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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

The Critical Period for Neuroprotection by Estrogen Replacement Therapy and the Potential Underlying Mechanisms

Author(s): Hang Guo, Min Liu, Lixia Zhang, Long Wang, Wugang Hou, Yaqun Ma* and Yulong Ma*

Volume 18, Issue 6, 2020

Page: [485 - 500] Pages: 16

DOI: 10.2174/1570159X18666200123165652

Price: $65

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Abstract

17β-Estradiol (estradiol or E2) is a steroid hormone that has been broadly applied as a neuroprotective therapy for a variety of neurodegenerative and cerebrovascular disorders such as ischemic stroke, Alzheimer's disease, and Parkinson's disease. Several laboratory and clinical studies have reported that Estrogen Replacement Therapy (ERT) had no effect against these diseases in elderly postmenopausal women, and at worst, increased their risk of onset and mortality. This review focuses on the growing body of data from in vitro and animal models characterizing the potential underlying mechanisms and signaling pathways that govern successful neuroprotection by ERT, including the roles of E2 receptors in mediating neuroprotection, E2 genomic regulation of apoptosis- related pathways, membrane-bound receptor-mediated non-genomic signaling pathways, and the antioxidant mechanisms of E2. Also discussed is the current evidence for a critical period of effective treatment with estrogen following natural or surgical menopause and the outcomes of E2 administration within an advantageous time period. The known mechanisms governing the duration of the critical period include depletion of E2 receptors, the switch to a ketogenic metabolic profile by neuronal mitochondria, and a decrease in acetylcholine that accompanies E2 deficiency. Also the major clinical trials and observational studies concerning postmenopausal Hormone Therapy (HT) are summarized to compare their outcomes with respect to neurological disease and discuss their relevance to the critical period hypothesis. Finally, potential controversies and future directions for this field are discussed throughout the review.

Keywords: Estrogen, neuroprotection, ischemic stroke, alzheimer's disease, parkinson's disease, menopause, critical period, hormone therapy.

Graphical Abstract
[1]
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.
[http://dx.doi.org/10.1016/j.brainres.2010.10.031] [PMID: 20965156]
[2]
Kato, I.; Toniolo, P.; Akhmedkhanov, A.; Koenig, K.L.; Shore, R.; Zeleniuch-Jacquotte, A. Prospective study of factors influencing the onset of natural menopause. J. Clin. Epidemiol., 1998, 51(12), 1271-1276.
[http://dx.doi.org/10.1016/S0895-4356(98)00119-X] [PMID: 10086819]
[3]
Woods, N.F.; Mitchell, E.S. Symptoms during the perimenopause: prevalence, severity, trajectory, and significance in women’s lives. Am. J. Med., 2005, 118(Suppl. 12B), 14-24.
[4]
Shuster, L.T.; Rhodes, D.J.; Gostout, B.S.; Grossardt, B.R.; Rocca, W.A. Premature menopause or early menopause: long-term health consequences. Maturitas, 2010, 65(2), 161-166.
[http://dx.doi.org/10.1016/j.maturitas.2009.08.003] [PMID: 19733988]
[5]
Henderson, V.W.; Sherwin, B.B. Surgical versus natural menopause: cognitive issues. Menopause, 2007, 14(3 Pt 2), 572-579.
[http://dx.doi.org/10.1097/gme.0b013e31803df49c] [PMID: 17476147]
[6]
Rocca, W.A.; Bower, J.H.; Maraganore, D.M.; Ahlskog, J.E.; Grossardt, B.R.; de Andrade, M.; Melton, L.J., III Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause. Neurology, 2007, 69(11), 1074-1083.
[http://dx.doi.org/10.1212/01.wnl.0000276984.19542.e6] [PMID: 17761551]
[7]
Rocca, W.A.; Shuster, L.T.; Grossardt, B.R.; Maraganore, D.M.; Gostout, B.S.; Geda, Y.E.; Melton, L.J., III Long-term effects of bilateral oophorectomy on brain aging: unanswered questions from the Mayo Clinic Cohort Study of Oophorectomy and Aging. Womens Health (Lond), 2009, 5(1), 39-48.
[http://dx.doi.org/10.2217/17455057.5.1.39] [PMID: 19102639]
[8]
Nation, D.A.; Hong, S.; Jak, A.J.; Delano-Wood, L.; Mills, P.J.; Bondi, M.W.; Dimsdale, J.E. Stress, exercise, and Alzheimer’s disease: a neurovascular pathway. Med. Hypotheses, 2011, 76(6), 847-854.
[http://dx.doi.org/10.1016/j.mehy.2011.02.034] [PMID: 21398043]
[9]
Appelros, P.; Stegmayr, B.; Terént, A. Sex differences in stroke epidemiology: a systematic review. Stroke, 2009, 40(4), 1082-1090.
[http://dx.doi.org/10.1161/STROKEAHA.108.540781] [PMID: 19211488]
[10]
Rivera, C.M.; Grossardt, B.R.; Rhodes, D.J.; Rocca, W.A. Increased mortality for neurological and mental diseases following early bilateral oophorectomy. Neuroepidemiology, 2009, 33(1), 32-40.
[http://dx.doi.org/10.1159/000211951] [PMID: 19365140]
[11]
Shen, L.; Song, L.; Liu, B.; Li, H.; Zheng, X.; Zhang, L.; Yuan, J.; Liang, Y.; Wang, Y. Effects of early age at natural menopause on coronary heart disease and stroke in Chinese women. Int. J. Cardiol., 2017, 241, 6-11.
[http://dx.doi.org/10.1016/j.ijcard.2017.03.127] [PMID: 28392079]
[12]
Murphy, S.J.; McCullough, L.D.; Smith, J.M. Stroke in the female: role of biological sex and estrogen. ILAR J., 2004, 45(2), 147-159.
[http://dx.doi.org/10.1093/ilar.45.2.147] [PMID: 15111734]
[13]
Rosenberg, L.; Park, S. Verbal and spatial functions across the menstrual cycle in healthy young women. Psychoneuroendocrinology, 2002, 27(7), 835-841.
[http://dx.doi.org/10.1016/S0306-4530(01)00083-X] [PMID: 12183218]
[14]
Sherwin, B.B. Estrogen and cognitive functioning in women. Endocr. Rev., 2003, 24(2), 133-151.
[http://dx.doi.org/10.1210/er.2001-0016] [PMID: 12700177]
[15]
Lord, C.; Buss, C.; Lupien, S.J.; Pruessner, J.C. Hippocampal volumes are larger in postmenopausal women using estrogen therapy compared to past users, never users and men: a possible window of opportunity effect. Neurobiol. Aging, 2008, 29(1), 95-101.
[http://dx.doi.org/10.1016/j.neurobiolaging.2006.09.001] [PMID: 17030472]
[16]
Jover, T.; Tanaka, H.; Calderone, A.; Oguro, K.; Bennett, M.V.; Etgen, A.M.; Zukin, R.S. Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. J. Neurosci., 2002, 22(6), 2115-2124.
[http://dx.doi.org/10.1523/JNEUROSCI.22-06-02115.2002] [PMID: 11896151]
[17]
Schmidt, R.; Fazekas, F.; Reinhart, B.; Kapeller, P.; Fazekas, G.; Offenbacher, H.; Eber, B.; Schumacher, M.; Freidl, W. Estrogen replacement therapy in older women: a neuropsychological and brain MRI study. J. Am. Geriatr. Soc., 1996, 44(11), 1307-1313.
