Estrogen receptors, the hippocampus, and memory

Neuroscientist

Volumn 20, Issue 5, 2014, Pages 534-545

  Bean, Linda A ^a   Ianov, Lara ^a,b   Foster, Thomas C ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

aging; estrogen; estrogen receptor alpha (ER ); hippocampus; memory

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; DIARYLPROPIONITRILE; DNA; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR; HISTONE; HISTONE DEACETYLASE; MESSENGER RNA; VIRUS VECTOR;

AGED; AGING; BRAIN FUNCTION; COGNITION; ENZYME ACTIVATION; ESTRADIOL BLOOD LEVEL; FEEDBACK SYSTEM; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HUMAN; KNOCKOUT MOUSE; MAZE TEST; MEMORY; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; COGNITIVE DEFECT; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

AGING; ANIMALS; COGNITION; COGNITION DISORDERS; HIPPOCAMPUS; HUMANS; MEMORY; RECEPTORS, ESTROGEN;

EID: 84902963207     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858413519865     Document Type: Review

References (80)

1. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci. 2002 ; 22 (9). 3608-14
2. 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 U S A. 2001 ; 98 (14). 8071-6
3. Aenlle KK, Foster TC. Aging alters the expression of genes for neuroprotection and synaptic function following acute estradiol treatment. Hippocampus. 2010 ; 20 (9). 1047-60
4. Aenlle KK, Kumar A, Cui L, Jackson TC, Foster TC. Estrogen effects on cognition and hippocampal transcription in middle-aged mice. Neurobiol Aging. 2009 ; 30 (6). 932-45
5. Bake S, Sohrabji F. 17β-Estradiol differentially regulates blood-brain barrier permeability in young and aging female rats. Endocrinology. 2004 ; 145 (12). 5471-5
6. Barker JM, Galea LA. Sex and regional differences in estradiol content in the prefrontal cortex, amygdala and hippocampus of adult male and female rats. Gen Comp Endocrinol. 2009 ; 164 (1). 77-84
7. Barkhem T, Carlsson B, Nilsson Y, Enmark E, Gustafsson J, Nilsson S. Differential response of estrogen receptor α and estrogen receptor β to partial estrogen agonists/antagonists. Mol Pharmacol. 1998 ; 54 (1). 105-12
8. Benedusi V, Meda C, Della Torre S, Monteleone G, Vegeto E, Maggi A. A lack of ovarian function increases neuroinflammation in aged mice. Endocrinology. 2012 ; 153 (6). 2777-88
9. Bohacek J, Daniel JM. The beneficial effects of estradiol on attentional processes are dependent on timing of treatment initiation following ovariectomy in middle-aged rats. Psychoneuroendocrinology. 2009 ; 35 (5). 694-705
10. Boulware MI, Heisler JD, Frick KM. The memory-enhancing effects of hippocampal estrogen receptor activation involve metabotropic glutamate receptor signaling. J Neurosci. 2013 ; 33 (38). 15184-94
11. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol. 2007 ; 193 (2). 311-21
12. Brinton RD. Cellular and molecular mechanisms of estrogen regulation of memory function and neuroprotection against Alzheimer's disease: recent insights and remaining challenges. Learn Mem. 2001 ; 8 (3). 121-33
13. Calabrese EJ. Estrogen and related compounds: biphasic dose responses. Crit Rev Toxicol. 2001 ; 31 (4-5). 503-15
14. Carroll JC, Pike CJ. Selective estrogen receptor modulators differentially regulate Alzheimer-like changes in female 3xTg-AD mice. Endocrinology. 2008 ; 149 (5). 2607-11
15. Chung WC, Pak TR, Suzuki S, Pouliot WA, Andersen ME, Handa RJ. Detection and localization of an estrogen receptor β splice variant protein (ERβ2) in the adult female rat forebrain and midbrain regions. J Comp Neurol. 2007 ; 505 (3). 249-67
16. Clark S, Rainville J, Zhao X, Katzenellenbogen BS, Pfaff D, Vasudevan N. Estrogen receptor-mediated transcription involves the activation of multiple kinase pathways in neuroblastoma cells. J Steroid Biochem Mol Biol 139C:. 2013 ;: 45-53
