ESTROGENS AND BRAIN
- Authors: Kareva E.N.1, Oleynikova О.M.1, Panov V.O.1, Shimanovskiy N.L.1, Skvortsova V.I.1
-
Affiliations:
- Pirogov Russian National scientific medical university Ministry of Healthcare and Social Development of Russia, Moscow
- Issue: Vol 67, No 2 (2012)
- Pages: 48-59
- Section: ENDOCRINOLOGY: CURRENT ISSUES
- Published: 22.02.2012
- URL: https://vestnikramn.spr-journal.ru/jour/article/view/345
- DOI: https://doi.org/10.15690/vramn.v67i2.122
- ID: 345
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Abstract
About the authors
E. N. Kareva
Pirogov Russian National scientific medical university Ministry of Healthcare and Social Development of Russia, Moscow
Author for correspondence.
Email: elenakareva@mail.ru
доктор медицинских наук, профессор кафедры молекулярной фармакологии и радио- биологии имени академика П.В. Сергеева ГБОУ ВПО РНИМУ им. Н.И. Пирогова Минздравсоцразвития России Адрес: 117997, Москва, ул. Островитянова, д. 1 Тел.: (916) 579-55-93 Россия
О. M. Oleynikova
Pirogov Russian National scientific medical university Ministry of Healthcare and Social Development of Russia, Moscow
Email: oleynikova@mail.ru
кандидат медицинских наук, доцент кафедры неврологии и нейрохирургии с курсом ФУВ лечебного факультета ГБОУ ВПО РНИМУ им. Н.И. Пирогова Минздравсоцразвития России Адрес: 117049, Москва, Ленинский проспект, д. 8, кор. 8 Тел.: (499) 764-50-02 Россия
V. O. Panov
Pirogov Russian National scientific medical university Ministry of Healthcare and Social Development of Russia, Moscow
Email: nabirf@gmail.com
кандидат медицинских наук, главный научный сотрудник НИИ цереброваскулярной пато- логии и инсульта ГБОУ ВПО РНИМУ им. Н.И. Пирогова Минздравсоцразвития России Адрес: 117415, Москва, ул. Лобачевского, д. 42, кор. 6 Тел.: (495) 432-97-34 Россия
N. L. Shimanovskiy
Pirogov Russian National scientific medical university Ministry of Healthcare and Social Development of Russia, Moscow
Email: shiman@rsmu.ru
член-корреспондент РАМН, профессор, заведующий кафедрой молекулярной фармакологии и радиобиологии имени академика П.В. Сергеева ГБОУ ВПО РНИМУ им. Н.И. Пирогова Минздравсоцразвития России Адрес: 119121, ул. Б. Пироговская, д. 9а Тел.: (499) 246-60-05 Россия
V. I. Skvortsova
Pirogov Russian National scientific medical university Ministry of Healthcare and Social Development of Russia, Moscow
Email: nabirf@gmail.com
доктор медицинских наук, профессор, заведующая кафедрой фундаментальной и кли- нической неврологии и нейрохирургии ГБОУ ВПО РНИМУ им. Н.И. Пирогова Минздравсоцразвития России Адрес: 117415, Москва, ул. Лобачевского, д. 42, кор. 6 Тел.: (495) 432-97-34 Россия
References
- Heldring N., Pike A., Andersson S. et al. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 2007; 87 (3): 905−931.
- Delaunay F., Pettersson K., Tujague M., Gustafsson J.A. Functional differences between the amino-terminal domains of estrogen receptors alpha and beta. Mol. Pharmacol. 2000; 58 (3): 584−590.
- Prokai L., Simpkins J.W. Structure ― non-genomic neuroprotection relationship of estrogens and estrogen-derived compounds. Pharmacol. Ther. 2007; 114 (1): 1–12.
- Dahlman-Wright K., Cavailles V., Fuqua S.A. et al. International Union of Pharmacology. LXIV. Estrogen receptors. Pharmacol. Rev. 2006; 58 (4): 773−781.
- Safe S. Transcriptional activati on of genes by 17 beta-estradiol through estrogen receptor-Sp1 interactions. Vitam. Horm. 2001; 62: 231−252.
