A nongenomic action of 17β-estradiol as the mechanism underlying the acute suppression of secretion of luteinizing hormone

Biology of Reproduction

Volumn 73, Issue 1, 2005, Pages 115-122

  Arreguin Arevalo, J Alejandro ^a   Nett, Terry M ^a,b  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b Animal Reproduction and Biotechnology Laboratory   (United States)

Author keywords

Anterior pituitary; Estradiol; Estradiol receptor; Gonadotropin releasing hormone; Luteinizing hormone

Indexed keywords

BOVINE SERUM ALBUMIN; CONJUGATED ESTROGEN; CONJUGATED ESTROGEN PLUS BOVINE SERUM ALBUMIN; CONJUGATED ESTROGEN PLUS SERYLGLYCYLGLYCYLGLUTAMYLVALYLVALYLVALYLASPARTYLGLUTAMINYLPROLYLMETHIONYLGLUTAMYLARGINYLLEUCYLTYROSINE; DIARYLPROPIONITRILE; ESTRADIOL; ESTRADIOL RECEPTOR; FULVESTRANT; GONADORELIN; HORMONE RECEPTOR STIMULATING AGENT; HYDROXYTAMOXIFEN; LUTEINIZING HORMONE; PEPTIDE; PROPYLPYRAZOLETRIOL; PROTEIN ESTRADIOL RECEPTOR ALPHA; PROTEIN ESTRADIOL RECEPTOR BETA; SERYLGLYCYLGLYCYLGLUTAMYLVALYLVALYLVALYLASPARTYLGLUTAMINYLPROLYLMETHIONYLGLUTAMYLARGINYLLEUCYLTYROSINE; TAMOXIFEN; UNCLASSIFIED DRUG; DRUG DERIVATIVE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HORMONE ANTAGONIST; NITRILE; PROPIONIC ACID DERIVATIVE; PROPYL PYRAZOLE TRIOL; PYRAZOLE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MEMBRANE; CONTROLLED STUDY; HORMONE INHIBITION; HORMONE RELEASE; HYPOPHYSIS CELL; INCUBATION TIME; NONHUMAN; PRIORITY JOURNAL; SHEEP; ADENOHYPOPHYSIS; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; KINETICS; PHYSIOLOGY; SECRETION;

OVIS;

ANIMALS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GONADOTROPIN-RELEASING HORMONE; HORMONE ANTAGONISTS; KINETICS; LUTEINIZING HORMONE; NITRILES; PITUITARY GLAND, ANTERIOR; PROPIONATES; PYRAZOLES; SECRETORY RATE; SHEEP; TAMOXIFEN;

EID: 20844443502     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.105.040329     Document Type: Article

References (82)