17. Corbo RM, Gambina G, Ruggeri M, Scacchi R. Association of estrogen receptor α (ESR1) PvuII and XbaI polymorphisms with sporadic Alzheimer's disease and their effect on apolipoprotein E concentrations. Dement Geriatr Cogn Disord. 2006 ; 22 (1). 67-72
18. Daniel JM. Effects of oestrogen on cognition: what have we learned from basic research?. J Neuroendocrinol. 2006 ; 18 (10). 787-95
19. Fan L, Zhao Z, Orr PT, Chambers CH, Lewis MC, Frick KM. Estradiol-induced object memory consolidation in middle-aged female mice requires dorsal hippocampal extracellular signal-regulated kinase and phosphatidylinositol 3-kinase activation. J Neurosci. 2010 ; 30 (12). 4390-400
20. Farr TD, Carswell HV, Gsell W, Macrae IM. Estrogen receptor β agonist diarylpropiolnitrile (DPN) does not mediate neuroprotection in a rat model of permanent focal ischemia. Brain Res. 2007 ; 1185: 275-82
21. Foster TC. Interaction of rapid signal transduction cascades and gene expression in mediating estrogen effects on memory over the life span. Front Neuroendocrinol. 2005 ; 26 (2). 51-64
22. Foster TC. Role of estrogen receptor α and β expression and signaling on cognitive function during aging. Hippocampus. 2012 ; 22 (4). 656-69
23. Foster TC, Rani A, Kumar A, Cui L, Semple-Rowland SL. Viral vector-mediated delivery of estrogen receptor-α to the hippocampus improves spatial learning in estrogen receptor-α knockout mice. Mol Ther. 2008 ; 16 (9). 1587-93
24. Foster TC, Sharrow KM, Kumar A, Masse J. Interaction of age and chronic estradiol replacement on memory and markers of brain aging. Neurobiol Aging. 2003 ; 24 (6). 839-52
25. Frye CA, Duffy CK, Walf AA. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol Learn Mem. 2007 ; 88 (2). 208-16
26. Fugger HN, Foster TC, Gustafsson J, Rissman EF. Novel effects of estradiol and estrogen receptor α and β on cognitive function. Brain Res. 2000 ; 883 (2). 258-64
27. Fugger HN, Kumar A, Lubahn DB, Korach KS, Foster TC. Examination of estradiol effects on the rapid estradiol mediated increase in hippocampal synaptic transmission in estrogen receptor α knockout mice. Neurosci Lett. 2001 ; 309 (3). 207-9
28. Gibbs RB. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging. 2000 ; 21 (1). 107-16
29. Gingerich S, Kim GL, Chalmers JA, Koletar MM, Wang X, Wang Y. Estrogen receptor alpha and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neuroscience. 2010 ; 170 (1). 54-66
30. Gore AC, Walker DM, Zama AM, Armenti AE, Uzumcu M. Early life exposure to endocrine-disrupting chemicals causes lifelong molecular reprogramming of the hypothalamus and premature reproductive aging. Mol Endocrinol. 2011 ; 25 (12). 2157-68
31. 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 (12). 5566-78
32. Hammond R, Mauk R, Ninaci D, Nelson D, Gibbs RB. Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm Behav. 2009 ; 56 (3). 309-14
33. Han X, Aenlle KK, Bean LA, Rani A, Semple-Rowland SL, Kumar A. Role of estrogen receptor alpha and beta in preserving hippocampal function during aging. J Neurosci. 2013 ; 33 (6). 2671-83
34. Hogervorst E, Bandelow S. Sex steroids to maintain cognitive function in women after the menopause: a meta-analyses of treatment trials. Maturitas. 2010 ; 66 (1). 56-71
35. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017α and P450 aromatase localized in neurons. Proc Natl Acad Sci U S A. 2004 ; 101 (3). 865-70
36. Ishunina TA, Swaab DF. Alterations in the human brain in menopause. Maturitas. 2007 ; 57 (1). 20-2
37. Jacome LF, Gautreaux C, Inagaki T, Mohan G, Alves S, Lubbers LS. Estradiol and ERβ agonists enhance recognition memory, and DPN, an ERβ agonist, alters brain monoamines. Neurobiol Learn Mem. 2010 ; 94 (4). 488-98