[http://dx.doi.org/10.1111/j.1532-5415.1996.tb01400.x] [PMID: 8909345]
[18]
Siani, F.; Greco, R.; Levandis, G. Influence of Estrogen Modulation on Glia Activation in a Murine Model of Parkinson’s Disease. Front. Neurosci., 2017, 11, 306.
[19]
Carrasquilla, G.D.; Frumento, P.; Berglund, A.; Borgfeldt, C.; Bottai, M.; Chiavenna, C. Postmenopausal hormone therapy and risk of stroke: A pooled analysis of data from population-based cohort studies. PLoS Med., 2017, 14(11) e1002445
[PMID: 29149179 ]
[20]
Chen, Y.H.; Hsieh, T.F.; Lee, C.C.; Wu, M.J.; Fu, Y.C. Estrogen therapy and ischemic stroke in women with diabetes aged over 55 years: a nation-wide prospective population-based study in Taiwan. PLoS One, 2015, 10(12)e0144910
[http://dx.doi.org/10.1371/journal.pone.0144910] [PMID: 26658781]
[21]
Canonico, M.; Carcaillon, L.; Plu-Bureau, G.; Oger, E.; Singh-Manoux, A.; Tubert-Bitter, P.; Elbaz, A.; Scarabin, P.Y. Postmenopausal hormone therapy and risk of stroke: impact of the route of estrogen administration and type of progestogen. Stroke, 2016, 47(7), 1734-1741.
[http://dx.doi.org/10.1161/STROKEAHA.116.013052] [PMID: 27256671]
[22]
Brann, D.W.; Dhandapani, K.; Wakade, C.; Mahesh, V.B.; Khan, M.M. Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids, 2007, 72(5), 381-405.
[http://dx.doi.org/10.1016/j.steroids.2007.02.003] [PMID: 17379265]
[23]
Hogervorst, E.; Williams, J.; Budge, M.; Riedel, W.; Jolles, J. The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience, 2000, 101(3), 485-512.
[http://dx.doi.org/10.1016/S0306-4522(00)00410-3] [PMID: 11113299]
[24]
Yaffe, K.; Sawaya, G.; Lieberburg, I.; Grady, D. Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. JAMA, 1998, 279(9), 688-695.
[http://dx.doi.org/10.1001/jama.279.9.688] [PMID: 9496988]
[25]
Kantarci, K.; Lowe, V.J.; Lesnick, T.G.; Tosakulwong, N.; Bailey, K.R.; Fields, J.A.; Shuster, L.T.; Zuk, S.M.; Senjem, M.L.; Mielke, M.M.; Gleason, C.; Jack, C.R.; Rocca, W.A.; Miller, V.M. Early Postmenopausal Transdermal 17β-Estradiol Therapy and Amyloid-β Deposition. J. Alzheimers Dis., 2016, 53(2), 547-556.
[http://dx.doi.org/10.3233/JAD-160258] [PMID: 27163830]
[26]
Wang, P.N.; Liao, S.Q.; Liu, R.S.; Liu, C.Y.; Chao, H.T.; Lu, S.R.; Yu, H.Y.; Wang, S.J.; Liu, H.C. Effects of estrogen on cognition, mood, and cerebral blood flow in AD: a controlled study. Neurology, 2000, 54(11), 2061-2066.
[http://dx.doi.org/10.1212/WNL.54.11.2061] [PMID: 10851363]
[27]
Mulnard, R.A.; Cotman, C.W.; Kawas, C.; van Dyck, C.H.; Sano, M.; Doody, R.; Koss, E.; Pfeiffer, E.; Jin, S.; Gamst, A.; Grundman, M.; Thomas, R.; Thal, L.J. Estrogen replacement therapy for treatment of mild to moderate Alzheimer disease: a randomized controlled trial. Alzheimer’s Disease Cooperative Study. JAMA, 2000, 283(8), 1007-1015.
[http://dx.doi.org/10.1001/jama.283.8.1007] [PMID: 10697060]
[28]
Henderson, V.W.; Paganini-Hill, A.; Miller, B.L.; Elble, R.J.; Reyes, P.F.; Shoupe, D.; McCleary, C.A.; Klein, R.A.; Hake, A.M.; Farlow, M.R. Estrogen for Alzheimer’s disease in women: randomized, double-blind, placebo-controlled trial. Neurology, 2000, 54(2), 295-301.
[http://dx.doi.org/10.1212/WNL.54.2.295] [PMID: 10668686]
[29]
Maki, P.M. Critical window hypothesis of hormone therapy and cognition: a scientific update on clinical studies. Menopause, 2013, 20(6), 695-709.
[http://dx.doi.org/10.1097/GME.0b013e3182960cf8] [PMID: 23715379]
[30]
Zandi, P.P.; Carlson, M.C.; Plassman, B.L.; Welsh-Bohmer, K.A.; Mayer, L.S.; Steffens, D.C.; Breitner, J.C. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA, 2002, 288(17), 2123-2129.
[http://dx.doi.org/10.1001/jama.288.17.2123] [PMID: 12413371]
[31]
Shumaker, S.A.; Legault, C.; Rapp, S.R.; Thal, L.; Wallace, R.B.; Ockene, J.K.; Hendrix, S.L.; Jones, B.N., III; 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(20), 2651-2662.
[http://dx.doi.org/10.1001/jama.289.20.2651] [PMID: 12771112]
[32]
Shao, H.; Breitner, J.C.; Whitmer, R.A.; Wang, J.; Hayden, K.; Wengreen, H.; Corcoran, C.; Tschanz, J.; Norton, M.; Munger, R.; Welsh-Bohmer, K.; Zandi, P.P. Hormone therapy and Alzheimer disease dementia: new findings from the Cache County Study. Neurology, 2012, 79(18), 1846-1852.
[http://dx.doi.org/10.1212/WNL.0b013e318271f823] [PMID: 23100399]
[33]
Barrett-Connor, E.; Grady, D.; Sashegyi, A.; Anderson, P.W.; Cox, D.A.; Hoszowski, K.; Rautaharju, P.; Harper, K.D. Raloxifene and cardiovascular events in osteoporotic postmenopausal women: four-year results from the MORE (Multiple Outcomes of Raloxifene Evaluation) randomized trial. JAMA, 2002, 287(7), 847-857.
[http://dx.doi.org/10.1001/jama.287.7.847] [PMID: 11851576]
[34]
Walsh, B.W.; Paul, S.; Wild, R.A.; Dean, R.A.; Tracy, R.P.; Cox, D.A.; Anderson, P.W. The effects of hormone replacement therapy and raloxifene on C-reactive protein and homocysteine in healthy postmenopausal women: a randomized, controlled trial. J. Clin. Endocrinol. Metab., 2000, 85(1), 214-218.
[PMID: 10634389]
[35]
Walsh, B.W.; Kuller, L.H.; Wild, R.A.; Paul, S.; Farmer, M.; Lawrence, J.B.; Shah, A.S.; Anderson, P.W. Effects of raloxifene on serum lipids and coagulation factors in healthy postmenopausal women. JAMA, 1998, 279(18), 1445-1451.
[http://dx.doi.org/10.1001/jama.279.18.1445] [PMID: 9600478]
[36]
Saitta, A.; Altavilla, D.; Cucinotta, D.; Morabito, N.; Frisina, N.; Corrado, F.; D’Anna, R.; Lasco, A.; Squadrito, G.; Gaudio, A.; Cancellieri, F.; Arcoraci, V.; Squadrito, F. Randomized, double-blind, placebo-controlled study on effects of raloxifene and hormone replacement therapy on plasma no concentrations, endothelin-1 levels, and endothelium-dependent vasodilation in postmenopausal women. Arterioscler. Thromb. Vasc. Biol., 2001, 21(9), 1512-1519.
