Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-α knock-out mice

Journal of Neuroscience

Volumn 20, Issue 5, 2000, Pages 1694-1700

  Singh, Meharvan ^a   Sétáló Jr , György ^a,c   Guan, Xiaoping ^a   Frail, Donald E ^d   Toran Allerand, C Dominique ^a,b,e  

^a Dept of Obstet and Gynecol C   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

^c UNIVERSITY OF PÉCS   (Hungary)

^d WYETH AYERST RESEARCH   (United States)

^e Dept of Anatomy and Cell Biology ^*  (United States)

Author keywords

Brain; Cerebral cortex; ERK; ERKO; Estradiol; Estrogen receptor; Signal transduction

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; FULVESTRANT; GENISTEIN; MITOGEN ACTIVATED PROTEIN KINASE; RAF PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; KNOCKOUT MOUSE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 0342803689     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-05-01694.2000     Document Type: Article

References (59)

1. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262:5592-5595.
2. Anuradha P, Khan SM, Karthikeyan N, Thampan RV (1994) The non-activated estrogen receptor (naER) of the goat uterus is a tyrosine kinase. Arch Biochem Biophys 309:195-204.
3. Asaithambi A, Mukherjee S, Thakur MK (1997) Expression of 112-kDa estrogen receptor in mouse brain cortex and its autoregulation with age. Biochem Biophys Res Commun 231:683-685.
4. Behl C, Widmann M, Trapp T, Holsboer F (1995) 17-Beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun 216:473-482.
5. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, Holsboer F (1997) Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535-541.
6. Black M, Aletta J, Greene L (1986) Regulation of microtubule composition and stability during nerve growth factor-promoted neurite out-growth. J Cell Biol 103:545-557.
7. Chiaia N, Foy M, Teyler TJ (1983) The hamster hippocampal slice. II. Neuroendocrine modulation. Behav Neurosci 97:839-843.
8. Couse JF, Lindzey J, Grandien K, Gustafsson JA, Korach KS (1997) Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinology 138:4613-4621.
9. Das SK, Taylor JA, Korach KS, Paria BC, Dey SK. Lubahn DB (1997) Estrogenic responses in estrogen receptor-alpha deficient mice reveal a distinct estrogen signaling pathway. Proc Natl Acad Sci USA 94:12786-12791.
10. Desdouits-Magnen J, Desdouits F, Takeda S, Syu LJ, Saltiel AR, Buxbaum JD. Czernik AJ, Nairn AC, Greengard P (1998) Regulation of secretion of Alzheimer amyloid precursor protein by the mitogen-activated protein kinase cascade. J Neurochem 70:524-530.
11. Drubin D, Feinstein S, Shooter E, Kirschner M (1985) Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J Cell Biol 101:1799-1807.
12. Federoff HJ, Grabczyk E, Fishman MC (1988) Dual regulation of GAP-43 gene expression by nerve growth factor and glucocorticoids. J Biol Chem 263:19290-19295.
13. Ferreira A, Caceres A (1991) Estrogen-enhanced neurite growth: evidence for a selective induction of tau and stable microtubules. J Neurosci 11:392-400.
14. Fillit H, Weinreb H, Cholst I, Luine V, McEwen B, Amador R, Zabriskie J (1986) Observations in a preliminary open trial of estradiol therapy for senile dementia-Alzheimer's type. Psychoneuroendocrinology 11:337-345.
15. Garcia-Segura LM. Olmos G, Tranque P, Naftolin F (1987) Rapid effects of gonadal steroids upon hypothalamic neuronal membrane ultrastructure. J Steroid Biochem 27:615-623.
16. Ginsburg M, MacLusky NJ, Morris ID, Thomas PJ (1977) The specificity of oestrogen receptor in brain, pituitary and uterus. Br J Pharmacol 59:397-402.
17. Green PS, Gridley KE, Simpkins JW (1996) Estradiol protects against beta-amyloid (25-35)-induced toxicity in SK-N-SH human neuroblastoma cells. Neurosci Lett 218:165-168.
18. Green PS, Bishop J, Simpkins JW (1997) 17 alpha-estradiol exerts neuroprotective effects on SK-N-SH cells. J Neurosci 17:511-515.
19. Gu Q, Korach KS, Moss RL (1999) Rapid action of 17beta-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology 140:660-666.
20. Guo JZ, Gorski J (1988) Estrogen effects on histone messenger rihonucleic acid levels in the rat uterus. Mol Endocrinol 2:693-700.
21. 125I]iodoestradiol with estrogen receptor and other steroid-binding proteins. Proc Natl Acad Sci USA 77:328-332.
22. Jaffe A, Toran-Allerand CD, Greengard P, Gandy S (1994) Estrogen regulates metabolism of Alzheimer amyloid beta precursor protein. J Biol Chem 269:13065-13068.
23. Karthikeyan N, Thampan RV (1996) Plasma membrane is the primary site of localization of the nonactivated estrogen receptor in the goat uterus: hormone binding causes receptor internalization. Arch Biochem Biophys 325:47-57.
24. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 95:15677-15682.
25. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93:5925-5930.
26. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138:863-870.
27. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252-4263.
28. Lorenzo A, Diaz H, Carrer H, Caceres A (1992) Amygdala neurons in vitro: neurite growth and effects of estradiol. J Neurosci Res 33:418-435.
29. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90:11162-11166.
30. Luine VN, Richards ST, Wu VY, Beck KD (1998) Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 34:149-162.
