Estrogen receptor agonists for attenuation of neuroinflammation and neurodegeneration

Brain Research Bulletin

Volumn 109, Issue , 2014, Pages 22-31

  Chakrabarti, Mrinmay ^a   Haque, Azizul ^b   Banik, Naren L ^b   Nagarkatti, Prakash ^a   Nagarkatti, Mitzi ^a   Ray, Swapan K ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Estrogen receptor agonists; Inflammation; Neurodisorders; Neuroprotection

Indexed keywords

17ALPHA ESTRADIOL; AFIMOXIFENE; ARZOXIFENE; BAZEDOXIFENE; COUMESTROL; DAIDZEIN; DROLOXIFENE; EQUILIN; EQUOL; ESTRADIOL; ESTRIOL; ESTROGEN RECEPTOR AGONIST; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FORMONONETIN; GENISTEIN; HORMONE RECEPTOR STIMULATING AGENT; LASOFOXIFENE; OSPEMIFENE; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN; UNCLASSIFIED DRUG; ESTROGEN; NEUROPROTECTIVE AGENT;

ALZHEIMER DISEASE; ANTIINFLAMMATORY ACTIVITY; ASTROCYTE; AXONAL INJURY; BRAIN ISCHEMIA; CELL ACTIVATION; CELL POPULATION; CELL SURVIVAL; COGNITION; DEGENERATIVE DISEASE; DISEASE COURSE; DRUG MECHANISM; HUMAN; MICROGLIA; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; PARKINSON DISEASE; REVIEW; SPINAL CORD INJURY; TRAUMATIC BRAIN INJURY; ANIMAL; DRUG EFFECTS; ENCEPHALITIS; NEURODEGENERATIVE DISEASES; SIGNAL TRANSDUCTION;

ANIMALS; ENCEPHALITIS; ESTROGENS; HUMANS; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; SIGNAL TRANSDUCTION;

EID: 84908332986     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2014.09.004     Document Type: Review

References (176)