1. Clarke IJ, Cummins JT. Direct pituitary effects of estrogen and progesterone on gonadotropin secretion in the ovariectomized ewes. Neuroendocrinology 1984; 39:267-274.
2. Gregg DW, Nett TM. Direct effects of estradiol-17 beta on the number of gonadotropin-releasing hormone receptors in the ovine pituitary. Biol Reprod 1989; 40:288-293.
3. Gregg DW, Allen MC, Nett TM. Estradiol-induced increase in number of gonadotropin-releasing hormone receptors in cultured ovine pituitary cells. Biol Reprod 1990; 43:1032-1036.
4. Evans NP, Dahl GE, Glover BH, Karsch FJ. Central regulation of pulsatile gonadotropin-releasing hormone (GnRH) secretion by estradiol during the period leading up to the preovulatory GnRH surge in the ewe. Endocrinology 1994; 134:1806-1811.
5. Nett TM, Crowder ME, Wise ME. Role of estradiol in inducing an ovulatory-like surge of luteinizing hormone in sheep. Biol Reprod 1984; 30:1208-1215.
6. Clarke IJ, Cummins JT, Crowder ME, Net TM. Pituitary receptors for gonadotropin-releasing hormone in relation to changes in pituitary and plasma gonadotropins in ovariectomized hypothalamo/pituitary-disconnected ewes. II. A marked rise in receptor number during the acute feedback effects of estradiol. Biol Reprod 1988; 39:349-354.
7. Mercer JE, Phillips DJ, Clarke IJ. Short-term regulation of gonadotropin subunit mRNA levels by estrogen: studies in the hypothalamopituitary intact and hypothalamo-pituitary disconnected ewe. J Neuroendocrinol 1993; 5:591-596.
8. Razandi M, Pedram A, Greene GL, Levin ER. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERα and ERβ expressed in Chinese hamster ovary cells. Mol Endocrinol 1999; 13:307-319.
9. Razandi M, Pedram A. Levin ER. Estrogen signal to the preservation of endothelial cell form and function. J Biol Chem 2000; 275:38540-38546.
10. Hisamoto K, Ohmichi M, Kurachi H, Hayakawa J, Kanda Y, Nishio Y, Adachi K, Tasaka K, Miyoshi E, Fujiwara N, Taniguchi N, Murata Y. Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 2001; 276: 3459-3467.
11. Wade CB, Robinson S, Shapiro RA, Dorsa DM. Estrogen receptor (ER) α and ERβ exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway. Endocrinology 2001; 142:2336-2342.
12. 2 effects on p42/044 MAPK, activation protein-1, and cAMP response element-binding protein in rat white adipocytes. Endocrinology 2002; 143:930-940.
13. Chen DB, Bird IM, Zheng J, Magness RR. Membrane estrogen receptor-dependent extracellular signal-regulated kinase pathway mediates acute activation of endothelial nitric oxide synthase by estrogen in uterine artery endothelial cells. Endocrinology 2004; 145:113-125.
14. Wong JK, Le HH, Zsarnovszky A, Belcher SM. Estrogen and ICI 182,780 (Fasoldex) modulate mitosis and cell death in immature cerebral neurons via rapid activation of p44/p42 mitogen-activated protein kinase. J Neurosci 2003; 23:4984-4995.
15. Levin ER. Genome and hormones: gender differences in physiology. Invited review: cell localization, physiology, and nongenomic actions of estrogen receptors. J Appl Physiol 2001; 91:1860-1867.
16. Simoncini T, Genazzani AR. Nongenomic actions of sex steroid hormones. Eur J Endocrinol 2003; 148:281-292.
17. Lösel RM, Falkenstein E, Feuring M, Schultz A, Tillmann H-C, Rossol-Haseroth K, Wehling M. Nongenomic steroid actions: controversies, questions, and answers. Physiol Rev 2003; 83:965-1016.
18. Kim HP, Lee JY, Jeong JK. Nongenomic stimulation of nitric oxide release by estrogen is mediated by estrogen receptor a localized in caveolae. Biochem Biophys Res Commun 1999; 263:257-262.
19. Chambliss KL, Yuhanna IS, Anderson RG, Mendelsohn ME, Shaul PW. Estrogen receptor α and endothelial nitric oxide synthase are organized into a functional signaling molecule in caveolae. Circ Res 2000; 87:E44-E52.
20. Chambliss KL, Yuhanna IS, Mineo C, Liu P, German Z, Sherman TS, Mendelsohn ME, Anderson RG, Shaul PW. Estrogen receptor β has nongenomic actions in caveolae. Endocrinology 2002; 16:938-946.