31. Lustig R, Sudol M, Pfaff D, Federoff H (1991) Estrogenic regulation and sex dimorphism of growth-associated protein 43 kDa (GAP-43) messenger RNA in the rat. Brain Res Mol Brain Res 11:125-132.
32. Merriam GR, MacLusky NJ, Johnson LA, Naftolin F (1980) 2-hydroxyestradiol-17 alpha and 4-hydroxyestradiol-17 alpha, catechol estrogen analogs with reduced estrogen receptor affinity. Steroids 36:13-20.
33. Migliaccio A, Pagano M, Auricchio F (1993) Immediate and transient stimulation of protein tyrosine phosphorylation by estradiol in MCF-7 cells. Oncogene 8:2183-2191.
34. Mills J, Laurent Charest D, Lam F, Beyreuther K, Ida N, Pelech SL, Reiner PB (1997) Regulation of amyloid precursor protein catabolism involves the mitogen-activated protein kinase signal transduction pathway. J Neurosci 17:9415-9422.
35. Miranda R, Sohrabji F, Toran-Allerand CD (1993) Neuronal colocalization of mRNAs for neurotrophins and their receptors in the developing central nervous system suggests a potential for autocrine interactions. Proc Natl Acad Sci USA 90:6439-6443.
36. Moffatt CA, Rissman EF, Shupnik MA, Blaustein JD (1998) Induction of progestin receptors by estradiol in the forebrain of estrogen receptor-alpha gene-disrupted mice. J Neurosci 18:9556-9563.
37. Mosselman S, Polman J, Dijkema R (1996) ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 392:49-53.
38. Ogawa S, Inoue S, Watanabe T, Hiroi H, Orimo A, Hosoi T, Ouchi Y, Muramatsu M (1998) The complete primary structure of human estrogen receptor beta (hER beta) and its heterodimerization with ER alpha in vivo and in vitro. Biochem Biophys Res Commun 243:122-126.
39. Pace P, Taylor J, Suntharalingam S, Coombes RC, Ali S (1997) Human estrogen receptor beta binds DNA in a manner similar to and dimerizes with estrogen receptor alpha. J Biol Chem 272:25832-25838.
40. Paganini-Hill A, Henderson VW (1994) Estrogen deficiency and risk of Alzheimer's disease in women. Am J Epidemiol 140:256-261.
41. Pappas TC, Gametchu B, Watson CS (1995) Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding. FASEB J 9:404-410.
42. Pettersson K, Grandien K, Kuiper GG, Gustafsson JA (1997) Mouse estrogen receptor beta forms estrogen response element-binding heterodimers with estrogen receptor alpha. Mol Endocrinol 11:1486-1496.
43. Pietras RJ, Szego CM (1977) Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 265:69-72.
44. Razandi M, Pedram A, Greene GL, Levin ER (1999) Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol Endocrinol 13:307-319.
45. Selkoe DJ (1994) Normal and abnormal biology of the beta-amyloid precursor protein. Annu Rev Neurosci 17:489-517.
46. Shughrue PJ, Lane MV, Merchenthaler I (1999) Biologically active estrogen receptor-beta: evidence from in vivo autoradiographic studies with estrogen receptor alpha-knockout mice. Endocrinology 140:2613-2620.
47. Simpkins JW, Green PS, Gridley KE, Singh M, de Fiebre NC, Rajakumar G (1997) Role of estrogen replacement therapy in memory enhancement and the prevention of neuronal loss associated with Alzheimer's disease. Am J Med 103:19S-25S.
48. Singh M, Meyer EM, Millard WJ, Simpkins JW (1994) Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 644:305-312.
49. Singh M, Sétáló Jr G, Guan X, Warren M, Toran-Allerand CD (1999) Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J Neurosci 19:1179-1188.
50. Sohrabji F, Greene L, Miranda R, Toran-Allerand CD (1994) Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. J Neurobiol 25:974-988.
51. Sukovich DA, Mukherjee R, Benfield PA (1994) A novel, cell-type-specific mechanism for estrogen receptor-mediated gene activation in the absence of an estrogen-responsive element. Mol Cell Biol 14:7134-7143.
52. Tang MX, Jacobs D, Stern Y, Marder K, Schofield P, Gurland B, Andrews H, Mayeux R (1996) Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 348:429-432.
53. Toran-Allerand CD (1976) Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res 106:407-412.
54. Toran-Allerand CD (1984) On the genesis of sexual differentiation of the central nervous system: morphogenetic consequences of steroidal exposure and possible role of alpha-fetoprotein. Prog Brain Res 61:63-98.
55. Toran-Allerand CD (1996) The estrogen/neurotrophin connection during neural development: is co-localization of estrogen receptors with the neurotrophins and their receptors biologically relevant? Dev Neurosci 18:36-48.
56. Toran-Allerand CD, Miranda R, Bentham W, Sohrabji F, Brown T, Hochberg R, MacLusky N (1992) Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proc Natl Acad Sci USA 89:4668-4672.
57. Witkowska HE, Carlquist M, Engstrom O, Carlsson B, Bonn T, Gustafsson JA, Shackleton CH (1997) Characterization of bacterially expressed rat estrogen receptor beta ligand binding domain by mass spectrometry: structural comparison with estrogen receptor alpha. Steroids 62:621-631.
58. Xu H, Gouras GK, Greenfield JP, Vincent B, Naslund J, Mazzarelli L, Fried G, Jovanovic JN, Seeger M, Relkin NR, Liao F, Checler F, Buxbaum JD, Chait BT, Thinakaran G, Sisodia SS, Wang R, Greengard P, Gandy S (1998) Estrogen reduces neuronal generation of Alzheimer beta-amyloid peptides. Nat Med 4:447-451.
59. Zhou X, Rush R (1995) Sympathetic neurons in neonatal rats require endogenous neurotrophin-3 for survival. J Neurosci 15:6521-6530.