Activation of transgenic estrogen receptor-beta by selected phytoestrogens in a stably transduced rat serotonergic cell line

Journal of Steroid Biochemistry and Molecular Biology

Volumn 120, Issue 4-5, 2010, Pages 208-217

  Amer, Dena A M ^a   Kretzschmar, Georg ^a   Müller, Nicole ^a   Stanke, Nicole ^b   Lindemann, Dirk ^b   Vollmer, Günter ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

17beta estradiol; Estrogen receptor beta; Isoflavones; Naringenin type flavanones; Raphe nuclei; RN46A B14 cells; RNDA cells

Indexed keywords

6 (1,1 DIMETHYLALLYL)NARINGENIN; 7 (O PRENYL)NARINGENIN 4' ACETATE; 8 PRENYLNARINGENIN; DAIDZEIN; EQUOL; ESTRADIOL; ESTROGEN RECEPTOR BETA; FULVESTRANT; GENISTEIN; LENTIVIRUS VECTOR; NARINGENIN; PHYTOESTROGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ESTROGEN ACTIVITY; MOOD; NONHUMAN; RAPHE NUCLEUS; RAT; SEROTONINERGIC NERVE CELL;

ANIMALS; CELL LINE; CLONING, MOLECULAR; ESTROGEN RECEPTOR BETA; FLAVANONES; GENES, REPORTER; HUMANS; PHYTOESTROGENS; RAPHE NUCLEI; RATS; TRANSDUCTION, GENETIC; TRANSGENES;

RATTUS;

EID: 77953614562     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2010.04.018     Document Type: Article

References (76)