21. Razandi M, Alton G, Pedram A, Ghonshani S, Webb P, Levin ER. Identification of a structural determinant necessary for the localization and functions of estrogen receptor α at the plasma membrane. Mol Cell Biol 2003; 23:1633-1646.
22. Clarke R, Van Der Berg HW, Murphy RF. Reduction of the membrane fluidity of human breast cancer cells by tamoxifen and 17β-estradiol. J Natl Cancer Inst 1990: 82:1702-1705.
23. Luconi M, Muratori M, Forti G, Baldi E. Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. J Clin Endocrinol Metab 1999; 84:1670-1678.
24. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B. Non-genomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor α and β. Proc Natl Acad Sci U S A 2000; 97:11603-11608.
25. Toran-Allerand CD, Guan X, MacLusky NJ, Horvath TL, Diano S, Singh M, Connolly ES, Nethrapalli IS, Tinnikov AA. ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci 2002; 22:8391-8401.
26. 2 dopamine-receptor activation of a potassium channel in rat lactotrophs. J Physiol 1993; 462:563-578.
27. Guo Z, Krucken J, Benten WPM, Wunderlich F. Estradiol-induced nongenomic calcium signaling regulates genotropic signaling in macrophages. J Biol Chem 2002; 277:7044-7050.
28. Korovkina VP, Brainard AM, Ismail P, Schmidt TJ, England SK. Estradiol binding to Maxi-K channels induces their downregulation via proteosomal degradation. J Biol Chem 2004; 279:1217-1223.
29. Rosner W, Hryb DJ, Khan MS, Nakhla AM, Romas NA. Sex hormone-binding globulin. Binding to cell membranes and generation of a second messenger. J Androl 1992; 13:101-106.
30. Nakhla AM, Romas NA, Rosner W. Estradiol activates the prostate androgen receptor and prostate-specific antigen secretion through the intermediacy of sex hormone-binding globulin. J Biol Chem 1997; 272:6838-6841.
31. Delbès G, Levacher C, Pairault C, Racine C, Duquenne C, Krust A, Habert R. Estrogen receptor β-mediated inhibition of male germ cell line development in mice by endogenous estrogen during perinatal life. Endocrinology 2004; 145:3395-3403.
32. Stossi F, Barnett DH, Frasor J, Komm B, Lyttle CR, Katzenellenbogen BS. Transcriptional profiling of estrogen-regulated gene expression via estrogen receptors (ER) α or ERβ in human osteosarcoma cells: distinct and common target genes for these receptors. Endocrinology 2004; 145:3473-3486.
33. Abraham IM, Todman MG, Korach KS, Herbison AE. Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain. Endocrinology 2004; 145:3055-3061.
34. Kudwa AE, Gustafsson JA, Rissman EF. Estrogen receptor β modulates estradiol induction of progestin receptor immunoreactivity in male, but not in female, mouse medial preoptic area. Endocrinology 2004; 145:4500-4506.
35. Katzenellenbogen BS, Katzenellenbogen JA. Estrogen-receptor transcription and transactivation of estrogen receptor alpha and estrogen receptor β: regulation by selective estrogen receptor modulators and importance in breast cancer. Rev Breast Cancer Res 2000; 2:335-344.
36. Kuiper GGJM, Carlsson B, Grandien K, Enmark E, Häggblad J, Nilsson S, Gustafsson J-A. Comparison of the ligand-binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 1997; 138:863-870.
37. Barkhem T, Carlsson BO, Nilsson Y, Enmark E, Gustafsson J-A, Nilsson S. Differential response of estrogen receptor α and estrogen receptor β to partial estrogen agonists/antagonists. Mol Pharmacol 1998; 54:105-112.
38. Hayashi T, Yamada K, Esaki T, Kuzuya M, Satake S, Ishikawa T, Hidaka H, Iguchi A. Estrogen increases endothelial nitric oxide by a receptor-mediated system. Biochem Biophys Res Commun 1995; 81: 355-362.
39. Labrie F, Labrie C, Belanger A, Giguere V, Simard J, Merand Y, Gauthier S, Luu-The V, Candas B, Martel C, Luo S. Pure selective estrogen-receptor modulators, new molecules having absolute cell specificity ranging from pure antiestrogenic to complete estrogen-like activities. Adv Protein Chem 2001; 56:293-368.