38. Ji Y, Urakami K, Wada-Isoe K, Adachi Y, Nakashima K. Estrogen receptor gene polymorphisms in patients with Alzheimer's disease, vascular dementia and alcohol-associated dementia. Dement Geriatr Cogn Disord. 2000 ; 11 (3). 119-22
39. Jones TT, Brewer GJ. Critical age-related loss of cofactors of neuron cytochrome C oxidase reversed by estrogen. Exp Neurol. 2009 ; 215 (2). 212-9
40. Kim J, Kim JY, Song KS, Lee YH, Seo JS, Jelinek J. Epigenetic changes in estrogen receptor beta gene in atherosclerotic cardiovascular tissues and in-vitro vascular senescence. Biochim Biophys Acta. 2007 ; 1772 (1). 72-80
41. Kuroki Y, Fukushima K, Kanda Y, Mizuno K, Watanabe Y. Putative membrane-bound estrogen receptors possibly stimulate mitogen-activated protein kinase in the rat hippocampus. Eur J Pharmacol 400(2-3):. 2000 ;: 205-9
42. Li LC, Shiina H, Deguchi M, Zhao H, Okino ST, Kane CJ. Age-dependent methylation of ESR1 gene in prostate cancer. Biochem Biophys Res Commun. 2004 ; 321 (2). 455-61
43. Liu F, Day M, Muniz LC, Bitran D, Arias R, Revilla-Sanchez R. Activation of estrogen receptor-β regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci. 2008 ; 11 (3). 334-43
44. Lonard DM, Nawaz Z, Smith CL, O'Malley BW. The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-α transactivation. Mol Cell. 2000 ; 5 (6). 939-48
45. Maki PM, Henderson VW. Hormone therapy, dementia, and cognition: the Women's Health Initiative 10 years on. Climacteric. 2012 ; 15 (3). 256-62
46. Markham JA, Pych JC, Juraska JM. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm Behav. 2002 ; 42 (3). 284-93
47. Markowska AL, Savonenko AV. Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci. 2002 ; 22 (24). 10985-95
48. Maruyama NO, Lucas TF, Porto CS, Abdalla FM. Estrogen receptor ESR1 regulates the phospholipase C-inositol phosphate signaling in the hippocampus from rats in proestrous and estrous phases. Steroids. 2013 ; 78 (1). 8-14
49. Mehra RD, Sharma K, Nyakas C, Vij U. Estrogen receptor α and β immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res. 2005 ; 1056 (1). 22-35
50. 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 (3). 355-71
51. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor α. Endocrinology. 2003 ; 144 (5). 2055-67
52. Mitterling KL, Spencer JL, Dziedzic N, Shenoy S, McCarthy K, Waters EM. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J Comp Neurol. 2010 ; 518 (14). 2729-43
53. Neese SL, Korol DL, Katzenellenbogen JA, Schantz SL. Impact of estrogen receptor α and β agonists on delayed alternation in middle-aged rats. Horm Behav. 2010 ; 58 (5). 878-90
54. Olsen L, Rasmussen HB, Hansen T, Bagger YZ, Tanko LB, Qin G. Estrogen receptor α and risk for cognitive impairment in postmenopausal women. Psychiatr Genet. 2006 ; 16 (2). 85-8
55. Packard MG. Posttraining estrogen and memory modulation. Horm and Behav. 1998 ; 34 (2). 126-39
56. Pettersson K, Delaunay F, Gustafsson JA. Estrogen receptor beta acts as a dominant regulator of estrogen signaling. Oncogene. 2000 ; 19 (43). 4970-8
57. Phan A, Lancaster KE, Armstrong JN, MacLusky NJ, Choleris E. Rapid effects of estrogen receptor α and β selective agonists on learning and dendritic spines in female mice. Endocrinology. 2011 ; 152 (4). 1492-502
58. Pinzone JJ, Stevenson H, Strobl JS, Berg PE. Molecular and cellular determinants of estrogen receptor α expression. Mol Cell Biol. 2004 ; 24 (11). 4605-12
59. Post WS, Goldschmidt-Clermont PJ, Wilhide CC, Heldman AW, Sussman MS, Ouyang P. Methylation of the estrogen receptor gene is associated with aging and atherosclerosis in the cardiovascular system. Cardiovasc Res. 1999 ; 43 (4). 985-91
60. Prange-Kiel J, Wehrenberg U, Jarry H, Rune GM. Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus. 2003 ; 13 (2). 226-34
