Oestradiol-Induced Synapse Formation in the Female Hippocampus: Roles of Oestrogen Receptor Subtypes

Journal of Neuroendocrinology

Volumn 26, Issue 7, 2014, Pages 439-447

  Zhou, L ^a   Fester, L ^a   Haghshenas, S ^a   de Vrese, X ^a   von Hacht, R ^a   Gloger, S ^a   Brandt, N ^a   Bader, M ^b   Vollmer, G ^b   Rune, G M ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

ArKO; Aromatase; Hippocampus; Oestrogen receptor

Indexed keywords

AROMATASE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA AGONIST; ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR BETA AGONIST; HORMONE RECEPTOR STIMULATING AGENT; SELECTIVE ESTROGEN RECEPTOR MODULATOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AROMATASE DEFICIENCY; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; HIPPOCAMPUS; HORMONE SYNTHESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SLICE CULTURE; SPINE; SYNAPSE; UPREGULATION; ANIMAL; C57BL MOUSE; CYTOLOGY; DENDRITIC SPINE; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; NERVOUS SYSTEM DEVELOPMENT; ORGAN CULTURE TECHNIQUE; RAT; WISTAR RAT;

ANIMALS; AROMATASE; DENDRITIC SPINES; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGENESIS; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; SYNAPSES;

EID: 84902990023     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12162     Document Type: Article

References (87)

