strickman-Stein, N., Ganjei-Azar, P., Xu, P., and Doerge., D. R., and Krischer, J. (2011) Soy isoflavones in the prevention of menopausal bone loss and menopausal symptoms: a randomized, double-blind trial. Arch. Intern. Med. 171, 1363-1369
14. Pitkin, J. (2012) Alternative and complementary therapies for the menopause. Menopause Int. 18, 20-27
15. Sacks, F. M., Lichtenstein, A., Van Horn, L., Harris, W., Kris-Etherton, P., and Winston, M. (2006) Soy protein, isoflavones, and cardiovascular health: an American Heart Association Science Advisory for professionals from the Nutrition Committee. Circulation 113, 1034-1044 (Pubitemid 43879479)
16. Hilakivi-Clarke, L., Andrade, J. E., and Helferich, W. (2010) Is soy consumption good or bad for the breast? J. Nutr. 140, 2326S-2334S
17. Kuiper, G. G., Carlsson, B., Grandien, K., Enmark, E., Haggblad, J., Nilsson, S., and Gustafsson, J. A. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863-870 (Pubitemid 27089735)
18. Harris, H. A. (2007) Estrogen receptor-beta: recent lessons from in vivo studies. Mol. Endocrinol. 21, 1-13 (Pubitemid 46041687)
19. Pettersson, K., and Gustafsson, J. A. (2001) Role of estrogen receptor beta in estrogen action. Annu. Rev. Physiol. 63, 165-192 (Pubitemid 32318327)
20. Katzenellenbogen, B. S., and Korach, K. S. (1997) A new actor in the estrogen receptor drama: enter ER-beta. Endocrinology 138, 861-862 (Pubitemid 27089734)
21. Sun, J., and Meyers., M. J., Fink, B. E., Rajendran, R., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. (1999) Novel ligands that function as selective estrogens or antiestrogens for estrogen receptor-alpha or estrogen receptor-beta. Endocrinology 140, 800-804 (Pubitemid 29058215)
22. Frasor, J., and Chang., E. C., Komm, B., Lin, C. Y., and Vega., V. B., Liu, E. T., Miller, L. D., Smeds, J., Bergh, J., and Katzenellenbogen, B. S. (2006) Gene expression preferentially regulated by tamoxifen in breast cancer cells and correlations with clinical outcome. Cancer Res. 66, 7334-7340 (Pubitemid 44197716)
23. Paruthiyil, S., Parmar, H., Kerekatte, V., Cunha, G. R., and Firestone., G. L., and Leitman, D. C. (2004) Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Res. 64, 423-428 (Pubitemid 38114127)
24. Chang, E. C., and Charn., T. H., Park, S. H., Helferich, W. G., Komm, B., and Katzenellenbogen., J. A., and Katzenellenbogen, B. S. (2008) Estrogen receptors alpha and beta as determinants of gene expression: influence of ligand, dose, and chromatin binding. Mol. Endocrinol. 22, 1032-1043 (Pubitemid 351629605)
25. Strom, A., Hartman, J., Foster, J. S., Kietz, S., Wimalasena, J., and Gustafsson, J. A. (2004) Estrogen receptor beta inhibits 17beta-estradiol- stimulated proliferation of the breast cancer cell line T47D. Proc. Natl. Acad. Sci. U. S. A. 101, 1566-1571 (Pubitemid 38236167)
26. Muthyala, R. S., and Ju., Y. H., Sheng, S., Williams, L. D., and Doerge., D. R., Katzenellenbogen, B. S., Helferich, W. G., and Katzenellenbogen, J. A. (2004) Equol, a natural estrogenic metabolite from soy isoflavones: convenient preparation and resolution of R- and S-equols and their differing binding and biological activity through estrogen receptors alpha and beta. Bioorg. Med. Chem. 12, 1559-1567 (Pubitemid 38304880)
27. Mersereau, J. E., Levy, N., Staub, R. E., Baggett, S., Zogovic, T., Chow, S., Ricke, W. A., Tagliaferri, M., Cohen, I., Bjeldanes, L. F., and Leitman, D. C. (2008) Liquiritigenin is a plant-derived highly selective estrogen receptor beta agonist. Mol. Cell. Endocrinol. 283, 49-57
28. Paruthiyil, S., Cvoro, A., Zhao, X., Wu, Z., Sui, Y., Staub, R. E., Baggett, S., and Herber., C. B., Griffin, C., Tagliaferri, M., Harris, H. A., Cohen, I., Bjeldanes, L. F., Speed, T. P., Schaufele, F., and Leitman, D. C. (2009) Drug and cell type-specific regulation of genes with different classes of estrogen receptor beta-selective agonists. PLoS ONE 4, e6271