40. Fritzpatrick SL, Berrodin TJ, Jenkins SF, Sindoni DM, Deecher DC, Frail DE. Effect of estrogen agonist and antagonist on induction of progesterone receptor in a rat hypothalamic cell line. Endocrinology 1999; 140:3928-3937.
41. Pedram A, Razandi M, Aitkenhead M, Hughest CCW, Levin ER. Integration of the nongenomic and genomic actions of estrogen. J Biol Chem 2002; 277:50768-50775.
42. Chen Z, Yuhanna IS, Galcheva-Gargova Z, Karas RH, Mendelsohn ME, Shaul PW. Estrogen receptor α mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Endocrinol Metab 1999; 103:401-406.
43. Prevot V, Croix D, Rialas CM, Poulain P, Fricchione GL, Stefano GB, Beauvillain J-C. Estradiol coupling to endothelial nitric oxide stimulates gonadotropin-releasing hormone release from rat median eminence via a membrane receptor. Endocrinology 1999; 140:652-659.
44. Russell KS, Haynes MP, Sinha D, Clerisme E, Bender JR. Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci U S A 2000; 97:5930-5935.
45. Watters JJ, Campbell JS, Cunningham MJ, Krebs EG, Dorsa DM. Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signaling cascade and c-fos immediate early gene transcription. Endocrinology 1997; 138: 4030-4033.
46. Razandi M, Pedram A, Levin ER. Plasma membrane estrogen-receptor signaling to antiapoptosis in breast cancer. Mol Endocrinol 2000; 14:1434-1447.
47. Sun J, Meyers J, Fink BF, Rajendran R, Katzenellenbogen JA, Katzenellenbogen BS. Novel ligands that function as selective estrogens or antiestrogens for estrogen receptor-α or estrogen receptor-β. Endocrinology 1999; 140:800-804.
48. Stauffer SR, Coletta CJ, Tedesco R, Nishiguchi G, Carlson K, Sun J, Katzenellenbogen BS, Katzenellenbogen JA. Pyrazole ligands structure-afunity/ activity relationships and estrogen receptor-α-selective agonists. J Med Chem 2000; 43:4934-4947.
49. Kraichely DM, Sun J, Katzenellenbogen JA, Katzenellenbogen BS. Conformational changes and coactivator recruitment by novel ligands for estrogen receptor-α and estrogen receptor-β: correlations with biological character and distinct differences among SRC coactivator family members. Endocrinology 2000; 141:3534-3545.
50. Meyers MJ, Sun J, Carlson K, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA. Estrogen receptor-β potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 2001; 44:4230-4251.
51. Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenellenbogen JA, Katzenellenbogen BS. Activities of estrogen receptor α- and β-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol 2003; 206:13-22.
52. Zheng J, Ali A, Ramirez VD. Steroids conjugated to bovine serum albumin as tools to demonstrate specific steroid neural membrane binding sites. J Psychiatry Neurosci 1996; 21:187-197.
53. 125I] bovine serum albumin conjugate. J Steroid Biochem Biol 1997; 62:327-336.
54. Caldwell JD, Walker CH, Rivkina A, Pedersen CA, Mason GA. Radioligand assays for estradiol and progesterone conjugated to protein reveal evidence for a common membrane-binding site in the median preoptic area-anterior hypothalamus and differential modulation by cholera toxin and GTPγS. J Neuroendocrinol 1999; 11:409-417.
55. Erlanger BF, Borek F, Beiser SM, Lieberman S. Steroid-protein conjugates. I. Preparation and characterization of conjugates of bovine serum albumin with testosterone and with cortisone. J Biol Chem 1959; 228:713-727.
56. Korenman SG, Stevens RH, Carpenter LA, Robb M, Niswender GD, Sherman BM. Estradiol radioimmunoassay without chromatography: procedure, validation and normal values. J Clin Endocrinol Metab 1974; 38:718-720.
57. Adams TE, Wagner TO, Sawyer HR, Nett TM. GnRH interaction with anterior pituitary. II. Cyclic AMP as an intracellular mediator in the GnRH-activated gonadotroph. Biol Reprod 1979; 21:735-747.
58. Niswender GD, Reichert LE Jr, Midgley AR Jr, Nalbandov AV. Radioimmunoassay for bovine and ovine luteinizing hormone. Endocrinology 1969; 84:1166-1173.
59. Niswender GD, Akbar AM, Nett TM. Use of specific antibodies for quantification of steroid hormones. Methods Enzymol 1975; 36:16-34.