[http://dx.doi.org/10.1161/hq0901.095565] [PMID: 11557681]
[37]
Goss, P.E. Emerging role of aromatase inhibitors in the adjuvant setting. Am. J. Clin. Oncol., 2003, 26(4), S27-S33.
[http://dx.doi.org/10.1097/00000421-200308001-00005] [PMID: 12902874]
[38]
Hozumi, Y.; Suemasu, K.; Takei, H.; Aihara, T.; Takehara, M.; Saito, T.; Ohsumi, S.; Masuda, N.; Ohashi, Y. The effect of exemestane, anastrozole, and tamoxifen on lipid profiles in Japanese postmenopausal early breast cancer patients: final results of National Surgical Adjuvant Study BC 04, the TEAM Japan sub-study. Ann. Oncol., 2011, 22(8), 1777-1782.
[http://dx.doi.org/10.1093/annonc/mdq707] [PMID: 21285133]
[39]
Amir, E.; Seruga, B.; Niraula, S.; Carlsson, L.; Ocaña, A. Toxicity of adjuvant endocrine therapy in postmenopausal breast cancer patients: a systematic review and meta-analysis. J. Natl. Cancer Inst., 2011, 103(17), 1299-1309.
[http://dx.doi.org/10.1093/jnci/djr242] [PMID: 21743022]
[40]
Chlebowski, R.T.; Haque, R.; Hedlin, H.; Col, N.; Paskett, E.; Manson, J.E.; Kubo, J.T.; Johnson, K.C.; Wactawski-Wende, J.; Pan, K.; Anderson, G. Benefit/risk for adjuvant breast cancer therapy with tamoxifen or aromatase inhibitor use by age, and race/ethnicity. Breast Cancer Res. Treat., 2015, 154(3), 609-616.
[http://dx.doi.org/10.1007/s10549-015-3647-1] [PMID: 26602222]
[41]
Hall, J.E.; Bhatta, N.; Adams, J.M.; Rivier, J.E.; Vale, W.W.; Crowley, W.F., Jr Variable tolerance of the developing follicle and corpus luteum to gonadotropin-releasing hormone antagonist-induced gonadotropin withdrawal in the human. J. Clin. Endocrinol. Metab., 1991, 72(5), 993-1000.
[http://dx.doi.org/10.1210/jcem-72-5-993] [PMID: 1902489]
[42]
Dubal, D.B.; Kashon, M.L.; Pettigrew, L.C.; Ren, J.M.; Finklestein, S.P.; Rau, S.W.; Wise, P.M. Estradiol protects against ischemic injury. J. Cereb. Blood Flow Metab., 1998, 18(11), 1253-1258.
[http://dx.doi.org/10.1097/00004647-199811000-00012] [PMID: 9809515]
[43]
Rusa, R.; Alkayed, N.J.; Crain, B.J.; Traystman, R.J.; Kimes, A.S.; London, E.D.; Klaus, J.A.; Hurn, P.D. 17beta-estradiol reduces stroke injury in estrogen-deficient female animals. Stroke, 1999, 30(8), 1665-1670.
[http://dx.doi.org/10.1161/01.STR.30.8.1665] [PMID: 10436119]
[44]
Dubal, D.B.; Zhu, H.; Yu, J.; Rau, S.W.; Shughrue, P.J.; Merchenthaler, I.; Kindy, M.S.; Wise, P.M. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. USA, 2001, 98(4), 1952-1957.
[http://dx.doi.org/10.1073/pnas.041483198] [PMID: 11172057]
[45]
Toung, T.J.; Traystman, R.J.; Hurn, P.D. Estrogen-mediated neuroprotection after experimental stroke in male rats. Stroke, 1998, 29(8), 1666-1670.
[http://dx.doi.org/10.1161/01.STR.29.8.1666] [PMID: 9707210]
[46]
Zhao, L.; Wu, T.W.; Brinton, R.D. Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Res., 2004, 1010(1-2), 22-34.
[http://dx.doi.org/10.1016/j.brainres.2004.02.066] [PMID: 15126114]
[47]
Ingberg, E.; Theodorsson, E.; Theodorsson, A.; Ström, J.O. Effects of high and low 17β-estradiol doses on focal cerebral ischemia in rats. Sci. Rep., 2016, 6, 20228.
[http://dx.doi.org/10.1038/srep20228] [PMID: 26839007]
[48]
Sharma, K.; Mehra, R.D. Long-term administration of estrogen or tamoxifen to ovariectomized rats affords neuroprotection to hippocampal neurons by modulating the expression of Bcl-2 and Bax. Brain Res., 2008, 1204, 1-15.
[http://dx.doi.org/10.1016/j.brainres.2008.01.080] [PMID: 18342840]
[49]
Xu, H.; Gouras, G.K.; Greenfield, J.P.; Vincent, B.; Naslund, J.; Mazzarelli, L.; Fried, G.; Jovanovic, J.N.; Seeger, M.; Relkin, N.R.; Liao, F.; Checler, F.; Buxbaum, J.D.; Chait, B.T.; Thinakaran, G.; Sisodia, S.S.; Wang, R.; Greengard, P.; Gandy, S. Estrogen reduces neuronal generation of Alzheimer β-amyloid peptides. Nat. Med., 1998, 4(4), 447-451.
[http://dx.doi.org/10.1038/nm0498-447] [PMID: 9546791]
[50]
Tschiffely, A.E.; Schuh, R.A.; Prokai-Tatrai, K.; Prokai, L.; Ottinger, M.A. A comparative evaluation of treatments with 17β-estradiol and its brain-selective prodrug in a double-transgenic mouse model of Alzheimer’s disease. Horm. Behav., 2016, 83, 39-44.
[http://dx.doi.org/10.1016/j.yhbeh.2016.05.009] [PMID: 27210479]
[51]
Liang, Z.; Valla, J.; Sefidvash-Hockley, S.; Rogers, J.; Li, R. Effects of estrogen treatment on glutamate uptake in cultured human astrocytes derived from cortex of Alzheimer’s disease patients. J. Neurochem., 2002, 80(5), 807-814.
[http://dx.doi.org/10.1046/j.0022-3042.2002.00779.x] [PMID: 11948244]
[52]
Jia, M.; Dahlman-Wright, K.; Gustafsson, J.Å. Estrogen receptor alpha and beta in health and disease. Best Pract. Res. Clin. Endocrinol. Metab., 2015, 29(4), 557-568.
[http://dx.doi.org/10.1016/j.beem.2015.04.008] [PMID: 26303083]
[53]
Merchenthaler, I.; Lane, M.V.; Numan, S.; Dellovade, T.L. Distribution of estrogen receptor alpha and beta in the mouse central nervous system: in vivo autoradiographic and immunocytochemical analyses. J. Comp. Neurol., 2004, 473(2), 270-291.
[http://dx.doi.org/10.1002/cne.20128] [PMID: 15101093]
[54]
Pérez, S.E.; Chen, E.Y.; Mufson, E.J. Distribution of estrogen receptor alpha and beta immunoreactive profiles in the postnatal rat brain. Brain Res. Dev. Brain Res., 2003, 145(1), 117-139.
[http://dx.doi.org/10.1016/S0165-3806(03)00223-2] [PMID: 14519499]
[55]
Mitra, S.W.; Hoskin, E.; Yudkovitz, J.; Pear, L.; Wilkinson, H.A.; Hayashi, S.; Pfaff, D.W.; Ogawa, S.; Rohrer, S.P.; Schaeffer, J.M.; McEwen, B.S.; Alves, S.E. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology, 2003, 144(5), 2055-2067.
