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Interaction of Estrogenic Chemicals and Phytoestrogens with Estrogen Receptor ␤

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Interaction of Estrogenic Chemicals and Phytoestrogens with Estrogen Receptor ␤ 0013-7227/98/$03.00/0 Vol. 139, No. 10 Endocrinology Printed in U.S.A. Copyright © 1998 by The Endocrine Society Interaction of Estrogenic Chemicals and Phytoestrogens with Estrogen Receptor b GEORGE G. J. M. KUIPER*, JOSEPHINE G. LEMMEN, BO CARLSSON, J. CHRISTOPHER CORTON, STEPHEN H. SAFE, PAUL T. VAN DER SAAG, BART VAN DER BURG†, AND JAN-ÅKE GUSTAFSSON‡ Center for Biotechnology and Department of Medical Nutrition (G.G.J.M.K., J.-Å.G.), Karolinska Institute and KaroBio AB (B.C.) Huddinge, Sweden; Hubrecht Laboratory, Netherlands Institute for Developmental Biology (B.v.d.B., P.T.v.d.S., J.G.L.) Utrecht, The Netherlands; Chemical Industry Institute of Toxicology (J.C.C.), Research Triangle Park, North Carolina; Department of Veterinary Physiology and Pharmacology (S.H.S.), Texas A&M University, College Station, Texas 77843-4466 ABSTRACT instance nonylphenol, bisphenol A, o, p9-DDT and 29,49,69-trichloro- The rat, mouse and human estrogen receptor (ER) exists as two 4-biphenylol stimulate the transcriptional activity of ERa and ERb at subtypes, ERa and ERb, which differ in the C-terminal ligand-bind- concentrations of 100-1000 nM. Phytoestrogens, including genistein, ing domain and in the N-terminal transactivation domain. In this coumestrol and zearalenone stimulate the transcriptional activity of study, we investigated the estrogenic activity of environmental chem- both ER subtypes at concentrations of 1–10 nM. The ranking of the icals and phytoestrogens in competition binding assays with ERa or estrogenic potency of phytoestrogens for both ER subtypes in the b .. 5 ER protein, and in a transient gene expression assay using cells in transactivation assay is different; that is, E2 zearalenone which an acute estrogenic response is created by cotransfecting cul- coumestrol . genistein . daidzein . apigenin 5 phloretin . bio- tures with recombinant human ERa or ERb complementary DNA chanin A 5 kaempferol 5 naringenin . formononetin 5 ipriflavone 5 5 a .. 5 . (cDNA) in the presence of an estrogen-dependent reporter plasmid. quercetin chrysin for ER and E2 genistein coumestrol Saturation ligand-binding analysis of human ERa and ERb protein zearalenone . daidzein . biochanin A 5 apigenin 5 kaempferol 5 3 b . 5 5 5 5 revealed a single binding component for [ H]-17 -estradiol (E2) with naringenin phloretin quercetin ipriflavone formononetin 5 b high affinity [dissociation constant (Kd) 0.05 - 0.1 nM]. All envi- chrysin for ER . Antiestrogenic activity of the phytoestrogens could ronmental estrogenic chemicals [polychlorinated hydroxybiphenyls, not be detected, except for zearalenone which is a full agonist for ERa dichlorodiphenyltrichloroethane (DDT) and derivatives, alkylphe- and a mixed agonist-antagonist for ERb. In summary, while the nols, bisphenol A, methoxychlor and chlordecone] compete with E2 for estrogenic potency of industrial-derived estrogenic chemicals is very binding to both ER subtypes with a similar preference and degree. In limited, the estrogenic potency of phytoestrogens is significant, es- most instances the relative binding affinities (RBA) are at least 1000- pecially for ERb, and they may trigger many of the biological re- fold lower than that of E2. Some phytoestrogens such as coumestrol, sponses that are evoked by the physiological estrogens. (Endocrinol- genistein, apigenin, naringenin, and kaempferol compete stronger ogy 139: 4252–4263, 1998) b a with E2 for binding to ER than to ER . Estrogenic chemicals, as for HE STEROID hormone estrogen influences the growth, tion of target genes (5–7). We have cloned a novel ER cDNA T differentiation, and functioning of many target tissues. from rat prostate (8), named ERb, different from the previ- These include tissues of the female and male reproductive ously cloned ER cDNA (consequently renamed ERa). Rat systems such as mammary gland, uterus, vagina, ovary, tes- ERb cDNA encodes a protein of 485 amino acid residues with tes, epididymis, and prostate (1). Estrogens also play an a calculated molecular weight of 54200. Rat ERb protein is important role in bone maintenance, in the central nervous highly homologous to rat ERa protein, particularly in the system and in the cardiovascular system where estrogens DNA binding domain (95% amino acid identity) and in the have certain cardioprotective effects (1–4). Estrogens diffuse C-terminal ligand binding domain (55% homology). In ad- in and out of cells but are retained with high affinity and dition, recently a variant rat ERb cDNA was cloned that has specificity in target cells by an intranuclear binding protein, an in-frame insertion of 54 nucleotides that results in the termed the estrogen receptor (ER). Once bound by estrogens, predicted insertion of 18 amino acids within the ligand- the ER undergoes a conformational change allowing the re- binding domain (9, 10). Mouse (11, 12) and human homologs ceptor to interact with chromatin and to modulate transcrip- (13, 14) of rat ERb have been cloned, and similar homologies in the various domains of the subtypes were found. Expres- Received January 2, 1998. sion of ERb was investigated by Northern blotting, RT-PCR, Address all correspondence and requests for reprints to: Dr. George and in situ hybridization; prominent expression was found Kuiper, Center for Biotechnology, NOVUM, S-14186 Huddinge, Swe- den. E-mail: [email protected]. in prostate, ovary, epididymis, testis, bladder, uterus, lung, * Supported by the Swedish Medical Research Council (MFR K98– thymus, colon, small intestine, vessel wall, pituitary, hypo- 04P-12596–01A), and the Loo och Hans Ostermans Stiftelse. thalamus, cerebellum, and brain cortex (4, 10–16a). Satura- † Supported in part by the European Union (EU-PL95–1223) Climate tion ligand binding experiments revealed high affinity and and Environment program. b b ‡ Supported in part by the Swedish Cancer Society and the European specific binding of 17 -estradiol (E2)byER protein, and Union (EU-PL95–1223) Climate and Environment program. ERb is able to stimulate transcription of an estrogen response 4252 ER b AND XENOESTROGENS 4253 element containing reporter gene in an E2-dependent manner plants (mycoestrogens). Chemically, the phytoestrogens can (10–13, 15). More extensive studies showed that some syn- be divided into three main classes: flavonoids (flavones, thetic estrogens and naturally occurring steroidal ligands isoflavones, flavanones and chalcones) such as genistein, have different relative affinities for ERa vs. ERb, although naringenin, and kaempferol; coumestans (such as coumes- most ligands (including various antiestrogens) bind with trol); and lignans (such as enterodiol and enterolactone). very similar affinity to both ER subtypes (15). Mycoestrogens are mainly zearalenone (resorcylic acid lac- There is increasing concern over the putative effects of tone) or derivatives thereof, which have been associated with various chemicals released into the environment on the re- estrogenizing syndromes in cattle fed with mold-infected production of humans and other species. Threats to the re- grain (1). Phytoestrogens and mycoestrogens act as weak productive capabilities of birds, fish, and reptiles have be- mitogens for breast tumor cells in vitro, compete with 17b- come evident and similar effects in humans have been estradiol for binding to ERa protein, and induce activity of proposed (17–21). In the past 50 yr, the incidence of testicular estrogen-responsive reporter gene constructs in the presence cancer and developmental male reproductive tract abnor- of ERa protein (36–38). Intake of phytoestrogens is signifi- malities appear to have increased in some developed coun- cantly higher in countries where the incidence of breast and tries (19). Several reports have also provided evidence for a prostate cancers is low, suggesting that they may act as decline in semen quality and/or sperm count over the same chemopreventive agents (39). The chemopreventive effect of period, although this change may not be universal (19 and dietary soy, which is rich in phytoestrogens, has been dem- references therein). Male offspring born to mothers who onstrated on the development of chemically or irradiation- were given diethylstilbestrol (DES), a very potent synthetic induced mammary tumors in mice (39 and references there- estrogen, to prevent miscarriages have an increased inci- in), and as a delayed development of dysplastic changes in dence of undescended testes, urogenital tract abnormalities, the prostate of neonatally estrogenized mice (40). The ex- and reduced semen quality compared with those from moth- pression of ERb in rat, mouse, and human prostate might be ers who did not take DES (22 and references therein). In mice of importance in this regard. Phytoestrogens are believed to injected with DES between days 9 and 16 of gestation, there exert their chemopreventive action by interacting with es- is an increased risk of intraabdominal testes, sterility, and trogen receptors, although alternative mechanisms, most no- abnormalities in the urogenital tract of the offspring (22 and tably inhibition of protein tyrosine kinase activity, have been references therein). The similarities between the observations proposed (39, 41). made in DES offspring and the abnormalities being observed In the present study, we have evaluated the estrogenic in the general population have led to the hypothesis that one activity of suspected environmental estrogens and phy- potential cause of the rise in male reproductive tract abnor- toestrogens in competition binding
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