1. Jover T., Tanaka H., Calderone A., Oguro K., Bennett M.V., Etgen A.M., Zukin R.S. Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. J. Neurosci. 2002, 22(6):2115-2124.
2. Rincavage H.L., McDonnell D.P., Kuhn C.M. Expression of functional estrogen receptor beta in locus coeruleus-derived Cath.a cells. Endocrinology 2003, 144(7):2829-2835.
3. Joels M. Steroid hormones and excitability in the mammalian brain. Front Neuroendocrinol. 1997, 18(1):2-48.
4. Wickelgren I. Estrogen stakes claim to cognition. Science 1997, 276(5313):675-678.
5. Bramlett H.M., Dietrich W.D. Neuropathological protection after traumatic brain injury in intact female rats versus males or ovariectomized females. J. Neurotrauma. 2001, 18(9):891-900.
6. Aguado-Llera D., Arilla-Ferreiro E., Chowen J.A., Argente J., Puebla-Jimenez L., Frago L.M., Barrios V. 17Beta-estradiol protects depletion of rat temporal cortex somatostatinergic system by beta-amyloid. Neurobiol. Aging 2007, 28(9):1396-1409.
7. Chen J., Lei T., Ritz M.F., Mendelowitsch A. Effect of 17 beta-estradiol on the brain damage and metabolic changes in rats. J. Tongji Med. Univ. 2001, 21(1). pp. 62-4, 74.
8. Honda K., Sawada H., Kihara T., Urushitani M., Nakamizo T., Akaike A., Shimohama S. Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J. Neurosci. Res. 2000, 60(3):321-327.
9. Callier S., Morissette M., Grandbois M., Pelaprat D., Di Paolo T. Neuroprotective properties of 17beta-estradiol, progesterone, and raloxifene in MPTP C57Bl/6 mice. Synapse 2001, 41(2):131-138.
10. Chen S., Nilsen J., Brinton R.D. Dose and temporal pattern of estrogen exposure determines neuroprotective outcome in hippocampal neurons: therapeutic implications. Endocrinology 2006, 147(11):5303-5313.
11. Beato M., Sanchez-Pacheco A. Interaction of steroid hormone receptors with the transcription initiation complex. Endocr. Rev. 1996, 17(6):587-609.
12. Koldzic-Zivanovic N., Seitz P.K., Watson C.S., Cunningham K.A., Thomas M.L. Intracellular signaling involved in estrogen regulation of serotonin reuptake. Mol. Cell Endocrinol. 2004, 226(1-2):33-42.
13. Kurata K., Takebayashi M., Kagaya A., Morinobu S., Yamawaki S. Effect of beta-estradiol on voltage-gated Ca(2+) channels in rat hippocampal neurons: a comparison with dehydroepiandrosterone. Eur. J. Pharmacol. 2001, 416(3):203-212.
14. Kelly M.J., Lagrange A.H., Wagner E.J., Ronnekleiv O.K. Rapid effects of estrogen to modulate G protein-coupled receptors via activation of protein kinase A and protein kinase C pathways. Steroids 1999, 64(1-2):64-75.
15. Bulayeva N.N., Gametchu B., Watson C.S. Quantitative measurement of estrogen-induced ERK 1 and 2 activation via multiple membrane-initiated signaling pathways. Steroids 2004, 69(3):181-192.
16. Shughrue P.J., Komm B., Merchenthaler I. The distribution of estrogen receptor-beta mRNA in the rat hypothalamus. Steroids 1996, 61(12):678-681.
17. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 1997, 388(4):507-525.
18. Henderson V.W., Paganini-Hill A., Emanuel C.K., Dunn M.E., Buckwalter J.G. Estrogen replacement therapy in older women. Comparisons between Alzheimer's disease cases and nondemented control subjects. Arch. Neurol. 1994, 51(9):896-900.
19. Sullivan J.M., El-Zeky F., Vander Zwaag R., Ramanathan K.B. Effect on survival of estrogen replacement therapy after coronary artery bypass grafting. Am. J. Cardiol. 1997, 79(7):847-850.
20. Torgerson D.J., Bell-Syer S.E. Hormone replacement therapy and prevention of nonvertebral fractures: a meta-analysis of randomized trials. JAMA 2001, 285(22):2891-2897.
21. Burger C.W., van Leeuwen F.E., Scheele F., Kenemans P. Hormone replacement therapy in women treated for gynaecological malignancy. Maturitas 1999, 32(2):69-76.