[http://dx.doi.org/10.1210/en.2002-221069] [PMID: 12697714]
[56]
Shughrue, P.J.; Lane, M.V.; Merchenthaler, I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol., 1997, 388(4), 507-525.
[http://dx.doi.org/10.1002/(SICI)1096-9861(19971201)388:4<507:AID-CNE1>3.0.CO;2-6] [PMID: 9388012]
[57]
Sudo, S.; Wen, T.C.; Desaki, J.; Matsuda, S.; Tanaka, J.; Arai, T.; Maeda, N.; Sakanaka, M. Beta-estradiol protects hippocampal CA1 neurons against transient forebrain ischemia in gerbil. Neurosci. Res., 1997, 29(4), 345-354.
[http://dx.doi.org/10.1016/S0168-0102(97)00106-5] [PMID: 9527626]
[58]
Chen, J.; Adachi, N.; Liu, K.; Arai, T. The effects of 17beta-estradiol on ischemia-induced neuronal damage in the gerbil hippocampus. Neuroscience, 1998, 87(4), 817-822.
[http://dx.doi.org/10.1016/S0306-4522(98)00198-5] [PMID: 9759969]
[59]
Burek, M.; Steinberg, K.; Förster, C.Y. Mechanisms of transcriptional activation of the mouse claudin-5 promoter by estrogen receptor alpha and beta. Mol. Cell. Endocrinol., 2014, 392(1-2), 144-151.
[http://dx.doi.org/10.1016/j.mce.2014.05.003] [PMID: 24846172]
[60]
Kang, H.S.; Ahn, H.S.; Kang, H.J.; Gye, M.C. Effect of estrogen on the expression of occludin in ovariectomized mouse brain. Neurosci. Lett., 2006, 402(1-2), 30-34.
[http://dx.doi.org/10.1016/j.neulet.2006.03.052] [PMID: 16632200]
[61]
Shin, J.A.; Yang, S.J.; Jeong, S.I.; Park, H.J.; Choi, Y.H.; Park, E.M. Activation of estrogen receptor β reduces blood-brain barrier breakdown following ischemic injury. Neuroscience, 2013, 235, 165-173.
[http://dx.doi.org/10.1016/j.neuroscience.2013.01.031] [PMID: 23376369]
[62]
Lu, D.; Qu, Y.; Shi, F.; Feng, D.; Tao, K.; Gao, G.; He, S.; Zhao, T. Activation of G protein-coupled estrogen receptor 1 (GPER-1) ameliorates blood-brain barrier permeability after global cerebral ischemia in ovariectomized rats. Biochem. Biophys. Res. Commun., 2016, 477(2), 209-214.
[http://dx.doi.org/10.1016/j.bbrc.2016.06.044] [PMID: 27311857]
[63]
Garcia-Segura, L.M.; Arévalo, M.A.; Azcoitia, I. Interactions of estradiol and insulin-like growth factor-I signalling in the nervous system: new advances. Prog. Brain Res., 2010, 181, 251-272.
[http://dx.doi.org/10.1016/S0079-6123(08)81014-X] [PMID: 20478442]
[64]
Miller, N.R.; Jover, T.; Cohen, H.W.; Zukin, R.S.; Etgen, A.M.; Anne, M. Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death. Endocrinology, 2005, 146(7), 3070-3079.
[http://dx.doi.org/10.1210/en.2004-1515] [PMID: 15817665]
[65]
Fitzpatrick, J.L.; Mize, A.L.; Wade, C.B.; Harris, J.A.; Shapiro, R.A.; Dorsa, D.M. Estrogen-mediated neuroprotection against β-amyloid toxicity requires expression of estrogen receptor α or β and activation of the MAPK pathway. J. Neurochem., 2002, 82(3), 674-682.
[http://dx.doi.org/10.1046/j.1471-4159.2002.01000.x] [PMID: 12153491]
[66]
Sehara, Y.; Sawicka, K.; Hwang, J.Y.; Latuszek-Barrantes, A.; Etgen, A.M.; Zukin, R.S. Survivin Is a transcriptional target of STAT3 critical to estradiol neuroprotection in global ischemia. J. Neurosci., 2013, 33(30), 12364-12374.
[http://dx.doi.org/10.1523/JNEUROSCI.1852-13.2013] [PMID: 23884942]
[67]
Pietras, R.J.; Szego, C.M. Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature, 1977, 265(5589), 69-72.
[http://dx.doi.org/10.1038/265069a0] [PMID: 834244]
[68]
Levin, E.R. Plasma membrane estrogen receptors. Trends Endocrinol. Metab., 2009, 20(10), 477-482.
[http://dx.doi.org/10.1016/j.tem.2009.06.009] [PMID: 19783454]
[69]
Marin, R.; Guerra, B.; Alonso, R.; Ramírez, C.M.; Díaz, M. Estrogen activates classical and alternative mechanisms to orchestrate neuroprotection. Curr. Neurovasc. Res., 2005, 2(4), 287-301.
[http://dx.doi.org/10.2174/156720205774322629] [PMID: 16181121]
[70]
Garcia-Segura, L.M.; Sanz, A.; Mendez, P. Cross-talk between IGF-I and estradiol in the brain: focus on neuroprotection. Neuroendocrinology, 2006, 84(4), 275-279.
[http://dx.doi.org/10.1159/000097485] [PMID: 17124377]
[71]
Sheppard, P.A.S.; Koss, W.A.; Frick, K.M.; Choleris, E. Rapid actions of oestrogens and their receptors on memory acquisition and consolidation in females. J. Neuroendocrinol., 2017, 30e12485
[http://dx.doi.org/10.1111/jne.12485]
[72]
Kelly, M.J.; Levin, E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab., 2001, 12(4), 152-156.
[http://dx.doi.org/10.1016/S1043-2760(01)00377-0] [PMID: 11295570]
[73]
Bryant, D.N.; Sheldahl, L.C.; Marriott, L.K.; Shapiro, R.A.; Dorsa, D.M. Multiple pathways transmit neuroprotective effects of gonadal steroids. Endocrine, 2006, 29(2), 199-207.
[http://dx.doi.org/10.1385/ENDO:29:2:199] [PMID: 16785596]
[74]
Lebesgue, D.; Chevaleyre, V.; Zukin, R.S.; Etgen, A.M. Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids, 2009, 74(7), 555-561.
[http://dx.doi.org/10.1016/j.steroids.2009.01.003] [PMID: 19428444]
[75]
Lingwood, D.; Simons, K. Lipid rafts as a membrane-organizing principle. Science, 2010, 327(5961), 46-50.
[http://dx.doi.org/10.1126/science.1174621] [PMID: 20044567]
[76]
Goodenough, S.; Schleusner, D.; Pietrzik, C.; Skutella, T.; Behl, C. Glycogen synthase kinase 3beta links neuroprotection by 17beta-estradiol to key Alzheimer processes. Neuroscience, 2005, 132(3), 581-589.
[http://dx.doi.org/10.1016/j.neuroscience.2004.12.029] [PMID: 15837120]
[77]
Wang, C.; Zhang, F.; Jiang, S.; Siedlak, S.L.; Shen, L.; Perry, G.; Wang, X.; Tang, B.; Zhu, X. Estrogen receptor-α is localized to neurofibrillary tangles in Alzheimer’s disease. Sci. Rep., 2016, 6, 20352.
[http://dx.doi.org/10.1038/srep20352] [PMID: 26837465]
[78]
Kvingedal, A.M.; Smeland, E.B. A novel putative G-protein-coupled receptor expressed in lung, heart and lymphoid tissue. FEBS Lett., 1997, 407(1), 59-62.