1. Gould E, Woolley CS, Frankfurt M, McEwen BS. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 1990; 10: 1286-1291.
2. Woolley CS, Gould E, Frankfurt M, McEwen BS. Naturally-occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 1990; 10: 4035-4039.
3. Spencer JL, Waters EM, Romeo RD, Wood GE, Milner TA, McEwen BS. Uncovering the mechanisms of estrogen effects on hippocampal function. Front Neuroendocrinol 2008; 29: 219-237.
4. McCarthy MM. A lumpers versus splitters approach to sexual differentiation of the brain. Front Neuroendocrinol 2011; 32: 114-123.
5. Daniel JM. Estrogens, estrogen receptors, and female cognitive aging: the impact of timing. Horm Behav 2013; 63: 231-237.
6. Frick KM. Epigenetics, estradiol, and hippocampal memory consolidation. J Neuroendocrinol 2013; 25: 1151-1162.
7. Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 1997; 388: 507-525.
8. Foster TC. Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging. Hippocampus 2012; 22: 656-669.
9. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, Alves SE. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 2001; 429: 355-371.
10. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 2003; 144: 2055-2067.
11. Srivastava DP, Woolfrey KM, Liu F, Brandon NJ, Penzes P. Estrogen receptor β activity modulates synaptic signaling and structure. J Neurosci 2010; 30: 13454-13460.
12. Kramár EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, Lynch G. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci 2009; 29: 12982-12993.
13. Liu F, Day M, Muniz LC, Bitran D, Arias R, Revilla-Sanchez R, Grauer S, Zhang G, Kelley C, Pulito V, Sung A, Mervis RF, Navarra R, Hirst WD, Reinhart PH, Marquis KL, Moss SJ, Pangalos MN, Brandon NJ. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 2008; 11: 334-343.
14. Tan XJ, Dai YB, Wu WF, Kim HJ, Barros RP, Richardson TI, Yaden BC, Warner M, McKinzie DL, Krishnan V, Gustafsson JA. Reduction of dendritic spines and elevation of GABAergic signaling in the brains of mice treated with an estrogen receptor beta ligand. Proc Natl Acad Sci USA 2012; 109: 1708-1712.
15. Qu N, Wang L, Liu Z-C, Tian Q, Zhang Q. Oestrogen receptor α agonist improved long-term ovariectomy-induced spatial cognition deficit in young rats. Int J Neuropsychopharmacol 2013; 16: 1071-1082.
16. Jelks KB, Wylie R, Floyd CL, McAllister AK, Wise P. Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-alpha. J Neurosci 2007; 27: 6903-6913.
17. Waters EM, Mitterling K, Spencer JL, Mazid S, McEwen BS, Milner TA. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res 2009; 1290: 1-11.
18. Spencer-Segal JL, Tsuda MC, Mattei L, Waters EM, Romeo RD, Milner TA, McEwen BS, Ogawa S. Estradiol acts via estrogen receptors alpha and beta on pathways important for synaptic plasticity in the mouse hippocampal formation. Neuroscience 2012; 202: 131-146.
19. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M, Gustafsson JA. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007; 87: 905-931.
20. Pettersson K, Grandien K, Kuiper GG, Gustafsson JA. Mouse estrogen receptor beta forms estrogen response element-binding heterodimers with estrogen receptor alpha. Mol Endocrinol 1997; 11: 1486-1496.
21. Nomura M, Korach KS, Pfaff DW, Ogawa S. Estrogen receptor beta (ERbeta) protein levels in neurons depend on estrogen receptor alpha (ERalpha) gene expression and on its ligand in a brain region-specific manner. Brain Res Mol Brain Res 2003; 110: 7-14.
22. Rissman EF, Heck AL, Leonard JE, Shupnik MA, Gustafsson JA. Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc Natl Acad Sci USA 2002; 99: 3996-4001.
23. Bjornstrom L, Sjoberg M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 2005; 19: 833-842.
24. Morissette M, Le Saux M, D'Astous M, Jourdain S, Al Sweidi S, Morin N, Estrada-Camarena E, Mendez P, Garcia-Segura LM, Di Paolo T. Contribution of estrogen receptors alpha and beta to the effects of estradiol in the brain. J Steroid Biochem Mol Biol 2008; 108: 327-338.
25. Romeo RD, McCarthy JB, Wang A, Milner TA, McEwen BS. Sex differences in hippocampal estradiol-induced N-methyl-D-aspartic acid binding and ultrastructural localization of estrogen receptor-alpha. Neuroendocrinology 2005; 81: 391-399.
26. Miranda P, Williams CL, Einstein G. Granule cells in aging rats are sexually dimorphic in their response to estradiol. J Neurosci 1999; 19: 3316-3325.
27. Adams MM, Shah RA, Janssen WG, Morrison JH. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc Natl Acad Sci USA 2001; 98: 8071-8076.
28. Yildirim M, Janssen WG, Tabori NE, Adams MM, Yuen GS, Akama KT, McEwen BS, Milner TA, Morrison JH. Estrogen and aging affect synaptic distribution of phosphorylated LIM kinase (pLIMK) in CA1 region of female rat hippocampus. Neuroscience 2008; 152: 360-370.
29. Bailey ME, Wang AC, Hao J, Janssen WG, Hara Y, Dumitriu D, Hof PR, Morrison JH. Interactive effects of age and estrogen on cortical neurons: implications for cognitive aging. Neuroscience 2011; 191: 148-158.
30. Witty CF, Gardella LP, Perez MC, Daniel JM. Short-term estradiol administration in aging ovariectomized rats provides lasting benefits for memory and the hippocampus: a role for insulin-like growth factor-I. Endocrinology 2013; 154: 842-852.