22. Pike M.C., Ross R.K. Progestins and menopause: epidemiological studies of risks of endometrial and breast cancer. Steroids 2000, 65(10-11):659-664.
23. Brown N.M., Setchell K.D. Animal models impacted by phytoestrogens in commercial chow: implications for pathways influenced by hormones. Lab Invest. 2001, 81(5):735-747.
24. Singleton D.W., Khan S.A. Xenoestrogen exposure and mechanisms of endocrine disruption. Front Biosci. 2003, 8:s110-s118.
25. Zierau O., Kretzschmar G., Moller F., Weigt C., Vollmer G. Time dependency of uterine effects of naringenin type phytoestrogens in vivo. Mol. Cell Endocrinol. 2008, 294(1-2):92-99.
26. Ren M.Q., Kuhn G., Wegner J., Chen J. Isoflavones, substances with multi-biological and clinical properties. Eur. J. Nutr. 2001, 40(4):135-146.
27. Rice S., Whitehead S.A. Phytoestrogens oestrogen synthesis and breast cancer. J. Steroid Biochem. Mol. Biol. 2008, 108(3-5):186-195.
28. Moller F.J., Zierau O., Hertrampf T., Bliedtner A., Diel P., Vollmer G. Long-term effects of dietary isoflavones on uterine gene expression profiles. J. Steroid Biochem. Mol. Biol. 2009, 113(3-5):296-303.
29. Markiewicz L., Garey J., Adlercreutz H., Gurpide E. In vitro bioassays of non-steroidal phytoestrogens. J Steroid Biochem. Mol. Biol. 1993, 45(5):399-405.
30. Morito K., Hirose T., Kinjo J., Hirakawa T., Okawa M., Nohara T., Ogawa S., Inoue S., Muramatsu M., Masamune Y. Interaction of phytoestrogens with estrogen receptors alpha and beta. Biol. Pharm. Bull. 2001, 24(4):351-356.
31. Schmitt E., Dekant W., Stopper H. Assaying the estrogenicity of phytoestrogens in cells of different estrogen sensitive tissues. Toxicol. In Vitro 2001, 15(4-5):433-439.
32. Gester S., Metz P., Zierau O., Vollmer G. An efficient synthesis of the potent phytoestrogens 8-prenylnaringenin and 6-(1,1-dimethylallyl)naringenin by europium(iii)-catalyzed claisen rearrangement. Tetrahedron 2001, 57:1015-1018.
33. Kretzschmar G., Vollmer G., Schwab P., Tischer S., Metz P., Zierau O. Effects of the chemically synthesized flavanone 7-(O-prenyl)naringenin-4'-acetate on the estrogen signaling pathway in vivo and in vitro. J. Steroid Biochem. Mol. Biol. 2007, 107(1-2):114-119.
34. Seo E.K., Silva G.L., Chai H.B., Chagwedera T.E., Farnsworth N.R., Cordell G.A., Pezzuto J.M., Kinghorn A.D. Cytotoxic prenylated flavanones from Monotes engleri. Phytochemistry 1997, 45(3):509-515.
35. Tokalov S.V., Henker Y., Schwab P., Metz P., Gutzeit H.O. Toxicity and cell cycle effects of synthetic 8-prenylnaringenin and derivatives in human cells. Pharmacology 2004, 71(1):46-56.
36. Donner N., Handa R.J. Estrogen receptor beta regulates the expression of tryptophan-hydroxylase 2 mRNA within serotonergic neurons of the rat dorsal raphe nuclei. Neuroscience 2009.
37. Moller F., Zierau O., Jandausch A., Rettenberger R., Kaszkin-Bettag M., Vollmer G. Subtype-specific activation of estrogen receptors by a special extract of Rheum rhaponticum (ERr 731), its aglycones and structurally related compounds in U2OS human osteosarcoma cells. Phytomedicine 2007, 14(11):716-726.
38. Wober J., Moller F., Richter T., Unger C., Weigt C., Jandausch A., Zierau O., Rettenberger R., Kaszkin-Bettag M., Vollmer G. Activation of estrogen receptor-beta by a special extract of Rheum rhaponticum (ERr 731), its aglycones and structurally related compounds. J. Steroid Biochem. Mol. Biol. 2007, 107(3-5):191-201.
39. White L.A., Eaton M.J., Castro M.C., Klose K.J., Globus M.Y., Shaw G., Whittemore S.R. Distinct regulatory pathways control neurofilament expression and neurotransmitter synthesis in immortalized serotonergic neurons. J. Neurosci. 1994, 14(11 Pt 1):6744-6753.