[http://dx.doi.org/10.1016/S0014-5793(97)00278-0] [PMID: 9141481]
[79]
Prossnitz, E.R.; Arterburn, J.B.; Smith, H.O.; Oprea, T.I.; Sklar, L.A.; Hathaway, H.J. Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu. Rev. Physiol., 2008, 70, 165-190.
[http://dx.doi.org/10.1146/annurev.physiol.70.113006.100518] [PMID: 18271749]
[80]
Wang, Z.F.; Pan, Z.Y.; Xu, C.S.; Li, Z.Q. Activation of G-protein coupled estrogen receptor 1 improves early-onset cognitive impairment via PI3K/Akt pathway in rats with traumatic brain injury. Biochem. Biophys. Res. Commun., 2017, 482(4), 948-953.
[http://dx.doi.org/10.1016/j.bbrc.2016.11.138] [PMID: 27908726]
[81]
Bessa, A.; Campos, F.L.; Videira, R.A.; Mendes-Oliveira, J.; Bessa-Neto, D.; Baltazar, G. GPER: A new tool to protect dopaminergic neurons? Biochim. Biophys. Acta, 2015, 1852(10 Pt A), 2035-2041.
[http://dx.doi.org/10.1016/j.bbadis.2015.07.004] [PMID: 26170064]
[82]
Chen, J.; Hu, R.; Ge, H.; Duanmu, W.; Li, Y.; Xue, X.; Hu, S.; Feng, H. G-protein-coupled receptor 30-mediated antiapoptotic effect of estrogen on spinal motor neurons following injury and its underlying mechanisms. Mol. Med. Rep., 2015, 12(2), 1733-1740.
[http://dx.doi.org/10.3892/mmr.2015.3601] [PMID: 25872489]
[83]
Ruiz-Palmero, I.; Hernando, M.; Garcia-Segura, L.M.; Arevalo, M.A. G protein-coupled estrogen receptor is required for the neuritogenic mechanism of 17β-estradiol in developing hippocampal neurons. Mol. Cell. Endocrinol., 2013, 372(1-2), 105-115.
[http://dx.doi.org/10.1016/j.mce.2013.03.018] [PMID: 23545157]
[84]
Tang, H.; Zhang, Q.; Yang, L.; Dong, Y.; Khan, M.; Yang, F.; Brann, D.W.; Wang, R. Reprint of “GPR30 mediates estrogen rapid signaling and neuroprotection”. Mol. Cell. Endocrinol., 2014, 389(1-2), 92-98.
[http://dx.doi.org/10.1016/j.mce.2014.05.005] [PMID: 24835924]
[85]
Sareddy, G.R.; Zhang, Q.; Wang, R.; Scott, E.; Zou, Y.; O’Connor, J.C.; Chen, Y.; Dong, Y.; Vadlamudi, R.K.; Brann, D. Proline-, glutamic acid-, and leucine-rich protein 1 mediates estrogen rapid signaling and neuroprotection in the brain. Proc. Natl. Acad. Sci. USA, 2015, 112(48), E6673-E6682.
[http://dx.doi.org/10.1073/pnas.1516729112] [PMID: 26627258]
[86]
Suzuki, S.; Brown, C.M.; Dela Cruz, C.D.; Yang, E.; Bridwell, D.A.; Wise, P.M. Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions. Proc. Natl. Acad. Sci. USA, 2007, 104(14), 6013-6018.
[http://dx.doi.org/10.1073/pnas.0610394104] [PMID: 17389368]
[87]
Zhang, Q.G.; Raz, L.; Wang, R.; Han, D.; De Sevilla, 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(44), 13823-13836.
[http://dx.doi.org/10.1523/JNEUROSCI.3574-09.2009] [PMID: 19889994]
[88]
Prokai, L.; Prokai-Tatrai, K.; Perjesi, P.; Zharikova, A.D.; Perez, E.J.; Liu, R.; Simpkins, J.W. Quinol-based cyclic antioxidant mechanism in estrogen neuroprotection. Proc. Natl. Acad. Sci. USA, 2003, 100(20), 11741-11746.
[http://dx.doi.org/10.1073/pnas.2032621100] [PMID: 14504383]
[89]
Sun, X.; He, G.; Qing, H.; Zhou, W.; Dobie, F.; Cai, F.; Staufenbiel, M.; Huang, L.E.; Song, W. Hypoxia facilitates Alzheimer’s disease pathogenesis by up-regulating BACE1 gene expression. Proc. Natl. Acad. Sci. USA, 2006, 103(49), 18727-18732.
[http://dx.doi.org/10.1073/pnas.0606298103] [PMID: 17121991]
[90]
Brinton, R.D. The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci., 2008, 31(10), 529-537.
[http://dx.doi.org/10.1016/j.tins.2008.07.003] [PMID: 18774188]
[91]
Labandeira-Garcia, J.L.; Rodriguez-Perez, A.I.; Valenzuela, R.; Costa-Besada, M.A.; Guerra, M.J. Menopause and Parkinson’s disease. Interaction between estrogens and brain renin-angiotensin system in dopaminergic degeneration. Front. Neuroendocrinol., 2016, 43, 44-59.
[http://dx.doi.org/10.1016/j.yfrne.2016.09.003] [PMID: 27693730]
[92]
Genazzani, A.R.; Pluchino, N.; Luisi, S.; Luisi, M. Estrogen, cognition and female ageing. Hum. Reprod. Update, 2007, 13(2), 175-187.
[http://dx.doi.org/10.1093/humupd/dml042] [PMID: 17135285]
[93]
Henderson, V.W. Alzheimer’s disease and other neurological disorders. Climacteric, 2007, 10(Suppl. 2), 92-96.
[http://dx.doi.org/10.1080/13697130701534097] [PMID: 17882682]
[94]
Maki, P.M. Hormone therapy and cognitive function: is there a critical period for benefit? Neuroscience, 2006, 138(3), 1027-1030.
[http://dx.doi.org/10.1016/j.neuroscience.2006.01.001] [PMID: 16488547]
[95]
Sherwin, B.B. The clinical relevance of the relationship between estrogen and cognition in women. J. Steroid Biochem. Mol. Biol., 2007, 106(1-5), 151-156.
[http://dx.doi.org/10.1016/j.jsbmb.2007.05.016] [PMID: 17588742]
[96]
Sherwin, B.B. The critical period hypothesis: can it explain discrepancies in the oestrogen-cognition literature? J. Neuroendocrinol., 2007, 19(2), 77-81.
[http://dx.doi.org/10.1111/j.1365-2826.2006.01508.x] [PMID: 17214869]
[97]
Sherwin, B.B. Estrogen therapy: is time of initiation critical for neuroprotection? Nat. Rev. Endocrinol., 2009, 5(11), 620-627.
[http://dx.doi.org/10.1038/nrendo.2009.193] [PMID: 19844249]
[98]
Brinton, R.D. Investigative models for determining hormone therapy-induced outcomes in brain: evidence in support of a healthy cell bias of estrogen action. Ann. N. Y. Acad. Sci., 2005, 1052, 57-74.
[http://dx.doi.org/10.1196/annals.1347.005] [PMID: 16024751]
[99]
Brinton, R.D. Estrogen regulation of glucose metabolism and mitochondrial function: therapeutic implications for prevention of Alzheimer’s disease. Adv. Drug Deliv. Rev., 2008, 60(13-14), 1504-1511.