31. Bohacek J, Daniel JM. The ability of oestradiol administration to regulate protein levels of oestrogen receptor alpha in the hippocampus and prefrontal cortex of middle-aged rats is altered following long-term ovarian hormone deprivation. J Neuroendocrinol 2009; 21: 640-647.
32. Mitterling KL, Spencer JL, Dziedzic N, Shenoy S, McCarthy K, Waters EM, McEwen BS, Milner TA. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J Comp Neurol 2010; 518: 2729-2743.
33. Kretz O, Fester L, Wehrenberg U, Zhou L, Brauckmann S, Zhao S, Prange-Kiel J, Naumann T, Jarry H, Frotscher M, Rune GM. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 2004; 24: 5913-5921.
34. Rune GM, Wehrenberg U, Prange-Kiel J, Zhou L, Adelmann G, Frotscher M. Estrogen up-regulates estrogen receptor alpha and synaptophysin in slice cultures of rat hippocampus. Neuroscience 2002; 113: 167-175.
35. Fester L, Zhou L, Bütow A, Huber C, von Lossow R, Prange-Kiel J, Jarry H, Rune GM. Cholesterol-promoted synaptogenesis requires the conversion of cholesterol to estradiol in the hippocampus. Hippocampus 2009; 19: 692-705.
36. Kato A, Hojo Y, Higo S, Komatsuzaki Y, Murakami G, Yoshino H, Uebayashi M, Kawato S. Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines. Front Neural Circuits 2013; 7: 149.
37. Prange-Kiel J, Jarry H, Schoen M, Kohlmann P, Lohse C, Zhou L, Rune GM. Gonadotropin-releasing hormone regulates spine density via its regulatory role in hippocampal estrogen synthesis. J Cell Biol 2008; 180: 417-426.
38. Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci USA 1998; 95: 6965-6970.
39. Robertson KM, O'Donnell L, Jones MEE, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI, Simpson ER. Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc Natl Acad Sci USA 1999; 96: 7986-7991.
40. Prange-Kiel J, Rune GM, Leranth C. Median raphe mediates estrogenic effects to the hippocampus in female rats. Eur J Neurosci 2004; 19: 309-317.
41. Sterio DC. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 1984; 134: 127-136.
42. Zhou L, Fester L, von Blittersdorff B, Hassu B, Nogens H, Prange-Kiel J, Jarry H, Wegscheider K, Rune GM. Aromatase inhibitors induce spine synapse loss in the hippocampus of ovariectomized mice. Endocrinology 2010; 151: 1153-1160.
43. Walf AA, Koonce CJ, Frye CA. Adult female wildtype, but not oestrogen receptor beta knockout, mice have decreased depression-like behaviour during pro-oestrus and following administration of oestradiol or diarylpropionitrile. J Psychopharmacol 2009; 23: 442-450.
44. Couse JF, Korach KS. Contrasting phenotypes in reproductive tissues of female estrogen receptor null mice. Ann N Y Acad Sci 2001; 948: 1-8.
45. Couse JF, Curtis SW, Washburn TF, Eddy EM, Schomberg DW, Korach KS. Disruption of the mouse oestrogen receptor gene: resulting phenotypes and experimental findings. Biochem Soc Trans 1995; 23: 929-935.
46. Prange-Kiel J, Fester L, Zhou L, Lauke H, Carretero J, Rune GM. Inhibition of hippocampal estrogen synthesis causes region-specific downregulation of synaptic protein expression in hippocampal neurons. Hippocampus 2006; 16: 464-471.
47. Snyder MA, Smejkalova T, Forlano PM, Woolley CS. Multiple ERbeta antisera label in ERbeta knockout and null mouse tissues. J Neurosci Methods 2010; 188: 226-234.
48. Zuloaga DG, Zuloaga KL, Hinds LR, Carbone DL, Handa RJ. Estrogen receptor beta expression in the mouse forebrain: age and sex differences. J Comp Neurol 2014; 522: 358-371.
49. Zhou L, Lehan N, Wehrenberg U, Disteldorf E, von Lossow R, Mares U, Jarry H, Rune GM. Neuroprotection by estradiol: a role of aromatase against spine synapse loss after blockade of GABA(A) receptors. Exp Neurol 2007; 203: 72-81.
50. Fester L, Ribeiro-Gouveia V, Prange-Kiel J, von Schassen C, Bottner M, Jarry H, Rune GM. Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J Neurochem 2006; 97: 1136-1144.
51. Kuo J, Hamid N, Bondar G, Prossnitz ER, Micevych P. Membrane estrogen receptors stimulate intracellular calcium release and progesterone synthesis in hypothalamic astrocytes. J Neurosci 2010; 30: 12950-12957.
52. Chamniansawat S, Chongthammakun S. A priming role of local estrogen on exogenous estrogen-mediated synaptic plasticity and neuroprotection. Exp Mol Med 2012; 44: 403-411.
53. Mendez P, Garcia-Segura LM, Muller D. Estradiol promotes spine growth and synapse formation without affecting pre-established networks. Hippocampus 2011; 21: 1263-1267.
54. Lindberg MK, Moverare S, Skrtic S, Gao H, Dahlman-Wright K, Gustafsson JA, Ohlsson C. Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a 'ying yang' relationship between ERalpha and ERbeta in mice. Mol Endocrinol 2003; 17: 203-208.
55. Hall JM, McDonnell DP. The estrogen receptor β-isoform (ERβ) of the human estrogen receptor modulates ERα transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 1999; 140: 5566-5578.
56. Gottfried-Blackmore A, Croft G, McEwen BS, Bulloch K. Transcriptional activity of estrogen receptors ERα and ERβ in the EtC.1 cerebellar granule cell line. Brain Res 2007; 1186: 41-47.