29. Chang, E. C., Frasor, J., Komm, B., and Katzenellenbogen, B. S. (2006) Impact of estrogen receptor beta on gene networks regulated by estrogen receptor alpha in breast cancer cells. Endocrinology 147, 4831-4842 (Pubitemid 44402189)
30. Heemstra, J. M., and Kerrigan., S. A., Doerge, D. R., Helferich, W. G., and Boulanger, W. A. (2006) Total synthesis of (S)-equol. Org. Lett. 8, 5441-5443
31. Carlson, K. E., Choi, I., Gee, A., Katzenellenbogen, B. S., and Katzenellenbogen, J. A. (1997) Altered ligand binding properties and enhanced stability of a constitutively active estrogen receptor: evidence that an open pocket conformation is required for ligand interaction. Biochemistry 36, 14897-14905 (Pubitemid 27524414)
32. Katzenellenbogen, J. A., and Johnson., H. J., Jr., and Carlson, K. E. (1973) Studies on the uterine, cytoplasmic estrogen binding protein: thermal stability and ligand dissociation rate: an assay of empty and filled sites by exchange. Biochemistry 12, 4092-4099
33. Jeyakumar, M., and Carlson., K. E., Gunther, J. R., and Katzenellenbogen, J. A. (2011) Exploration of dimensions of estrogen potency: parsing ligand binding and coactivator binding affinities. J. Biol. Chem. 286, 12971-12982
34. Tamrazi, A., and Carlson., K. E., Daniels, J. R., Hurth, K. M., and Katzenellenbogen, J. A. (2002) Estrogen receptor dimerization: ligand binding regulates dimer affinity and dimer dissociation rate. Mol. Endocrinol. 16, 2706-2719 (Pubitemid 36020652)
35. Gunther, J. R., Du, Y., Rhoden, E., Lewis, I., Revennaugh, B., Moore, T. W., and Kim., S. H., Dingledine, R., Fu, H., and Katzenellenbogen, J. A. (2009) A set of time-resolved fluorescence resonance energy transfer assays for the discovery of inhibitors of estrogen receptor-coactivator binding. J. Biomol. Screen. 14, 181-193
36. Choi, I., Ko, C., Park-Sarge, O. K., Nie, R., Hess, R. A., Graves, C, and Katzenellenbogen, B. S. (2001) Human estrogen receptor beta-specific monoclonal antibodies: characterization and use in studies of estrogen receptor beta protein expression in reproductive tissues. Mol. Cell. Endocrinol. 181, 139-150 (Pubitemid 32703756)
37. Barnett, D. H., Sheng, S., Charn, T. H., Waheed, A., and Sly., W. S., Lin, C. Y., Liu, E. T., and Katzenellenbogen, B. S. (2008) Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res. 68, 3505-3515
38. Bergamaschi, A., and Katzenellenbogen, B. S. (2012) Tamoxifen downregulation of miR-451 increases 14-3-3zeta and promotes breast cancer cell survival and endocrine resistance. Oncogene 31, 39-47
39. Pike, A. C, Brzozowski, A. M., and Hubbard., R. E., Bonn, T., Thorsell, A. G., Engstrom, O., Ljunggren, J., Gustafsson, J. A., and Carlquist, M. (1999) Structure of the ligand-binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBOJ. 18, 4608-4618 (Pubitemid 29415516)
40. Wong, J. M., and Kendall., C. W., Marchie, A., Liu, Z., Vidgen, E., Holmes, C, and Jackson., C. J., Josse, R. G., Pencharz, P. B., and Rao., A. V., Vuksan, V., Singer, W., and Jenkins, D.J. (2012) Equol status and blood lipid profile in hyperlipidemia after consumption of diets containing soyfoods. Am. J. Clin. Nutr. 95, 564-571
41. Anstead, G. M., and Carlson., K. E., and Katzenellenbogen, J. A. (1997) The estradiol pharmacophore: ligand structure-estrogen receptor binding affinity relationships and a model for the receptor binding site. Steroids 62, 268-303 (Pubitemid 27114399)
42. Jeyakumar, M., and Katzenellenbogen, J. A. (2009) A dual-acceptor time-resolved Foster resonance energy transfer assay for simultaneous determination of thyroid hormone regulation of corepressor and coactivator binding to the thyroid hormone receptor: mimicking the cellular context of thyroid hormone action. Anal. Biochem. 386, 73-78
43. Jeyakumar, M., Webb, P., Baxter, J. D., and Scanlan., T. S., and Katzenellenbogen, J. A. (2008) Quantification of ligand-regulated nuclear receptor corepressor and coactivator binding, key interactions determining ligand potency and efficacy for the thyroid hormone receptor. Biochemistry 47, 7465-7476 (Pubitemid 351991025)