1. Abdelhamid R., Luo J., Vandevrede L., Kundu I., Michalsen B., Litosh V.A., Schiefer I.T., Gherezghiher T., Yao P., Qin Z., Thatcher G.R. Benzothiophene selective estrogen receptor modulators provide neuroprotection by a novel GPR30-dependent mechanism. ACS Chem. Neurosci. 2011, 2:256-268.
2. Agrawal S.K., Nashmi R., Fehlings M.G. Role of L- and N-type calcium channels in the pathophysiology of traumatic spinal cord white matter injury. Neuroscience 2000, 99:179-188.
3. Arevalo M.A., Diz-Chaves Y., Santos-Galindo M., Bellini M.J., Garcia-Segura L.M. Selective oestrogen receptor modulators decrease the inflammatory response of glial cells. J. Neuroendocrinol. 2012, 24:183-190.
4. Azcoitia I., Moreno A., Carrero P., Palacios S., Garcia-Segura L.M. Neuroprotective effects of soy phytoestrogens in the rat brain. Gynecol. Endocrinol. 2006, 22:63-69.
5. Baldereschi M., Di Carlo A., Rocca W.A., Vanni P., Maggi S., Perissinotto E., Grigoletto F., Amaducci L., Inzitari D. Parkinson's disease and Parkinsonism in a longitudinal study: two-fold higher incidence in men. ILSA Working Group. Italian Longitudinal Study on Aging. Neurology 2000, 55:1358-1363.
6. + channel function in cerebral arterioles in piglets. Stroke 1996, 27:1874-1880.
7. Barkhem T., Carlsson B., Nilsson Y., Enmark E., Gustafsson J., Nilsson S. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol. Pharmacol. 1998, 54:105-112.
8. Barreto G., Santos-Galindo M., Diz-Chavez Y., Pernia O., Carrero P., Azcoitia I., Garcia-Segura L.M. Selective estrogen receptor modulators decrease reactive astrogliosis in the injured brain: effects of aging prolonged depletion of ovarian hormones. Endocrinology 2009, 150:5010-5015.
9. Barrett-Connor E., Bush T.L. Estrogen and coronary heart disease in women. J. Am. Med. Assoc. 1991, 265:1861-1867.
10. Bayir H., Marion D.W., Puccio A.M., Wisniewski S.R., Janesko K.L., Clark R.S., Kochanek P.M. Marked gender effect on lipid peroxidation after severe traumatic brain injury in adult patients. J. Neurotrauma 2004, 21:1-8.
11. Bebo B.F., Fyfe-Johnson A., Adlard K., Beam A.G., Vandenbark A.A., Offner H. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J. Immunol. 2001, 166:2080-2089.
12. Behl C., Widmann M., Trapp T., Holsboer F. 17-β estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem. Biophys. Res. Commun. 1995, 216:473-482.
13. Blanchet P.J., Fang J., Hyland K., Arnold L.A., Mouradian M.M., Chase T.N. Short-term effects of high-dose 17β-estradiol in postmenopausal PD patients: a crossover study. Neurology 1999, 53:91-95.
14. Bolger R., Wiese T.E., Ervin K., Nestich S., Checovich W. Rapid screening of environmental chemicals for estrogen receptor binding capacity. Environ. Health Perspect. 1998, 106:551-555.
15. Bourque M., Dluzen D.E., Di Paolo T. Signaling pathways mediating the neuroprotective effects of sex steroids and SERMs in Parkinson's disease. Front. Neuroendocrinol. 2012, 33:169-178.
16. Bower J.H., Maraganore D.M., McDonnell S.K., Rocca W.A. Incidence and distribution of Parkinsonism in Olmsted County, Minnesota, 1976-1990. Neurology 1999, 52:1214-1220.
17. Bower J.H., Maraganore D.M., McDonnell S.K., Rocca W.A. Influence of strict, intermediate, and broad diagnostic criteria on the age- and sex-specific incidence of Parkinson's disease. Mov. Disord. 2000, 15:819-825.
18. Brinton R.D. Requirements of a brain selective estrogen: advances and remaining challenges for developing a NeuroSERM. J. Alzheimers Dis. 2004, 6:S27-S35.
19. Brzozowski F.A.M., Pike A.C., Dauter Z., Hubbard R.E., Bonn T., Engstrom O., Ohman L., Greene G.L., Gustafsson J.A., Carlquist M. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997, 389:753-758.
20. Cadet K., Ladenheim B., Baum I., Carlson E., Epstein C. Cu,Zn-superoxide dismutase (CuZnSOD) transgenic mice show resistance to the lethal effects of methylenedioxyamphetamine (MDA) and of methylenedioxymethamphetamine (MDMA). Brain Res. 1994, 655:259-262.
21. Carlson S.L., Parrish M.E., Springer J.E., Doty K., Dossett L. Acute inflammatory response in spinal cord following impact injury. Exp. Neurol. 1998, 151:77-88.
