Estrogens, estrogen receptors, and female cognitive aging: The impact of timing

Hormones and Behavior

Volumn 63, Issue 2, 2013, Pages 231-237

  Daniel, Jill M ^a  

^a TULANE UNIVERSITY   (United States)

Author keywords

Aging; Critical period; Estradiol; Hippocampus; Learning and memory; Window of opportunity

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA;

AGING; BRAIN FUNCTION; CHOLINERGIC SYSTEM; COGNITION; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; LEARNING; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TASK PERFORMANCE; WORKING MEMORY;

AGING; ANIMALS; BRAIN; COGNITION; ESTROGENS; FEMALE; HUMANS; MODELS, BIOLOGICAL; RECEPTORS, ESTROGEN; TIME FACTORS;

EID: 84872876186     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.05.003     Document Type: Review

References (78)

1. Adams M.M., Shah R.A., Janssen W.G., Morrison J.H. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8071-8076.
2. Adams M.M., Fink S.E., Shah R.A., Janssen W.G., Hayashi S., Milner T.A., McEwen B.S., Morrison J.H. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J. Neurosci. 2002, 22:3608-3614.
3. Bagger Y.Z., Tanko L.B., Alexandersen P., Qin G., Christiansen C. Early postmenopausal hormone therapy may prevent cognitive impairment later in life. Menopause 2005, 12:12-17.
4. Bimonte-Nelson H.A., Acosta J.I., Talboom J.S. Neuroscientists as cartographers: mapping the crossroads of gonadal hormones, memory and age using animal models. Molecules 2010, 15:6050-6105.
5. Bohacek J., Daniel J.M. 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.
6. Bohacek J., Daniel J.M. The beneficial effects of estradiol on attentional processes are dependent on timing of treatment initiation following ovariectomy in middle-aged rats. Psychoneuroendocrinology 2010, 35:694-705.
7. Bohacek J., Bearl A.M., Daniel J.M. Long-term ovarian hormone deprivation alters the ability of subsequent oestradiol replacement to regulate choline acetyltransferase protein levels in the hippocampus and prefrontal cortex of middle-aged rats. J. Neuroendocrinol. 2008, 20:1023-1027.
8. Bora S.H., Liu Z., Kecojevic A., Merchenthaler I., Koliatsos V.E. Direct, complex effects of estrogens on basal forebrain cholinergic neurons. Exp. Neurol. 2005, 194:506-522.
9. Cardona-Gomez G.P., DonCarlos L., Garcia-Segura L.M. Insulin-like growth factor I receptors and estrogen receptors colocalize in female rat brain. Neuroscience 2000, 99:751-760.
10. Daniel J.M. Effects of oestrogen on cognition: what have we learned from basic research?. J. Neuroendocrinol. 2006, 18:787-795.
11. Daniel J.M., Dohanich G.P. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J. Neurosci. 2001, 21:6949-6956.
12. Daniel J.M., Hulst J.L., Lee C.D. Role of hippocampal M2 muscarinic receptors in the estrogen-induced enhancement of working memory. Neuroscience 2005, 132:57-64.
13. Daniel J.M., Hulst J.L., Berbling J.L. Estradiol replacement enhances working memory in middle-aged rats when initiated immediately after ovariectomy but not after a long-term period of ovarian hormone deprivation. Endocrinology 2006, 147:607-614.
14. Dohanich G.P., Korol D.L., Shors T.J. Steroids, learning and memory. Hormones, Brain and Behavior 2009, 539-576. Academic Press, San Diego. D.W. Pfaff, A.P. Arnold, S.E. Fahrbach, A.M. Etgen, R.T. Rubin (Eds.).
15. Dumas J., Hancur-Bucci C., Naylor M., Sites C., Newhouse P. Estradiol interacts with the cholinergic system to affect verbal memory in postmenopausal women: evidence for the critical period hypothesis. Horm. Behav. 2008, 53:159-169.
16. Espeland M.A., Rapp S.R., Shumaker S.A., Brunner R., Manson J.E., Sherwin B.B., Hsia J., Margolis K.L., Hogan P.E., Wallace R., Dailey M., Freeman R., Hays J. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004, 291:2959-2968.