44. Simmler, C, Hajirahimkhan, A., Lankin, D. C, Bolton, J. L., Jones, T., and Soejarto., D. D., Chen, S. N., and Pauli, G. F. (2013) Dynamic residual complexity of the isoliquiritigenin-liquiritigenin interconversion during bioassay. J. Agric. Food Chem. 61, 2146-2157
45. Saijo, K., and Collier., J. G., Li, A. C, Katzenellenbogen, J. A., and Glass, C. K. (2011) An ADIOL-ERbeta-CtBP transrepression pathway negatively regulates microglia-mediated inflammation. Cell 145, 584-595
46. Charn, T. H., and Liu., E. T., Chang, E. C, Lee, Y. K., and Katzenellenbogen., J. A., and Katzenellenbogen, B. S. (2010) Genome-wide dynamics of chromatin binding of estrogen receptors alpha and beta: mutual restriction and competitive site selection. Mol. Endocrinol. 24, 47-59
47. Madak-Erdogan, Z., Charn, T.-H., Jiang, Y, and Liu., E. T., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. (2013) Integrative genomics of gene and metabolic regulation by estrogen receptors α and β and their coregulators. Mol. Syst. Biol. 9, 676
48. Williams, C, Edvardsson, K., Lewandowski, S. A., Strom, A., and Gustafsson, J. A. (2008) A genome-wide study of the repressive effects of estrogen receptor beta on estrogen receptor alpha signaling in breast cancer cells. Oncogene 27, 1019-1032 (Pubitemid 351225390)
49. Sareddy, G. R., and Nair., B. C., Gonugunta, V. K., Zhang, Q. G., Brenner, A., and Brann., D. W., Tekmal, R. R., and Vadlamudi, R. K. (2012) Therapeutic significance of estrogen receptor beta agonists in gliomas. Mol. Cancer Ther. 11, 1174-1182
50. Harrington, W. R., Sengupta, S., and Katzenellenbogen, B. S. (2006) Estrogen regulation of the glucuronidation enzyme UGT2B15 in estrogen receptor-positive breast cancer cells. Endocrinology 147, 3843-3850 (Pubitemid 44079389)
51. Peterson, T. G., and Ji., G. P., Kirk, M., Coward, L., Falany, C. N., and Barnes, S. (1998) Metabolism of the isoflavones genistein and biochanin A in human breast cancer cell lines. Am. J. Clin Nutr. 68, 1505S-1511S (Pubitemid 28550938)
52. Lindberg, M. K., Moverare, S., Skrtic, S., Gao, H., Dahlman-Wright, K., Gustafsson, J. A., and Ohlsson, C. (2003) Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice. Mol. Endocrinol. 17, 203-208 (Pubitemid 36187395)
53. Saji, S., Hirose, M., and Toi, M. (2005) Clinical significance of estrogen receptor beta in breast cancer. Cancer Chemother. Pharmacol. 56(Suppl. 1), 21-26
54. Shaaban, A. M., O'Neill, P. A., Davies, M. P., Sibson, R., West, C. R., Smith, P. H., and Foster, C. S. (2003) Declining estrogen receptor-beta expression defines malignant progression of human breast neoplasia. Am. J. Surg. Pathol. 27, 1502-1512 (Pubitemid 37486611)
55. Speirs, V., and Carder., P. J., Lane, S., Dodwell, D., Lansdown, M. R., and Hanby, A. M. (2004) Oestrogen receptor beta: what it means for patients with breast cancer. Lancet Oncol. 5, 174-181 (Pubitemid 38262850)
56. Gruvberger-Saal, S. K., Bendahl, P. O., and Saal., L. H., Laakso, M., Hegardt, C., Eden, P., Peterson, C., Malmstrom, P., Isola, J., Borg, A., and Ferno, M. (2007) Estrogen receptor beta expression is associated with tamoxifen response in ERalpha-negative breast carcinoma. Clin. Cancer Res. 13, 1987-1994 (Pubitemid 46649864)
57. Nilsson, S., and Koehler., K. F., and Gustafsson, J. A. (2011) Development of subtype-selective oestrogen receptor-based therapeutics. Nat. Rev. Drug Discov. 10, 778-792
58. Suzuki, S., and Gerhold., L. M., Bottner, M., Rau, S. W., Dela Cruz, C., Yang, E., Zhu, H., Yu, J., Cashion, A. B., Kindy, M. S., Merchenthaler, I., Gage, F. H., and Wise, P. M. (2007) Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J. Comp. Neurol. 500, 1064-1075 (Pubitemid 46110642)
59. Hartman, J., Strom, A., and Gustafsson, J. A. (2012) Current concepts and significance of estrogen receptor beta in prostate cancer. Steroids 77, 1262-1266
60. Prins, G. S., and Korach, K. S. (2008) The role of estrogens and estrogen receptors in normal prostate growth and disease. Steroids 73, 233-244