22. Carswell H.V.O., Anderson N.H., Clark J.S., Graham D., Jeffs B., Dominizak A.F., Macrae I.M. Genetic and gender influences on sensitivity to focal cerebral ischemia in the stroke-prone SHR. Hypertension 1999, 33:681-685.
23. +-ATPase inhibition and affords histological neuroprotection to male rats receiving cerebral global ischemia. Neurol. Res. 2014, 36:198-206.
24. Castro S.B., Junior C.O., Alves C.C., Dias A.T., Alves L.L., Mazzoccoli L., Mesquita F.P., Figueiredo N.S., Juliano M.A., Castañon M.C., Gameiro J., Almeida M.V., Teixeira H.C., Ferreira A.P. Immunomodulatory effects and improved prognosis of experimental autoimmune encephalomyelitis after O-tetradecanoyl-genistein treatment. Int. Immunopharmacol. 2012, 12:465-470.
25. Cerciat M., Unkila M., Garcia-Segura L.M., Arevalo M.A. Selective estrogen receptor modulators decrease the production of interleukin-6 and interferon-γ-inducible protein-10 by astrocytes exposed to inflammatory challenge in vitro. Glia 2010, 58:93-102.
26. Chakrabarti M., Banik N.L., Ray S.K. miR-7-1 potentiated estrogen receptor agonists for functional neuroprotection in VSC4.1 motoneurons. Neuroscience 2014, 256:322-333.
27. Christian M.S. Introduction/overview: gender-based differences in pharmacologic and toxicologic responses. Int. J. Toxicol. 2001, 20:145-148.
28. Cipolla M.J., Bullinger L.V. Reactivity of brain parenchymal arterioles after ischemia and reperfusion. Microcirculation 2008, 15:495-501.
29. Corder E.H., Ghebremedhin E., Taylor M.G., Thal D.R., Ohm T.G., Braak H. The biphasic relationship between regional brain senile plaque and neurofibrillary tangle distributions: modification by age, sex, and APOE polymorphism. Ann. N. Y. Acad. Sci. 2004, 1019:24-28.
30. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us. Endocr. Rev. 1999, 20:358-417.
31. Crocker S.J., Smith P.D., Jackson-Lewis V., Lamba W.R., Hayley S.P., Grimm E., Callaghan S.M., Slack R.S., Melloni E., Przedborski S., Robertson G.S., Anisman H., Merali Z., Park D.S. Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J. Neurosci. 2003, 23:4081-4091.
32. Currie L.J., Harrison M.B., Trugman J.M., Bennett J.P., Wooten G.F. Postmenopausal estrogen use affects risk for Parkinson disease. Arch. Neurol. 2004, 61:886-888.
33. Das A., Sribnick E.A., Wingrave J.M., Del Re A.M., Woodward J.J., Appel S.H., Banik N.L., Ray S.K. Calpain activation in apoptosis of ventral spinal cord 4.1 (VSC4.1) motoneurons exposed to glutamate: calpain inhibition provides functional neuroprotection. J. Neurosci. Res. 2005, 81:551-562.
34. de Rijk M.C., Breteler M.M., Graveland G.A., Ott A., Grobbee D.E., van der Meche F.G., Hofman A. Prevalence of Parkinson's disease in the elderly: the Rotterdam Study. Neurology 1995, 45:2143-2146.
35. Dhillon H.S., Carman H.M., Prasad R.M. Regional activities of phospholipase C after experimental brain injury in the rat. Neurochem. Res. 1999, 24:751-755.
36. Dimayuga F.O., Reed J.L., Carnero G.A., Wang C., Dimayuga E.R., Dimayuga V.M., Perger A., Wilson M.E., Keller J.N., Bruce-Keller A.J. Estrogen and brain inflammation: effects on microglial expression of MHC, co-stimulatory molecules and cytokines. J. Neuroimmunol. 2005, 161:123-136.
37. Do Y., Ryu S., Nagarkatti M., Nagarkatti P.S. Role of death receptor pathway in estradiol-induced T-cell apoptosis in vivo. Toxicol. Sci. 2002, 70:63-72.
38. 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, 18:1253-1258.
39. Dubal D.B., Zhu H., Yu J., Rau S.W., Shughrue P.J., Merchenthaler I., Kindy M.S., Wise P.M. Estrogen receptor α, not β, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1952-1957.
40. Dumitriu D., Rapp P.R., McEwen B.S., Morrison J.H. Estrogen and the aging brain: an elixir for the weary cortical network. Ann. N. Y. Acad. Sci. 2010, 1204:104-112.
41. Enmark E., Pelto-Huikko M., Grandien K., Lagercrantz S., Lagercrantz J., Fried G., Nordenskjold M., Gustafsson J.A. Human estrogen receptor beta-gene structure, chromosomal localization, expression pattern. J. Clin. Endocrinol. Metab. 1997, 82:4258-4265.
42. Flohé S.B., Agrawal H., Flohé S., Rani M., Bangen J.M., Schade F.U. Diversity of interferon gamma and granulocyte-macrophage colony-stimulating factor in restoring immune dysfunction of dendritic cells and macrophages during polymicrobial sepsis. Mol. Med. 2008, 14:247-256.