40. Eaton M.J., Whittemore S.R. Autocrine BDNF secretion enhances the survival and serotonergic differentiation of raphe neuronal precursor cells grafted into the adult rat CNS. Exp. Neurol. 1996, 140(2):105-114.
41. Bethea C.L., Lu N.Z., Reddy A., Shlaes T., Streicher J.M., Whittemore S.R. Characterization of reproductive steroid receptors and response to estrogen in a rat serotonergic cell line. J. Neurosci. Methods 2003, 127(1):31-41.
42. DuBridge R.B., Tang P., Hsia H.C., Leong P.M., Miller J.H., Calos M.P. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell Biol. 1987, 7(1):379-387.
43. Rasheed S., Nelson-Rees W.A., Toth E.M., Arnstein P., Gardner M.B. Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 1974, 33(4):1027-1033.
44. Greene L.A., Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. U.S.A. 1976, 73(7):2424-2428.
45. Mochizuki H., Schwartz J.P., Tanaka K., Brady R.O., Reiser J. High-titer human immunodeficiency virus type 1-based vector systems for gene delivery into nondividing cells. J. Virol. 1998, 72(11):8873-8883.
46. Wakeling A.E., Bowler J. Steroidal pure antioestrogens. J. Endocrinol. 1987, 112(3):R7-10.
47. Wakeling A.E., Bowler J. ICI 182, 780, a new antioestrogen with clinical potential. J. Steroid Biochem. Mol. Biol. 1992, 43(1-3):173-177.
48. Nomura M., Akama K.T., Alves S.E., Korach K.S., Gustafsson J.A., Pfaff D.W., Ogawa S. Differential distribution of estrogen receptor (ER)-alpha and ER-beta in the midbrain raphe nuclei and periaqueductal gray in male mouse: predominant role of ER-beta in midbrain serotonergic systems. Neuroscience 2005, 130(2):445-456.
49. Beral V., Banks E., Reeves G. Evidence from randomised trials on the long-term effects of hormone replacement therapy. Lancet 2002, 360(9337):942-944.
50. Cos P., De Bruyne T., Apers S., Vanden Berghe D., Pieters L., Vlietinck A.J. Phytoestrogens: recent developments. Planta Med. 2003, 69(7):589-599.
51. Ososki A.L., Kennelly E.J. Phytoestrogens: a review of the present state of research. Phytother. Res. 2003, 17(8):845-869.
52. Hrabovszky E., Kallo I., Hajszan T., Shughrue P.J., Merchenthaler I., Liposits Z. Expression of estrogen receptor-beta messenger ribonucleic acid in oxytocin and vasopressin neurons of the rat supraoptic and paraventricular nuclei. Endocrinology 1998, 139(5):2600-2604.
53. Zierau O., Kolba S., Olff S., Vollmer G., Diel P. Analysis of the promoter-specific estrogenic potency of the phytoestrogens genistein, daidzein and coumestrol. Planta Med. 2006, 72(2):184-186.
54. Kretzschmar G., Zierau O., Wober J., Tischer S., Metz P., Vollmer G. Prenylation has a compound specific effect on the estrogenicity of naringenin and genistein. J. Steroid Biochem. Mol. Biol. 2009.
55. Caldarelli A., Diel P., Vollmer G. Effect of phytoestrogens on gene expression of carbonic anhydrase II in rat uterus and liver. J. Steroid Biochem. Mol. Biol. 2005, 97(3):251-256.
56. Hertrampf T., Ledwig C., Kulling S., Molzberger A., Moller F.J., Zierau O., Vollmer G., Moors S., Degen G.H., Diel P. Responses of estrogen sensitive tissues in female Wistar rats to pre- and postnatal isoflavone exposure. Toxicol. Lett. 2009, 191(2-3):181-188.
57. Schmidt S., Degen G.H., Seibel J., Hertrampf T., Vollmer G., Diel P. Hormonal activity of combinations of genistein, bisphenol A and 17beta-estradiol in the female Wistar rat. Arch. Toxicol. 2006, 80(12):839-845.
58. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der Burg B., Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139(10):4252-4263.
59. Routledge E.J., White R., Parker M.G., Sumpter J.P. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J. Biol. Chem. 2000, 275(46):35986-35993.