60. SAS. SAS User's Guide, Statistics. Cary, NC: Statistical Analysis System Institute, Inc.; 1987.
61. Gaetjens E, Pertschuk LP. Synthesis of fluorescein-labeled steroid hormone-albumin conjugates for the fluorescent histochemical detection of hormone receptors. J Steroid Biochem 1980; 13:214-216.
62. Pappas TC, Gametchu B, Yannariello Brown J, Collins TJ. Watson CS. Membrane estrogen receptors in GH3/B6 cells are associated with rapid estrogen-induced release of prolactin. Endocrine 1994; 2:813-822.
63. Norfleet AM, Clarke CH, Gametchu B, Watson CS. Antibodies to the estrogen receptor-α modulate rapid prolactin release from rat pituitary tumor cells through plasma membrane estrogen receptors. FASEB J 2000; 14:157-165.
64. Kon T. Destruction and restoration of the insulin effector system of isolated fat cells. J Biol Chem 1969: 244:5777-5784.
65. Amsterdam A, Jamieson JD. Studies on dispersed pancreatic exocrine cells. II. Functional characteristics of separated cells. J Cell Biol 1974; 63:1057-1 173.
66. Goetz RM, Thatte HS, Prabhakar P, Cho MR, Michel T, Golan DE. Estradiol induces the calcium-dependent translocation of endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 1999; 96:2788-2793.
67. Watters JJ, Chun TY, Kim YN, Bertics PJ, Gorski J. Estrogen modulation of prolactin gene expression requires an intact mitogen-activated protein kinase signal transduction pathway in culture rat pituitary cells. Mol Endocrinol 2000; 14:1872-1881.
68. Singer CA, Rogers KL, Strickland TM, Dorsal DM. Estrogen protects primary cortical neurons from glutamate neurotoxicity. Neurosci Lett 1996; 9:2565-2568.
69. Aronica SM, Kraus WL, Katzenellenbogen BS. Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc Natl Acad Sci U S A 1994; 91:8517-8521.
70. Bourassa PA, Milos PM, Gaynor BJ, Breslow JL, Aiello RL. Estrogen reduces atherosclerotic lesion development in apolipoprotein E-deficient mice. Proc Natl Acad Sci U S A 1996; 93:10022-10027.
71. Hisamoto K, Ohmichi M, Kurachi H, Hayakawa J, Kanda Y, Nishio Y, Adachi K, Tasaka K, Miyoshi E, Fujiwara N, Taniguchi N, Murata Y. Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 2001; 276: 3459-3467.
72. Simoncini T, Genazzani AR. Raloxifene acutely stimulates nitric oxide release from human endothelial cells via an activation of endothelial nitric oxide synthase. J Clin Endocrinol Metab 2000; 85:2966-2969.
73. ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J 1996; 15:1292-1300.
74. Singer CA, Figueroa-Masot A, Batchelor RH, Dorsal DM. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci 1999; 19:2455-2463.
75. Razandi M, Pedram A, Park ST, Levin ER. Proximal events in signaling by plasma membrane estrogen receptors. J Biol Chem 2003; 278:2701-2712.
76. Song RXD, McPherson RA, Adam L, Bao Y, Shupnik M, Kumar R, Santen RJ. Linkage of rapid estrogen action to MAPK activation by ERα-Shc association and Shc pathway activation. Mol Endocrinol 2002; 16:116-127.
77. Mize AL, Shapiro RA, Dorsa DM. Estrogen receptor-mediated neuroprotection from oxidative stress requires activation of the mitogen-activated kinase pathway. Endocrinology 2003; 144:306-312.
78. Wade CB, Dorsa DM. Estrogen activation of cyclic adenosine 5′-monophosphate response element-mediated transcription requires the extracellularly regulated kinase/mitogen-activated protein kinase pathway. Endocrinology 2003; 144:832-838.
79. Gu Q, Korach KS, Moss RL. Rapid action of 17β-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology 1999; 140:660-666.
80. Singh M, Setalo G Jr. Guan X, Frail DE, Toran-Allerand CD. Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-α-knock-out mice. J Neurosci 2000; 20:1694-1700.
81. Watters JJ, Dorsa DM. Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms. J Neurosci 1998; 18:6672-6680.
82. Montgomery S, Shawn L, Pantetides N, Taggart M, Austin C. Acute effects of estrogen receptor subtype-specific agonists on vascular contractility. Br J Pharmacol 2003; 139:1249-1253.