- Choudhry M.A., Bland K.I., Chaudry I.H. Trauma and immune response ― effect of gender differences. Injury. 2007; 38 (12): 1382−1391.
- Sergeev P.V., Denisov Yu.P., Suleimanov S.Sh. Farmakologiya i toksikologiya = Pharmacology and toxicology. 1981; 4: 429−432.
- Rozen V.B. Osnovy endokrinologii [Basics of Endocrinology]. Moscow, MGU. 1994. 384 p.
- Sergeev P.V., Shimanovskii N.L., Petrov V.I. Retseptory fiziologicheski aktivnykh veshchestv [Receptors of physiologically active substances]. Moscow, Volgograd, 1999.
- Kan A.M., Matyushin A.I. Problemy endokrinologii = Problems of endocrinology. 1991: 53−54.
- Luoma J.I., Boulware M.I., Mermelstein P.G. Caveolin proteins and estrogen signaling in the brain. Mol. Cell Endocrinol. 2008; 290 (1−2): 8–13.
- Micevych P., Kuo J., Christensen A. Physiology of Membrane Estrogen Receptor Signaling in Reproduction. J. Neuroendocrinol. 2009; 21 (4): 249–256.
- Maggiolini M., Picard D. The unfolding stories of GPR30, a new membrane-bound estrogen receptor. Endocrinol. 2010; 204: 105−114.
- Pandey D.P., Lappano R., Albanito L. et al. Estrogenic GPR30 signalling induces proliferation and migration of breast cancer cells through CTGF. EMBO J. 2009; 28 (5): 523–532.
- Shughrue P.J., Scrimo P.J., Merchenthaler I. Evidence for the colocalization of estrogen receptor-beta mRNA and estrogen receptor-alpha immunoreactivity in neurons of the rat forebrain. Endocrinology. 1998; 139: 5267–5270.
- Milner T.A., Ayoola K., Drake C.T. et al. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 2005; 491: 81–95.
- Perlman W.R., Tomaskovic-Crook E., Montague D.M. et al. Alteration in estrogen receptor alpha mRNA levels in frontal cortex and hippocampus of patients with major mental illness. Biol. Psychiatry. 2005; 58 (10): 812−824.
- Hajszan T., Milner T.A., Leranth C. Sex steroids and the dentate gyrus. Progr. Brain. Res. 2007; 163: 399–416.
- Micevych P., Sinchak K. Estradiol regulation of progesterone synthesis in the brain. Mol. Cell Endocrinol. 2008; 290 (1–2): 44–50.
- Ramachandran S., Kwon K.Y., Shin S.J. et al. Cyclin-dependent kinase inhibitor p27 Kip1 controls growth and cell cycle progression in human uterine leiomyoma. Korean. Med. Sci. 2008; 23 (4): 667–673.
- Chambliss K.L., Yuhanna I.S., Mineo C. et al. Estrogen receptor alpha and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circ. Res. 2000; 87 (11): 44–52.
- Mermelstein P.G. Membrane-localised oestrogen receptor alpha and beta influence neuronal activity through activation of metabotropic glutamate receptors. Neuroendocrinol. 2009; 21 (4): 257–262.
- Morissette M., Le Saux M., D'Astous M. et al. Contribution of estrogen receptors alpha and beta to the effects of estradiol in the brain. J. Steroid. Biochem. Mol. Biol. 2008; 108 (3–5): 327–338.
- Cyr M., Thibault C., Morissette M. et al. Estrogen-like activity of tamoxifen and raloxifene on NMDA receptor binding and expression of its subunits in rat brain. Neuropsychopharmacology. 2001; 25 (2): 242−257.
- Hudgens E.D., Ji L., Clifford D. et al. The gad2 promoter is a transcriptional target of estrogen receptor α (ERα) and ERβ: A unifying hypothesis to explain diverse effects of estradiol. Neurosci. 2009; 29 (27): 8790–8797.