[http://dx.doi.org/10.1016/j.addr.2008.06.003] [PMID: 18647624]
[100]
Wassertheil-Smoller, S.; Hendrix, S.L.; Limacher, M.; Heiss, G.; Kooperberg, C.; Baird, A.; Kotchen, T.; Curb, J.D.; Black, H.; Rossouw, J.E.; Aragaki, A.; Safford, M.; Stein, E.; Laowattana, S.; Mysiw, W.J. Effect of estrogen plus progestin on stroke in postmenopausal women: the Women’s Health Initiative: a randomized trial. JAMA, 2003, 289(20), 2673-2684.
[http://dx.doi.org/10.1001/jama.289.20.2673] [PMID: 12771114]
[101]
MacLennan, A.H.; Henderson, V.W.; Paine, B.J.; Mathias, J.; Ramsay, E.N.; Ryan, P.; Stocks, N.P.; Taylor, A.W. Hormone therapy, timing of initiation, and cognition in women aged older than 60 years: the REMEMBER pilot study. Menopause, 2006, 13(1), 28-36.
[http://dx.doi.org/10.1097/01.gme.0000191204.38664.61] [PMID: 16607096]
[102]
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(1), 159-169.
[http://dx.doi.org/10.1016/j.yhbeh.2007.09.011] [PMID: 17964576]
[103]
Rocca, W.A.; Grossardt, B.R.; Shuster, L.T. Oophorectomy, menopause, estrogen, and cognitive aging: the timing hypothesis. Neurodegener. Dis., 2010, 7(1-3), 163-166.
[http://dx.doi.org/10.1159/000289229] [PMID: 20197698]
[104]
Thinnes, F.P. New findings concerning vertebrate porin II--on the relevance of glycine motifs of type-1 VDAC. Mol. Genet. Metab., 2013, 108(4), 212-224.
[http://dx.doi.org/10.1016/j.ymgme.2013.01.008] [PMID: 23419876]
[105]
Hodis, H.N.; Mack, W.J.; Henderson, V.W.; Shoupe, D.; Budoff, M.J.; Hwang-Levine, J.; Li, Y.; Feng, M.; Dustin, L.; Kono, N.; Stanczyk, F.Z.; Selzer, R.H.; Azen, S.P. Vascular Effects of Early versus Late Postmenopausal Treatment with Estradiol. N. Engl. J. Med., 2016, 374(13), 1221-1231.
[http://dx.doi.org/10.1056/NEJMoa1505241] [PMID: 27028912]
[106]
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 17β-estradiol and equol after long-term ovariectomy: implication for a therapeutic window of opportunity. Brain Res., 2011, 1379, 11-22.
[http://dx.doi.org/10.1016/j.brainres.2011.01.029] [PMID: 21241683]
[107]
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(1), 607-614.
[http://dx.doi.org/10.1210/en.2005-0998] [PMID: 16239296]
[108]
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(5), 694-705.
[http://dx.doi.org/10.1016/j.psyneuen.2009.10.010] [PMID: 19926225]
[109]
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. USA, 2010, 107(45), 19543-19548.
[http://dx.doi.org/10.1073/pnas.1009307107] [PMID: 20974957]
[110]
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(7), 2638-2648.
[http://dx.doi.org/10.1523/JNEUROSCI.6081-10.2011] [PMID: 21325532]
[111]
Yin, W.; Maguire, S.M.; Pham, B.; Garcia, A.N.; Dang, N.V.; Liang, J.; Wolfe, A.; Hofmann, H.A.; Gore, A.C. Testing the critical window hypothesis of timing and duration of estradiol treatment on hypothalamic gene networks in reproductively mature and aging female rats. Endocrinology, 2015, 156(8), 2918-2933.
[http://dx.doi.org/10.1210/en.2015-1032] [PMID: 26018250]
[112]
Baxter, M.G.; Santistevan, A.C.; Bliss-Moreau, E.; Morrison, J.H. Timing of cyclic estradiol treatment differentially affects cognition in aged female rhesus monkeys. Behav. Neurosci., 2018, 132(4), 213-223.
[http://dx.doi.org/10.1037/bne0000259] [PMID: 29952604]
[113]
Hara, Y.; Yuk, F.; Puri, R.; Janssen, W.G.; Rapp, P.R.; Morrison, J.H. Presynaptic mitochondrial morphology in monkey prefrontal cortex correlates with working memory and is improved with estrogen treatment. Proc. Natl. Acad. Sci. USA, 2014, 111(1), 486-491.
[http://dx.doi.org/10.1073/pnas.1311310110] [PMID: 24297907]
[114]
Li, Z.; Okamoto, K.; Hayashi, Y.; Sheng, M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 2004, 119(6), 873-887.
[http://dx.doi.org/10.1016/j.cell.2004.11.003] [PMID: 15607982]
[115]
Hara, Y.; Waters, E.M.; McEwen, B.S.; Morrison, J.H. Estrogen Effects on Cognitive and Synaptic Health Over the Lifecourse. Physiol. Rev., 2015, 95(3), 785-807.
[http://dx.doi.org/10.1152/physrev.00036.2014] [PMID: 26109339]
[116]
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. USA, 2011, 108(35), E617-E624.
[http://dx.doi.org/10.1073/pnas.1104391108] [PMID: 21808025]
[117]
Pratt, W.B.; Toft, D.O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev., 1997, 18(3), 306-360.
[PMID: 9183567]
[118]
Fan, M.; Park, A.; Nephew, K.P. CHIP (carboxyl terminus of Hsc70-interacting protein) promotes basal and geldanamycin-induced degradation of estrogen receptor-alpha. Mol. Endocrinol., 2005, 19(12), 2901-2914.
[http://dx.doi.org/10.1210/me.2005-0111] [PMID: 16037132]
[119]
Berry, N.B.; Fan, M.; Nephew, K.P. Estrogen receptor-alpha hinge-region lysines 302 and 303 regulate receptor degradation by the proteasome. Mol. Endocrinol., 2008, 22(7), 1535-1551.
[http://dx.doi.org/10.1210/me.2007-0449] [PMID: 18388150]
[120]
Tateishi, Y.; Kawabe, Y.; Chiba, T.; Murata, S.; Ichikawa, K.; Murayama, A.; Tanaka, K.; Baba, T.; Kato, S.; Yanagisawa, J. Ligand-dependent switching of ubiquitin-proteasome pathways for estrogen receptor. EMBO J., 2004, 23(24), 4813-4823.
[http://dx.doi.org/10.1038/sj.emboj.7600472] [PMID: 15538384]
[121]
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(1), 23-34.
[http://dx.doi.org/10.1677/JME-07-0067] [PMID: 18096994]
[122]
Weitsman, G.E.; Weebadda, W.; Ung, K.; Murphy, L.C. Reactive oxygen species induce phosphorylation of serine 118 and 167 on estrogen receptor alpha. Breast Cancer Res. Treat., 2009, 118(2), 269-279.
[http://dx.doi.org/10.1007/s10549-008-0221-0] [PMID: 18941890]
[123]
Srivastava, D.P.; Waters, E.M.; Mermelstein, P.G.; Kramár, E.A.; Shors, T.J.; Liu, F. Rapid estrogen signaling in the brain: implications for the fine-tuning of neuronal circuitry. J. Neurosci., 2011, 31(45), 16056-16063.
[http://dx.doi.org/10.1523/JNEUROSCI.4097-11.2011] [PMID: 22072656]
[124]
Meitzen, J.; Mermelstein, P.G. Estrogen receptors stimulate brain region specific metabotropic glutamate receptors to rapidly initiate signal transduction pathways. J. Chem. Neuroanat., 2011, 42(4), 236-241.