61. Qu N, Wang L, Liu ZC, Tian Q, Zhang Q. Oestrogen receptor α agonist improved long-term ovariectomy-induced spatial cognition deficit in young rats. Int J Neuropsychopharmacol. 2013 ; 16 (5). 1071-82
62. Rao YS, Mott NN, Wang Y, Chung WC, Pak TR. MicroRNAs in the aging female brain: a putative mechanism for age-specific estrogen effects. Endocrinology. 2013 ; 154 (8). 2795-806
63. Resnick SM, Metter EJ, Zonderman AB. Estrogen replacement therapy and longitudinal decline in visual memory. A possible protective effect?. Neurology. 1997 ; 49 (6). 1491-7
64. 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 U S A. 2002 ; 99 (6). 3996-4001
65. Rodgers SP, Bohacek J, Daniel JM. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology. 2010 ; 151 (3). 1194-203
66. Schwarz JM, Nugent BM, McCarthy MM. Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology. 2010 ; 151 (10). 4871-81
67. Sherwin BB. Estrogen therapy: is time of initiation critical for neuroprotection?. Nat Rev Endocrinol. 2009 ; 5 (11). 620-7
68. Suzuki S, Brown CM, Wise PM. Neuroprotective effects of estrogens following ischemic stroke. Front Neuroendocrinol. 2009 ; 30 (2). 201-11
69. Szymczak S, Kalita K, Jaworski J, Mioduszewska B, Savonenko A, Markowska A. Increased estrogen receptor β expression correlates with decreased spine formation in the rat hippocampus. Hippocampus. 2006 ; 16 (5). 453-63
70. Tateishi Y, Sonoo R, Sekiya Y, Sunahara N, Kawano M, Wayama M. Turning off estrogen receptor β-mediated transcription requires estrogen-dependent receptor proteolysis. Mol Cell Biol. 2006 ; 26 (21). 7966-76
71. Walf AA, Koonce CJ, Frye CA. Estradiol or diarylpropionitrile administration to wild type, but not estrogen receptor β knockout, mice enhances performance in the object recognition and object placement tasks. Neurobiol Learn Mem. 2008 ; 89 (4). 513-21
72. Waters EM, Yildirim M, Janssen WG, Lou WY, McEwen BS, Morrison JH. Estrogen and aging affect the synaptic distribution of estrogen receptor β-immunoreactivity in the CA1 region of female rat hippocampus. Brain Res. 2011 ; 1379: 86-97
73. Westberry JM, Trout AL, Wilson ME. Epigenetic regulation of estrogen receptor beta expression in the rat cortex during aging. Neuroreport. 2011 ; 22 (9). 428-32
74. Witty CF, Foster TC, Semple-Rowland SL, Daniel JM. Increasing hippocampal estrogen receptor α levels via viral vectors increases MAP kinase activation and enhances memory in aging rats in the absence of ovarian estrogens. PLoS One. 2012 ; 7 (12). e51385
75. Wu TW, Chen S, Brinton RD. Membrane estrogen receptors mediate calcium signaling and MAP kinase activation in individual hippocampal neurons. Brain Res. 2011 ; 1379: 34-43
76. Wu WW, Bryant DN, Dorsa DM, Adelman JP, Maylie J. Ovarian hormone loss impairs excitatory synaptic transmission at hippocampal CA3-CA1 synapses. J Neurosci. 2013 ; 33 (41). 16158-69
77. Yaffe K, Lui LY, Grady D, Stone K, Morin P. Estrogen receptor 1 polymorphisms and risk of cognitive impairment in older women. Biol Psychiatry. 2002 ; 51 (8). 677-82
78. Zandi PP, Carlson MC, Plassman BL, Welsh-Bohmer KA, Mayer LS, Steffens DC. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA. 2002 ; 288 (17). 2123-9
79. Zhang QG, Han D, Wang RM, Dong Y, Yang F, Vadlamudi RK. C terminus of Hsc70-interacting protein (CHIP)-mediated degradation of hippocampal estrogen receptor-α and the critical period hypothesis of estrogen neuroprotection. Proc Natl Acad Sci U S A. 2011 ; 108 (35). E617-24
80. Zhang QG, Raz L, Wang R, Han D, De Sevilla L, Yang F. Estrogen attenuates ischemic oxidative damage via an estrogen receptor α-mediated inhibition of NADPH oxidase activation. J Neurosci. 2009 ; 29 (44). 13823-36