- Xu S., Cheng Y., Keast J.R., Osborne P.B. 17β-Estradiol Activates Estrogen Receptor β-Signalling and Inhibits Transient Receptor Potential Vanilloid Receptor 1 Activation by Capsaicin in Adult Rat Nociceptor Neurons. Endocrinology. 2008; 149 (11): 5540–5548.
- Kuhn J., Dina O.A., Goswami C. et al. GPR30 estrogen receptor agonists induce mechanical hyperalgesia in the rat. Eur. J. Neurosci. 2008; 27 (7): 1700−9.
- Alyea R.A., Watson C.S. Nongenomic mechanisms of physiological estrogen-mediated dopamine efflux. BMC Neurosci. 2009; 10: 59. Available at: http://www.biomedcentral.com/1471-2202/10/59
- Xu H., Qin S., Carrasco G.A. et al. Extra-nuclear estrogen receptor GPR30 regulates serotonin function in rat hypothalamus. Neurosci. 2009; 158: 1599–1607.
- Holton K.L., Loder M.K., Melikian H.E. Nonclassical, distinct endocytic signals dictate constitutive and PKC-regulated neurotransmitter transporter internalization. Nat. Neurosci. 2005; 8: 881–888.
- Watson C.S., Alyea R.A., Hawkins B.E. et al. Estradiol effects on the dopamine transporter ― protein levels, subcellular location, and function. J. Mol. Signal. 2006; 1: 5.
- Dennis M.K., Burai R., Ramesh C. et al. In vivo effects of a GPR30 antagonist. Nat. Chem. Biol. 2009; 5: 421–427.
- Krejza J., Mariak Z., Nowacka A. et al. Influence of 17-beta-estradiol on cerebrovascular impedance during menstrual cycle in women. J. Neurol. Sci. 2004; 221: 61–67.
- Krause D.N., Sue P. Duckles, Dale A. Pelligrino nfluence of sex steroid hormones on cerebrovascular function. J. Appl. Physiol. 2006; 101: 1252−1261.
- Shearman A.M., Cooper J.A., Kotwinski P.J. et al. Estrogen receptor alpha gene variation and the risk of stroke. Stroke. 2005; 36 (10): 2281−2.
- Johnson M.P., Fernandez F., Colson N.J., Griffiths L.R. A pharmacogenomic evaluation of migraine therapy. Expert. Opin. Pharmacother. 2007; 8 (12): 1821−1835.
- Miller V.M., Duckles S.P. Vascular Actions of Estrogens: Functional Implications. Pharmacol. Rev. 2008; 60 (2): 210–241.
- Tsang S.Y., Yao X., Essin K. et al. Raloxifene relaxes rat cerebral arteries in vitro and inhibits L-type voltage-sensitive Ca2+ channels. Stroke. 2004; 35: 1709–1714.
- Ospina J.A., Duckles S.P., Krause D.N. 17b-Estradiol decreases vascular tone in cerebral arteries by shifting COX-dependent vasoconstriction to vasodilation. Am. J. Physiol. Heart Circ. Physiol. 2003; 285: 241–250.
- Sunday L., Ospina J., Krause D.N., Duckles S.P. Estrogen modifies cerebral vascular inflammation. Stroke. 2004; 35: 249.
- Gonzales R.J., Ansar S., Duckles S.P., Krause D.N. Androgenic/estrogenic balance in the male rat cerebral circulation: metabolic enzymes and sex steroid receptors. J. Cereb. Blood Flow Metab. 2007; 27 (11): 1841–1852.
- Chrissobolis S., Budzyn K., Marley P.D., Sobey C.G. Evidence that estrogen suppresses rho-kinase function in the cerebral circulation in vivo. Stroke. 2004; 35: 2200–2205.
- Stirone C., Duckles S.P., Krause D.N., Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol. Pharmacol. 2005; 68: 959–965.
- Simpkins J.W., Wang J., Wang X. et al. Mitochondria play a central role in estrogen-induced neuroprotection. Curr Drug Targets CNS. Neurol. Disord. 2005; 4: 69–83.
- Liu R., Liu Q., He S. et al. Combination Therapy of 17-beta-Estradiol and Recombinant Tissue Plasminogen Activator for Experimental Ischemic Stroke J. Pharmacol. 2010; 332 (3): 1006– 1012.