17. Fader A.J., Johnson P.E., Dohanich G.P. Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine of a radial-arm maze. Pharmacol. Biochem. Behav. 1999, 62:711-717.
18. Foster T.C. Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging. Hippocampus 2012, 22:656-669.
19. Foster T.C., Rani A., Kumar A., Cui L., Semple-Rowland S.L. Viral vector-mediated delivery of estrogen receptor-alpha to the hippocampus improves spatial learning in estrogen receptor-alpha knockout mice. Mol. Ther. 2008, 16:1587-1593.
20. Foy M.R., Xu J., Xie X., Brinton R.D., Thompson R.F., Berger T.W. 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J. Neurophysiol. 1999, 81:925-929.
21. Frick K.M. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here?. Horm. Behav. 2009, 55:2-23.
22. Gabor R., Nagle R., Johnson D.A., Gibbs R.B. Estrogen enhances potassium-stimulated acetylcholine release in the rat hippocampus. Brain Res. 2003, 962:244-247.
23. Gallagher M., Rapp P.R. The use of animal models to study the effects of aging on cognition. Annu. Rev. Psychol. 1997, 48:339-370.
24. Ghosh S., Thakur M.K. Age-dependent decrease in the interaction of beta-tubulin with estrogen receptor alpha transactivation domain in mouse brain. Neurosci. Lett. 2009, 464:218-221.
25. Gibbs R.B. Expression of estrogen receptor-like immunoreactivity by different subgroups of basal forebrain cholinergic neurons in gonadectomized male and female rats. Brain Res. 1996, 720:61-68.
26. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol. Aging 2000, 21:107-116.
27. Gibbs R.B. Effects of ageing and long-term hormone replacement on cholinergic neurones in the medial septum and nucleus basalis magnocellularis of ovariectomized rats. J. Neuroendocrinol. 2003, 15:477-485.
28. Gibbs R.B. Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr. Rev. 2010, 31:224-253.
29. Gibbs R.B., Mauk R., Nelson D., Johnson D.A. Donepezil treatment restores the ability of estradiol to enhance cognitive performance in aged rats: evidence for the cholinergic basis of the critical period hypothesis. Horm. Behav. 2009, 56:73-83.
30. Gould E., Woolley C.S., Frankfurt M., McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 1990, 10:1286-1291.
31. Hall J.M., Couse J.F., Korach K.S. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 2001, 276:36869-36872.
32. Hamilton R.T., Rettberg J.R., Mao Z., To J., Zhao L., Appt S.E., Register T.C., Kaplan J.R., Brinton R.D. Hippocampal responsiveness to 17beta-estradiol and equol after long-term ovariectomy: implication for a therapeutic window of opportunity. Brain Res. 2011, 1379:11-22.
33. Henderson V.W. Action of estrogens in the aging brain: dementia and cognitive aging. Biochim. Biophys. Acta 2010, 1800:1077-1083.
34. Kalesnykas G., Roschier U., Puolivali J., Wang J., Miettinen R. The effect of aging on the subcellular distribution of estrogen receptor-alpha in the cholinergic neurons of transgenic and wild-type mice. Eur. J. Neurosci. 2005, 21:1437-1442.
35. Kang J.H., Grodstein F. Postmenopausal hormone therapy, timing of initiation. APOE and cognitive decline. Neurobiol. Aging 2012, 33:1129-1137.
36. Kato S., Endoh H., Masuhiro Y., Kitamoto T., Uchiyama S., Sasaki H., Masushige S., Gotoh Y., Nishida E., Kawashima H., Metzger D., Chambon P. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995, 270:1491-1494.
37. Kelly J.F., Bienias J.L., Shah A., Meeke K.A., Schneider J.A., Soriano E., Bennett D.A. Levels of estrogen receptors alpha and beta in frontal cortex of patients with Alzheimer's disease: relationship to Mini-Mental State Examination scores. Curr. Alzheimer Res. 2008, 5:45-51.
38. Korol D.L. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol. Learn. Mem. 2004, 82:309-323.