[http://dx.doi.org/10.1016/j.jchemneu.2011.02.002] [PMID: 21458561]
[125]
Micevych, P.E.; Kelly, M.J. Membrane estrogen receptor regulation of hypothalamic function. Neuroendocrinology, 2012, 96(2), 103-110.
[http://dx.doi.org/10.1159/000338400] [PMID: 22538318]
[126]
Lan, Y.L.; Zhao, J.; Li, S. Update on the neuroprotective effect of estrogen receptor alpha against Alzheimer’s disease. J. Alzheimers Dis., 2015, 43(4), 1137-1148.
[http://dx.doi.org/10.3233/JAD-141875] [PMID: 25159676]
[127]
Alonso, A.; Gonzalez, C. Neuroprotective role of estrogens: relationship with insulin/IGF-1 signaling. Front. Biosci. (Elite Ed.), 2012, 4, 607-619.
[http://dx.doi.org/10.2741/e403] [PMID: 22201898]
[128]
Arevalo, M.A.; Azcoitia, I.; Gonzalez-Burgos, I.; Garcia-Segura, L.M. Signaling mechanisms mediating the regulation of synaptic plasticity and memory by estradiol. Horm. Behav., 2015, 74, 19-27.
[http://dx.doi.org/10.1016/j.yhbeh.2015.04.016] [PMID: 25921586]
[129]
Marin, R. Signalosomes in the brain: relevance in the development of certain neuropathologies such as Alzheimer’s disease. Front. Physiol., 2011, 2, 23.
[http://dx.doi.org/10.3389/fphys.2011.00023] [PMID: 21852974]
[130]
Marin, R.; Ramírez, C.M.; González, M.; González-Muñoz, E.; Zorzano, A.; Camps, M.; Alonso, R.; Díaz, M. Voltage-dependent anion channel (VDAC) participates in amyloid beta-induced toxicity and interacts with plasma membrane estrogen receptor alpha in septal and hippocampal neurons. Mol. Membr. Biol., 2007, 24(2), 148-160.
[http://dx.doi.org/10.1080/09687860601055559] [PMID: 17453421]
[131]
Marin, R.; Díaz, M.; Alonso, R.; Sanz, A.; Arévalo, M.A.; Garcia-Segura, L.M. Role of estrogen receptor alpha in membrane-initiated signaling in neural cells: interaction with IGF-1 receptor. J. Steroid Biochem. Mol. Biol., 2009, 114(1-2), 2-7.
[http://dx.doi.org/10.1016/j.jsbmb.2008.12.014] [PMID: 19167493]
[132]
Ramírez, C.M.; González, M.; Díaz, M.; Alonso, R.; Ferrer, I.; Santpere, G.; Puig, B.; Meyer, G.; Marin, R. VDAC and ERalpha interaction in caveolae from human cortex is altered in Alzheimer’s disease. Mol. Cell. Neurosci., 2009, 42(3), 172-183.
[http://dx.doi.org/10.1016/j.mcn.2009.07.001] [PMID: 19595769]
[133]
Thinnes, F.P. After all, plasmalemmal expression of type-1 VDAC can be understood. Phosphorylation, nitrosylation, and channel modulators work together in vertebrate cell volume regulation and either apoptotic pathway. Front. Physiol., 2015, 6, 126.
[http://dx.doi.org/10.3389/fphys.2015.00126] [PMID: 25964761]
[134]
Herrera, J.L.; Diaz, M.; Hernández-Fernaud, J.R.; Salido, E.; Alonso, R.; Fernández, C.; Morales, A.; Marin, R. Voltage-dependent anion channel as a resident protein of lipid rafts: post-transductional regulation by estrogens and involvement in neuronal preservation against Alzheimer’s disease. J. Neurochem., 2011, 116(5), 820-827.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06987.x] [PMID: 21214547]
[135]
Fabelo, N.; Martín, V.; Santpere, G.; Marín, R.; Torrent, L.; Ferrer, I.; Díaz, M. Severe alterations in lipid composition of frontal cortex lipid rafts from Parkinson’s disease and incidental Parkinson’s disease. Mol. Med., 2011, 17(9-10), 1107-1118.
[http://dx.doi.org/10.2119/molmed.2011.00119] [PMID: 21717034]
[136]
Fabelo, N.; Martín, V.; Marín, R.; Moreno, D.; Ferrer, I.; Díaz, M. Altered lipid composition in cortical lipid rafts occurs at early stages of sporadic Alzheimer’s disease and facilitates APP/BACE1 interactions. Neurobiol. Aging, 2014, 35(8), 1801-1812.
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.02.005] [PMID: 24613671]
[137]
Marin, R.; Fabelo, N.; Martín, V.; Garcia-Esparcia, P.; Ferrer, I.; Quinto-Alemany, D.; Díaz, M. Anomalies occurring in lipid profiles and protein distribution in frontal cortex lipid rafts in dementia with Lewy bodies disclose neurochemical traits partially shared by Alzheimer’s and Parkinson’s diseases. Neurobiol. Aging, 2017, 49, 52-59.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.08.027] [PMID: 27768960]
[138]
Ariga, T. The pathogenic role of ganglioside metabolism in Alzheimer’s Disease-cholinergic neuron-specific gangliosides and neurogenesis. Mol. Neurobiol., 2017, 54(1), 623-638.
[http://dx.doi.org/10.1007/s12035-015-9641-0] [PMID: 26748510]
[139]
Marin, R.; Ramírez, C.; Morales, A.; González, M.; Alonso, R.; Díaz, M. Modulation of Abeta-induced neurotoxicity by estrogen receptor alpha and other associated proteins in lipid rafts. Steroids, 2008, 73(9-10), 992-996.
[http://dx.doi.org/10.1016/j.steroids.2007.12.007] [PMID: 18242653]
[140]
Canerina-Amaro, A.; Hernandez-Abad, L.G.; Ferrer, I.; Quinto-Alemany, D.; Mesa-Herrera, F.; Ferri, C.; Puertas-Avendano, R.A.; Diaz, M.; Marin, R. Lipid raft ER signalosome malfunctions in menopause and Alzheimer’s disease. Front. Biosci. (Schol. Ed.), 2017, 9, 111-126.
[http://dx.doi.org/10.2741/s476] [PMID: 27814578]
[141]
Wang, J.M.; Hou, X.; Adeosun, S.; Hill, R.; Henry, S.; Paul, I.; Irwin, R.W.; Ou, X.M.; Bigler, S.; Stockmeier, C.; Brinton, R.D.; Gomez-Sanchez, E. A dominant negative ERβ splice variant determines the effectiveness of early or late estrogen therapy after ovariectomy in rats. PLoS One, 2012, 7(3)e33493
[http://dx.doi.org/10.1371/journal.pone.0033493] [PMID: 22428062]
[142]
Bean, L.A.; Kumar, A.; Rani, A.; Guidi, M.; Rosario, A.M.; Cruz, P.E.; Golde, T.E.; Foster, T.C. Re-Opening the Critical Window for Estrogen Therapy. J. Neurosci., 2015, 35(49), 16077-16093.
[http://dx.doi.org/10.1523/JNEUROSCI.1890-15.2015] [PMID: 26658861]
[143]
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(10), 1121-1126.
[http://dx.doi.org/10.1016/j.bbagen.2010.06.002] [PMID: 20538040]
[144]
Yao, J.; Irwin, R.; Chen, S.; Hamilton, R.; Cadenas, E.; Brinton, R.D. Ovarian hormone loss induces bioenergetic deficits and mitochondrial β-amyloid. Neurobiol. Aging, 2012, 33(8), 1507-1521.