57. Tanaka M, Sokabe M. Bidirectional modulatory effect of 17beta-estradiol on NMDA receptors via ERalpha and ERbeta in the dentate gyrus of juvenile male rats. Neuropharmacology 2013; 75: 262-273.
58. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997; 138: 863-870.
59. Tremblay GB, Tremblay A, Copeland NG, Gilbert DJ, Jenkins NA, Labrie F, Giguere V. Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. Mol Endocrinol 1997; 11: 353-365.
60. Phan A, Lancaster KE, Armstrong JN, MacLusky NJ, Choleris E. Rapid effects of estrogen receptor alpha and beta selective agonists on learning and dendritic spines in female mice. Endocrinology 2011; 152: 1492-1502.
61. Fester L, Prange-Kiel J, Zhou L, Blittersdorf BV, Bohm J, Jarry H, Schumacher M, Rune GM. Estrogen-regulated synaptogenesis in the hippocampus: sexual dimorphism in vivo but not in vitro. J Steroid Biochem Mol Biol 2012; 131: 24-29.
62. Szymczak S, Kalita K, Jaworski J, Mioduszewska B, Savonenko A, Markowska A, Merchenthaler I, Kaczmarek L. Increased estrogen receptor β expression correlates with decreased spine formation in the rat hippocampus. Hippocampus 2006; 16: 453-463.
63. Sun W, McConnell E, Pare JF, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 2013; 339: 197-200.
64. Petanjek Z, Judas M, Simic G, Rasin MR, Uylings HB, Rakic P, Kostovic I. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci USA 2011; 108: 13281-13286.
65. Sharma PK, Thakur MK. Expression of estrogen receptor (ER) alpha and beta in mouse cerebral cortex: effect of age, sex and gonadal steroids. Neurobiol Aging 2006; 27: 880-887.
66. Thakur MK, Sharma PK. Transcription of estrogen receptor alpha and beta in mouse cerebral cortex: effect of age, sex, 17beta-estradiol and testosterone. Neurochem Int 2007; 50: 314-321.
67. Gibbs RB. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging 2000; 21: 107-116.
68. Savonenko AV, Markowska AL. The cognitive effects of ovariectomy and estrogen replacement are modulated by aging. Neuroscience 2003; 119: 821-830.
69. Daniel JM, Sulzer JK, Hulst JL. Estrogen increases the sensitivity of ovariectomized rats to the disruptive effects produced by antagonism of D2 but not D1 dopamine receptors during performance of a response learning task. Horm Behav 2006; 49: 38-44.
70. Smith AL, Wein AJ. Estrogen replacement therapy for the treatment of postmenopausal genitourinary tract dysfunction. Discov Med 2010; 10: 500-510.
71. Sherwin BB. Estrogen and cognitive aging in women. Neuroscience 2006; 138: 1021-1026.
72. Bean LA, Ianov L, Foster TC. Estrogen receptors, the hippocampus, and memory. Neuroscientist 2014; doi: 10.1177/1073858413519865. Epub ahead of print.
73. Li C, Brake WG, Romeo RD, Dunlop JC, Gordon M, Buzescu R, Magarinos AM, Allen PB, Greengard P, Luine V, McEwen BS. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc Natl Acad Sci USA 2004; 101: 2185-2190.
74. Xu X, Zhang Z. Effects of estradiol benzoate on learning-memory behavior and synaptic structure in ovariectomized mice. Life Sci 2006; 79: 1553-1560.
75. Phan A, Gabor CS, Favaro KJ, Kaschack S, Armstrong JN, MacLusky NJ, Choleris E. Low doses of 17beta-estradiol rapidly improve learning and increase hippocampal dendritic spines. Neuropsychopharmacology 2012; 37: 2299-2309.
76. Murphy DD, Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 1996; 16: 4059-4068.
77. Smith CC, McMahon LL. Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J Neurosci 2005; 25: 7780-7791.
78. Mosselman S, Polman J, Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 1996; 392: 49-53.
79. McInerney EM, Weis KE, Sun J, Mosselman S, Katzenellenbogen BS. Transcription activation by the human estrogen receptor subtype beta (ER beta) studied with ER beta and ER alpha receptor chimeras. Endocrinology 1998; 139: 4513-4522.
80. Cowley SM, Parker MG. A comparison of transcriptional activation by ER alpha and ER beta. J Steroid Biochem Mol Biol 1999; 69: 165-175.
81. Mendoza-Garcés L, Mendoza-Rodríguez CA, Jiménez-Trejo F, Picazo O, Rodríguez MC, Cerbón M. Differential expression of estrogen receptors in two hippocampal regions during the estrous cycle of the rat. Anat Rec (Hoboken) 2011; 294: 1913-1919.
82. Murphy DD, Cole NB, Greenberger V, Segal M. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J Neurosci 1998; 18: 2550-2559.
83. Prange-Kiel J, Wehrenberg U, Jarry H, Rune GM. Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus 2003; 13: 226-234.
84. Fester L, Labitzke J, Hinz R, Behem C, Horling K, Bernard T, Bader M, Vollmer G, Rune GM. Estradiol responsiveness of synaptopodin in hippocampal neurons is mediated by ERβ. J Steroid Biochem Mol Biol 2013; 138: 455-461.
85. Higaki S, Takumi K, Itoh M, Watanabe G, Taya K, Shimizu K, Hayashi M, Oishi T. Response of ERbeta and aromatase expression in the monkey hippocampal formation to ovariectomy and menopause. Neurosci Res 2012; 72: 148-154.
86. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, McEwen BS, Morrison JH. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 2002; 22: 3608-3614.
87. Han J, Murthy R, Wood B, Song B, Wang S, Sun B, Malhi H, Kaufman RJ. ER stress signalling through eIF2alpha and CHOP, but not IRE1alpha, attenuates adipogenesis in mice. Diabetologia 2013; 56: 911-924.