39. Kretz O., Fester L., Wehrenberg U., Zhou L., Brauckmann S., Zhao S., Prange-Kiel J., Naumann T., Jarry H., Frotscher M., Rune G.M. Hippocampal synapses depend on hippocampal estrogen synthesis. J. Neurosci. 2004, 24:5913-5921.
40. Luine V.N. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp. Neurol. 1985, 89:484-490.
41. Luine V.N. Sex steroids and cognitive function. J. Neuroendocrinol. 2008, 20:866-872.
42. MacLusky N.J., Luine V.N., Hajszan T., Leranth C. The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 2005, 146:287-293.
43. Maki P.M. A systematic review of clinical trials of hormone therapy on cognitive function: effects of age at initiation and progestin use. Ann. N. Y. Acad. Sci. 2005, 1052:182-197.
44. Maki P.M., Dennerstein L., Clark M., Guthrie J., Lamontagne P., Fornelli D., Little D., Henderson V.W., Resnick S.M. Perimenopausal use of hormone therapy is associated with enhanced memory and hippocampal function later in life. Brain Res. 2011, 1379:232-243.
45. Markowska A.L., Savonenko A.V. Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J. Neurosci. 2002, 22:10985-10995.
46. McLaughlin K.J., Bimonte-Nelson H., Neisewander J.L., Conrad C.D. Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17beta-estradiol effectiveness in altering CA1 spines. Horm. Behav. 2008, 54:386-395.
47. Mehra R.D., Sharma K., Nyakas C., Vij U. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res. 2005, 1056:22-35.
48. Miettinen R.A., Kalesnykas G., Koivisto E.H. Estimation of the total number of cholinergic neurons containing estrogen receptor-alpha in the rat basal forebrain. J. Histochem. Cytochem. 2002, 50:891-902.
49. Miller V.M., Black D.M., Brinton E.A., Budoff M.J., Cedars M.I., Hodis H.N., Lobo R.A., Manson J.E., Merriam G.R., Naftolin F., Santoro N., Taylor H.S., Harman S.M. Using basic science to design a clinical trial: baseline characteristics of women enrolled in the Kronos Early Estrogen Prevention Study (KEEPS). J. Cardiovasc. Transl. Res. 2009, 2:228-239.
50. Mukai H., Kimoto T., Hojo Y., Kawato S., Murakami G., Higo S., Hatanaka Y., Ogiue-Ikeda M. Modulation of synaptic plasticity by brain estrogen in the hippocampus. Biochim. Biophys. Acta 2010, 1800:1030-1044.
51. Rapp S.R., Espeland M.A., Shumaker S.A., Henderson V.W., Brunner R.L., Manson J.E., Gass M.L., Stefanick M.L., Lane D.S., Hays J., Johnson K.C., Coker L.H., Dailey M., Bowen D. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003, 289:2663-2672.
52. Resnick S.M., Henderson V.W. Hormone therapy and risk of Alzheimer disease: a critical time. JAMA 2002, 288:2170-2172.
53. Rocca W.A., Bower J.H., Maraganore D.M., Ahlskog J.E., Grossardt B.R., de Andrade M., Melton L.J. Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause. Neurology 2007, 69:1074-1083.
54. Rocca W.A., Grossardt B.R., Shuster L.T. Oophorectomy, menopause, estrogen treatment, and cognitive aging: clinical evidence for a window of opportunity. Brain Res. 2011, 1379:188-198.
55. Rodgers S.P., Bohacek J., Daniel J.M. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 2010, 151:1194-1203.
56. Rudick C.N., Gibbs R.B., Woolley C.S. A role for the basal forebrain cholinergic system in estrogen-induced disinhibition of hippocampal pyramidal cells. J. Neurosci. 2003, 23:4479-4490.
57. Sandstrom N.J., Williams C.L. Memory retention is modulated by acute estradiol and progesterone replacement. Behav. Neurosci. 2001, 115:384-393.
58. Sherwin B.B., Henry J.F. Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: a critical review. Front. Neuroendocrinol. 2008, 29:88-113.
59. Shumaker S.A., Legault C., Rapp S.R., Thal L., Wallace R.B., Ockene J.K., Hendrix S.L., Jones B.N., Assaf A.R., Jackson R.D., Kotchen J.M., Wassertheil-Smoller S., Wactawski-Wende J. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003, 289:2651-2662.