- Shi J., Simpkins J.W. 17b-Estradiol modulation of glucose transporter 1 expression in blood-brain barrier. Am. J. Physiol. Endocrinol. Metab. 1997; 272: 1016–1022.
- Kanda N., Watanabe S. 17b-Estradiol enhances the production of nerve growth factor in THP-1- or peripheral blood monocyte-derived macrophages. J. Invest Dermatol. 2003; 121: 771–780.
- Sato T., Teramoto T., Tanaka K. et al. Effects of ovariectomy and calcium deficiency on learning and memory of eight-arm radial maze in middle-aged female rats. Behav. Brain Res. 2003; 142: 207–216.
- Gibson C.L., Gray L.J., Murphy S.P., Bath P.M. Estrogens and experimental ischemic stroke: a systematic review. J. Cereb. Blood Flow Metab. 2006; 26 (9фф): 1103−13.
- Nunez J., Zhengang Y., Yuhui J. et al. 17b-Estradiol Protects the Neonatal Brain from Hypoxia-Ischemia. Exp. Neurol. 2007; 208 (2): 269–276.
- Wang C., Dehghani B., Magrisso I.J. et al. GPR30 contributes to estrogen-induced thymic atrophy. Mol. Endocrinol. 2008; 22: 636–648.
- Alonso A., Jick S.S., Olek M.J. et al. Recent use of oral contraceptives and the risk of multiple sclerosis. Arch. Neurol. 2005; 62 (9): 1362.
- Smith R.G., Betancourt L., Sun Y. Molecular Endocrinology and Physiology of the Aging Central Nervous System Endocrine Reviews. 2005; 26 (2): 203−250.
- Gerstner B., Sifringer M., Dzietko M. et al. Estradiol attenuates hyperoxia-induced cell death in the developing white matter. Ann. Neurol. 2007; 61: 562–573.
- Westberry J.M., Prewitt A.K., Wilson M.E. Epigenetic regulation of the estrogen receptor alpha promoter in the cerebral cortex following ischemia in male and female rats. Neuroscience. 2008; 152 (4): 982–989.
- Wang L. et al. Murphy Estradiol attenuates neuroprotective benefits of isoflurane preconditioning in ischemic mouse brain. J. Cereb. Blood Flow Metab. 2008; 28 (11): 1824–1834.
- Fox E.M., Andrade J., Shupnik M.A. Novel actions of estrogen to promote proliferation. Steroids. 2009; 74 (7): 622−627.
- Nicholls D.G., Budd S.L. Mitochondria and neuronal survival. Physiol. Rev. 2000; 80: 315–360.
- Wallace D.C. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Ann. Rev. Genet. 2005; 39: 359–407.
- Chen J.Q., Yager J.D. Estrogen's effects on mitochondrial gene expression: mechanisms and potential contributions to estrogen carcinogenesis. Ann. NY Acad. Sci. 2004; 1028: 258−272.
- Irwin R.W., Yao J., Hamilton R.T. et al. Progesterone and Estrogen Regulate Oxidative Metabolism in Brain Mitochondria. Endocrinology. 2008; 149 (6): 3167–3175.
- Razmara A. et al. Estrogen Suppresses Brain Mitochondrial Oxidative Stress in Female and Male Rats. Brain Res. 2007; 1176: 71–81.
- Zheng J., Ramirez V.D. Purification and identification of an estrogen binding protein from rat brain: oligomycin sensitivity-conferring protein (OSCP), a subunit of mitochondrial F0F1-ATP synthase/ATPase. J. Steroid Biochem Mol. Biol. 1999; 68: 65–75.
- St-Pierre J. et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 2006; 127: 397–408.
- Nilsen J. et al. Estrogen protects neuronal cells from amyloid beta-induced apoptosis via regulation of mitochondrial proteins and function. BMC Neurosci. 2006; 7: 74.
- Fowler C.D. Estrogen and adult neurogenesis in the amygdala and hypothalamus. Brain Res. Rev. 2008; 57 (2): 342–351.