60. Legler J., van den Brink C.E., Brouwer A., Murk A.J., van der Saag P.T., Vethaak A.D., van der Burg B. Development of a stably transfected estrogen receptor-mediated luciferase reporter gene assay in the human T47D breast cancer cell line. Toxicol. Sci. 1999, 48(1):55-66.
61. Meerts I.A., Letcher R.J., Hoving S., Marsh G., Bergman A., Lemmen J.G., van der Burg B., Brouwer A. In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PDBEs, and polybrominated bisphenol A compounds. Environ. Health Perspect. 2001, 109(4):399-407.
62. Rivas A., Lacroix M., Olea-Serrano F., Laios I., Leclercq G., Olea N. Estrogenic effect of a series of bisphenol analogues on gene and protein expression in MCF-7 breast cancer cells. J. Steroid Biochem. Mol. Biol. 2002, 82(1):45-53.
63. Choi S.Y., Ha T.Y., Ahn J.Y., Kim S.R., Kang K.S., Hwang I.K., Kim S. Estrogenic activities of isoflavones and flavones and their structure-activity relationships. Planta Med. 2008, 74(1):25-32.
64. Ruh M.F., Zacharewski T., Connor K., Howell J., Chen I., Safe S. Naringenin: a weakly estrogenic bioflavonoid that exhibits antiestrogenic activity. Biochem. Pharmacol. 1995, 50(9):1485-1493.
65. Zierau O., Gester S., Schwab P., Metz P., Kolba S., Wulf M., Vollmer G. Estrogenic activity of the phytoestrogens naringenin, 6-(1,1-dimethylallyl)naringenin and 8-prenylnaringenin. Planta Med. 2002, 68(5):449-451.
66. Zierau O., Morrissey C., Watson R.W., Schwab P., Kolba S., Metz P., Vollmer G. Antiandrogenic activity of the phytoestrogens naringenin, 6-(1,1-dimethylallyl)naringenin and 8-prenylnaringenin. Planta Med. 2003, 69(9):856-858.
67. Zierau O., Hamann J., Tischer S., Schwab P., Metz P., Vollmer G., Gutzeit H.O., Scholz S. Naringenin-type flavonoids show different estrogenic effects in mammalian and teleost test systems. Biochem. Biophys. Res. Commun. 2005, 326(4):909-916.
68. Zand R.S., Jenkins D.J., Diamandis E.P. Steroid hormone activity of flavonoids and related compounds. Breast Cancer Res. Treat 2000, 62(1):35-49.
69. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., Gustafsson J.A. Mechanisms of estrogen action. Physiol. Rev. 2001, 81(4):1535-1565.
70. Gruber C.J., Tschugguel W., Schneeberger C., Huber J.C. Production and actions of estrogens. N. Engl. J. Med. 2002, 346(5):340-352.
71. Shang Y., Brown M. Molecular determinants for the tissue specificity of SERMs. Science 2002, 295(5564):2465-2468.
72. Paige L.A., Christensen D.J., Gron H., Norris J.D., Gottlin E.B., Padilla K.M., Chang C.Y., Ballas L.M., Hamilton P.T., McDonnell D.P., Fowlkes D.M. Estrogen receptor (ER) modulators each induce distinct conformational changes in ER alpha and ER beta. Proc. Natl. Acad. Sci. U.S.A. 1999, 96(7):3999-4004.
73. Milligan S.R., Kalita J.C., Pocock V., Van De Kauter V., Stevens J.F., Deinzer M.L., Rong H., De Keukeleire D. The endocrine activities of 8-prenylnaringenin and related hop (Humulus lupulus L.) flavonoids. J. Clin. Endocrinol. Metab. 2000, 85(12):4912-4915.
74. Effenberger K.E., Johnsen S.A., Monroe D.G., Spelsberg T.C., Westendorf J.J. Regulation of osteoblastic phenotype and gene expression by hop-derived phytoestrogens. J. Steroid Biochem. Mol. Biol. 2005, 96(5):387-399.
75. Overk C.R., Guo J., Chadwick L.R., Lantvit D.D., Minassi A., Appendino G., Chen S.N., Lankin D.C., Farnsworth N.R., Pauli G.F., van Breemen R.B., Bolton J.L. In vivo estrogenic comparisons of Trifolium pratense (red clover) Humulus lupulus (hops), and the pure compounds isoxanthohumol and 8-prenylnaringenin. Chem. Biol. Interact. 2008, 176(1):30-39.
76. Kuiper G.G., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S., Gustafsson J.A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997, 138(3):863-870.