60. Shumaker S.A., Legault C., Kuller L., Rapp S.R., Thal L., Lane D.S., Fillit H., Stefanick M.L., Hendrix S.L., Lewis C.E., Masaki K., Coker L.H. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004, 291:2947-2958.
61. Smith C.C., McMahon L.L. Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J. Neurosci. 2006, 26:8517-8522.
62. Smith C.C., Vedder L.C., Nelson A.R., Bredemann T.M., McMahon L.L. Duration of estrogen deprivation, not chronological age, prevents estrogen's ability to enhance hippocampal synaptic physiology. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:19543-19548.
63. Spencer J.L., Waters E.M., Romeo R.D., Wood G.E., Milner T.A., McEwen B.S. Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol. 2008, 29:219-237.
64. Stelly C.E., Cronin J., Daniel J.M., Schrader L.A. Long-term oestradiol treatment enhances hippocampal synaptic plasticity that is dependent on muscarinic acetylcholine receptors in ovariectomised female rats. J. Neuroendocrinol. 2012, 24:887-896.
65. Towart L.A., Alves S.E., Znamensky V., Hayashi S., McEwen B.S., Milner T.A. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J. Comp. Neurol. 2003, 463:390-401.
66. Valley C.C., Solodin N.M., Powers G.L., Ellison S.J., Alarid E.T. Temporal variation in estrogen receptor-alpha protein turnover in the presence of estrogen. J. Mol. Endocrinol. 2008, 40:23-34.
67. Warren S.G., Humphreys A.G., Juraska J.M., Greenough W.T. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res. 1995, 703:26-30.
68. Waters E.M., Yildirim M., Janssen W.G., Lou W.Y., McEwen B.S., Morrison J.H., Milner T.A. Estrogen and aging affect the synaptic distribution of estrogen receptor beta-immunoreactivity in the CA1 region of female rat hippocampus. Brain Res. 2011, 1379:86-97.
69. Whitmer R.A., Quesenberry C.P., Zhou J., Yaffe K. Timing of hormone therapy and dementia: the critical window theory revisited. Ann. Neurol. 2011, 69:163-169.
70. Woolley C.S., McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 1992, 12:2549-2554.
71. Woolley C.S., McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism. J. Neurosci. 1994, 14:7680-7687.
72. Woolley C.S., Weiland N.G., McEwen B.S., Schwartzkroin P.A. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci. 1997, 17:1848-1859.
73. Wu W.W., Adelman J.P., Maylie J. Ovarian hormone deficiency reduces intrinsic excitability and abolishes acute estrogen sensitivity in hippocampal CA1 pyramidal neurons. J. Neurosci. 2011, 31:2638-2648.
74. Yaffe K., Lui L.Y., Grady D., Stone K., Morin P. Estrogen receptor 1 polymorphisms and risk of cognitive impairment in older women. Biol. Psychiatry 2002, 51:677-682.
75. Yaffe K., Lindquist K., Sen S., Cauley J., Ferrell R., Penninx B., Harris T., Li R., Cummings S.R. Estrogen receptor genotype and risk of cognitive impairment in elders: findings from the Health ABC study. Neurobiol. Aging 2009, 30:607-614.
76. Yao J., Hamilton R.T., Cadenas E., Brinton R.D. Decline in mitochondrial bioenergetics and shift to ketogenic profile in brain during reproductive senescence. Biochim. Biophys. Acta 2010, 1800:1121-1126.
77. Zhang Q.G., Raz L., Wang R., Han D., De S.L., Yang F., Vadlamudi R.K., Brann D.W. Estrogen attenuates ischemic oxidative damage via an estrogen receptor alpha-mediated inhibition of NADPH oxidase activation. J. Neurosci. 2009, 29:13823-13836.
78. Zhang Q.G., Han D., Wang R.M., Dong Y., Yang F., Vadlamudi R.K., Brann D.W. C terminus of Hsc70-interacting protein (CHIP)-mediated degradation of hippocampal estrogen receptor-alpha and the critical period hypothesis of estrogen neuroprotection. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:E617-E624.