- Ray R., Novotny N.M., Crisostomo P.R. et al. Sex Steroids and Stem Cell Function. Mol. Med. 2008; 14 (7−8): 493–501.
- Jezierski M.K., Sohrabji F. Region- and peptide-specific regulation of the neurotrophins by estrogen. Mol. Brain Res. 2000; 85: 75–84.
- Pencea V., Bingaman K.D., Wiegand S.J., Luskin M.B. Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J. Neurosci. 2001; 21: 6706–671.
- Kokoeva M.V., Yin H., Flier J.S. Neurogenesis in the hypothalamus of adult mice: Potential role in energy balance. Science. 2005; 310: 679–683.
- Jover T., Tanaka H., Calderone A. et al. Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. J. Neurosci. 2002; 22: 2115–24.
- Meltser I., Tahera Y., Simpson E. et al. Estrogen receptor β protects against acoustic trauma in mice. J. Clin. Invest. 2008; 118 (4): 1563–1570.
- Mohapel P., Leanza G., Kokaia M., Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol. Aging. 2005; 26 (6): 939−946.
- Jacobs B.L., Praag H., Gage F.H. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol. Psychiatry. 2000; 5: 262–269.
- Szymczak S., Kalita K., Jaworski J. et al. Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus. Hippocampus. 2006; 16 (5): 453−463.
- Liu L., Kim J.Y., Koike M.A. et al. FasL shedding is reduced by hypothermia in experimental stroke. J. Neurochem. 2008; 106 (2): 541–550.
- Jamous M.A., Nagahiro S., Kitazato K.T. et al. Role of estrogen deficiency in the formation and progression of cerebral aneurysms. Part II: experimental study of the effects of hormone replacement therapy in rats. J. Neurosurg. 2005; 103: 1052–1057.
- Ardelt A.A., McCullough L.D., Korach K.S. et al. Estradiol regulates angiopoietin-1 mRNA expression through estrogen receptor-alpha in a rodent experimental stroke model. Stroke. 2005; 36: 337–341.
- Lu A., Ran R.Q., Clark J. et al. 17-beta-estradiol induces heat shock proteins in brain arteries and potentiates ischemic heat shock protein induction in glia and neurons. J. Cereb. Blood Flow Metab. 2002; 22: 183–195.
- Dietrich J.B. Endothelial cells of the blood-brain barrier: a target for glucocorticoids and estrogens? Front Biosci. 2004; 9: 684–693.
- Voumvourakis K.I., Kitsos T.S., Stamboulis E. Gender hormones: role in the pathogenesis of central nervous system disease and demyelination. Curr. Neurovasc Res. 2008; 5 (4): 224–35.
- Cvoro A., Tatomer D., Tee M.K. et al. Selective estrogen receptor-beta agonists repress transcription of proinflammatory genes. Immunol. 2008; 180: 630–636.
- Vegeto E., Belcredito S., Etteri S. et al. Estrogen receptor-alpha mediates the brain anti-inflammatory activity of estradiol. Proc. Natl. Acad. Sci USA. 2004; 101: 9614–9619.
- Ghisletti S., Meda C., Maggi A., Vegeto E. 17 beta-estradiol inhibits inflammatory gene expression by controlling NF-kappa B intracellular localization. Mol. Cell Biol. 2005; 25: 2957–2968.
- Garidou L., Laffont S., Douin-Echinard V. et al. Estrogen Receptor alfa Signaling in Inflammatory Leukocytes Is Dispensable for 17beta-Estradiol-Mediated Inhibition of Experimental Autoimmune Encephalomyelitis. The Journal of Immunology. 2004; 173: 2435–2442.
- Alt C., Laschinger M., Engelhardt B. Functional expression of the lymphoid chemokines CCL19 (ELC) and CCL 21 (SLC) at the blood-brain barrier suggests their involvement in G-protein-dependent lymphocyte recruitment into the central nervous system during experimental autoimmune encephalomyelitis. Eur. J. Immunol. 2002; 32: 2133.
- Rossouw J.E., Anderson G.L., Prentice R.L. et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA. 2002; 288: 321–333.