[http://dx.doi.org/10.1016/j.neurobiolaging.2011.03.001] [PMID: 21514693]
[145]
Yao, J.; Irwin, R.W.; Zhao, L.; Nilsen, J.; Hamilton, R.T.; Brinton, R.D. Mitochondrial bioenergetic deficit precedes Alzheimer’s pathology in female mouse model of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2009, 106(34), 14670-14675.
[http://dx.doi.org/10.1073/pnas.0903563106] [PMID: 19667196]
[146]
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(8), 1023-1027.
[http://dx.doi.org/10.1111/j.1365-2826.2008.01752.x] [PMID: 18540996]
[147]
Bekinschtein, P.; Cammarota, M.; Izquierdo, I.; Medina, J.H. BDNF and memory formation and storage. Neuroscientist, 2008, 14(2), 147-156.
[http://dx.doi.org/10.1177/1073858407305850] [PMID: 17911219]
[148]
Bekinschtein, P.; Cammarota, M.; Katche, C.; Slipczuk, L.; Rossato, J.I.; Goldin, A.; Izquierdo, I.; Medina, J.H. BDNF is essential to promote persistence of long-term memory storage. Proc. Natl. Acad. Sci. USA, 2008, 105(7), 2711-2716.
[http://dx.doi.org/10.1073/pnas.0711863105] [PMID: 18263738]
[149]
Bingham, D.; Macrae, I.M.; Carswell, H.V. Detrimental effects of 17beta-oestradiol after permanent middle cerebral artery occlusion. J. Cereb. Blood Flow Metab., 2005, 25(3), 414-420.
[http://dx.doi.org/10.1038/sj.jcbfm.9600031] [PMID: 15647739]
[150]
Dhandapani, K.M.; Wade, F.M.; Mahesh, V.B.; Brann, D.W. Astrocyte-derived transforming growth factor-beta mediates the neuroprotective effects of 17beta-estradiol: involvement of nonclassical genomic signaling pathways. Endocrinology, 2005, 146(6), 2749-2759.
[http://dx.doi.org/10.1210/en.2005-0014] [PMID: 15746252]
[151]
Galbiati, M.; Magnaghi, V.; Martini, L.; Melcangi, R.C. Hypothalamic transforming growth factor beta1 and basic fibroblast growth factor mRNA expression is modified during the rat oestrous cycle. J. Neuroendocrinol., 2001, 13(6), 483-489.
[http://dx.doi.org/10.1046/j.1365-2826.2001.00659.x] [PMID: 11412334]
[152]
Davies, P.; Maloney, A.J.F. Selective loss of central cholinergic neurons in Alzheimer’s disease., Lancet, 1976, 2(8000), 1403-1403.
[http://dx.doi.org/10.1016/S0140-6736(76)91936-X] [PMID: 63862]
[153]
Bowen, D.M.; Smith, C.B.; White, P.; Davison, A.N. Neurotransmitter-related enzymes and indices of hypoxia in senile dementia and other abiotrophies., Brain, 1976, 99(3), 459-496.
[http://dx.doi.org/10.1093/brain/99.3.459] [PMID: 11871]
[154]
Gritti, I.; Mainville, L.; Mancia, M.; Jones, B.E. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J. Comp. Neurol., 1997, 383(2), 163-177.
[http://dx.doi.org/10.1002/(SICI)1096-9861(19970630)383:2<163:AID-CNE4>3.0.CO;2-Z] [PMID: 9182846]
[155]
Mesulam, M.M.; Mufson, E.J.; Levey, A.I.; Wainer, B.H. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J. Comp. Neurol., 1983, 214(2), 170-197.
[http://dx.doi.org/10.1002/cne.902140206] [PMID: 6841683]
[156]
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(5), 477-485.
[http://dx.doi.org/10.1046/j.1365-2826.2003.01012.x] [PMID: 12694373]
[157]
Perry, E.K.; Perry, R.H.; Blessed, G.; Tomlinson, B.E. Necropsy evidence of central cholinergic deficits in senile dementia., Lancet, 1977, 1(8004), 189.
[http://dx.doi.org/10.1016/S0140-6736(77)91780-9] [PMID: 64712]
[158]
Whitehouse, P.J.; Price, D.L.; Struble, R.G.; Clark, A.W.; Coyle, J.T.; Delon, M.R. Alzheimer’s disease and senile dementia: loss of neurons in the basal forebrain. Science, 1982, 215(4537), 1237-1239.
[http://dx.doi.org/10.1126/science.7058341] [PMID: 7058341]
[159]
Schliebs, R.; Arendt, T. The significance of the cholinergic system in the brain during aging and in Alzheimer’s disease. J. Neural Transm. (Vienna), 2006, 113(11), 1625-1644.
[http://dx.doi.org/10.1007/s00702-006-0579-2] [PMID: 17039298]
[160]
van Amelsvoort, T.; Murphy, D.G.M.; Robertson, D.; Daly, E.; Whitehead, M.; Abel, K. Effects of long-term estrogen replacement therapy on growth hormone response to pyridostigmine in healthy postmenopausal women. Psychoneuroendocrinology, 2003, 28(1), 101-112.
[http://dx.doi.org/10.1016/S0306-4530(02)00012-4] [PMID: 12445839]
[161]
Craig, M.C.; Murphy, D.G. Estrogen therapy and Alzheimer’s dementia. Ann. N. Y. Acad. Sci., 2010, 1205, 245-253.
[http://dx.doi.org/10.1111/j.1749-6632.2010.05673.x] [PMID: 20840280]
[162]
Gibbs, R.B. Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr. Rev., 2010, 31(2), 224-253.
[http://dx.doi.org/10.1210/er.2009-0036] [PMID: 20019127]
[163]
Woolley, C.S. Effects of oestradiol on hippocampal circuitry. Novartis Found. Symp., 2000, 230, 173-180.
[PMID: 10965508]
[164]
Yankova, M.; Hart, S.A.; Woolley, C.S. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proc. Natl. Acad. Sci. USA, 2001, 98(6), 3525-3530.
[http://dx.doi.org/10.1073/pnas.051624598] [PMID: 11248111]
[165]
Toran-Allerand, C.D.; Miranda, R.C.; Bentham, W.D.; Sohrabji, F.; Brown, T.J.; Hochberg, R.B.; MacLusky, N.J. Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proc. Natl. Acad. Sci. USA, 1992, 89(10), 4668-4672.
[http://dx.doi.org/10.1073/pnas.89.10.4668] [PMID: 1316615]
[166]
Miranda, R.C.; Sohrabji, F.; Toran-Allerand, C.D. Presumptive estrogen target neurons express mrnas forboth the neurotrophins and neurotrophin receptors: A basis for potential developmental interactions of estrogen with the neurotrophins. Mol. Cell. Neurosci., 1993, 4(6), 510-525.
[http://dx.doi.org/10.1006/mcne.1993.1063] [PMID: 19912958]
[167]
Milne, M.R.; Haug, C.A.; Ábrahám, I.M.; Kwakowsky, A. Estradiol modulation of neurotrophin receptor expression in female mouse basal forebrain cholinergic neurons in vivo. Endocrinology, 2015, 156(2), 613-626.
[http://dx.doi.org/10.1210/en.2014-1669] [PMID: 25415243]
[168]
Kwakowsky, A.; Milne, M.R.; Waldvogel, H.J.; Faull, R.L. Effect of estradiol on neurotrophin receptors in basal forebrain cholinergic neurons: relevance for Alzheimer’s disease. Int. J. Mol. Sci., 2016, 17(12), 2122.
[http://dx.doi.org/10.3390/ijms17122122] [PMID: 27999310]

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