43. Giladi N., Honigman S. Hormones and Parkinson's disease. Neurology 1995, 45:1028-1029.
44. Green P.S., Simpkins J.W. Neuroprotective effects of estrogens: potential mechanisms of action. Int. J. Dev. Neurosci. 2000, 18:347-358.
45. Gronemeyer H., Gustafsson J.A., Laudet V. Principles for modulation of the nuclear receptor superfamily. Nat. Rev. Drug Discov. 2004, 3:950-964.
46. Haas E., Meyer M.R., Schurr U., Bhattacharya I., Minotti R., Nguyen H.H., Heigl A., Lachat M., Genoni M., Barton M. Differential effects of 17β-estradiol on function and expression of estrogen receptor alpha, estrogen receptor beta, and GPR30 in arteries and veins of patients with atherosclerosis. Hypertension 2007, 49:1358-1363.
47. Hall E.D., Sutter D.M. Gender differences in infarct size in mice after permanent focal ischemia and in the protective effects of Cu-Zn superoxide dismutase over expression. Annual Meeting of the Society of Neuroscience 1998.
48. Hart S.A., Patton J.D., Woolley C.S. Quantitative analysis of ERα and GAD colocalization in the hippocampus of the adult female rat. J. Comp. Neurol. 2001, 440:144-155.
49. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., Tujague M., Ström A., Treuter E., Warner M., Gustafsson J.A. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 2007, 87:905-931.
50. Henderson V.W., Paganini-Hill A., Emanuel C.K., Dunn M.E., Buckwalter J.G. Estrogen replacement therapy in older women. Comparisons between Alzheimer's disease cases and nondemented control subjects. Arch. Neurol. 1994, 51:896-900.
51. Herrera J.L., Fernandez C., Diaz M., Cury D., Marin R. Estradiol and tamoxifen differentially regulate a plasmalemmal voltage-dependent anion channel involved in amyloid-beta induced neurotoxicity. Steroids 2011, 76:840-844.
52. Hornykiewicz O. The neurochemical basis of the pharmacology of Parkinson's disease. Handbook of Experimental Pharmacology 1989, 185-204. Springer Verlag, New York. D.B. Calne (Ed.).
53. Hossmann K.A. Pathophysiology and therapy of experimental stroke. Cell. Mol. Neurobiol. 2006, 26:1057-1083.
54. Hurn P.D., Macrae I.M. Estrogen as a neuroprotectant in stroke. J. Cereb. Blood Flow Metab. 2000, 20:631-652.
55. Hurtado O., Ballesteros I., Cuartero M.I., Moraga A., Pradillo J.M., Ramírez-Franco J., Bartolomé-Martín D., Pascual D., Torres M., Sánchez-Prieto J., Salom J.B., Lizasoain I., Moro M.A. Daidzein has neuroprotective effects through ligand-binding-independent PPARγ activation. Neurochem. Int. 2012, 61:119-127.
56. Ishunina T.A., Sluiter A.A., Swaab D.F., Verwer R.W. Transcriptional activity of human brain estrogen receptor-α splice variants: evidence for cell type-specific regulation. Brain Res. 2013, 1500:1-9.
57. Ito A., Bebo B.F., Matejuk A., Zamora A., Silverman M., Fyfe-Johnson A., Offner H. Estrogen treatment down-regulates TNF-alpha production and reduces the severity of experimental autoimmune encephalomyelitis in cytokine knockout mice. J. Immunol. 2001, 167:542-552.
58. Jackman K.A., Woodman O.L., Chrissobolis S., Sobey C.G. Vasorelaxant and antioxidant activity of the isoflavone metabolite equol in carotid and cerebral arteries. Brain Res. 2007, 1141:99-107.
59. Jensen E.V. On the mechanism of estrogen action. Perspect. Biol. Med. 1962, 6:47-59.
60. Jorm A.F., Korten A.E., Henderson A.S. The prevalence of dementia: a quantitative integration of the literature. Acta Psychiatr. Scand. 1987, 76:465-479.
61. 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, 22:2115-2124.
62. Jung M.E., Wilson A.M., Simpkins J.W. A nonfeminizing estrogen analog protects against ethanol withdrawal toxicity in immortalized hippocampal cells. J. Pharmacol. Exp. Ther. 2006, 319:543-550.
63. Kassi E., Moutsatsou P. Estrogen receptor signaling and its relationship to cytokines in systemic lupus erythematosus. J. Biomed. Biotechnol. 2010, 2010:317452.
64. Katzenellenbogen B.S., Katzenellenbogen J.A. Biomedicine. Defining the "S" in SERMs. Science 2002, 295:2380-2381.
65. Kawas C., Resnick S., Morrison A., Brookmeyer R., Corrada M., Zonderman A., Bacal C., Donnell Lingle D., Metter E. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore Longitudinal Study of Aging. Neurology 1997, 48:1517-1521.
66. Kim H., Bang O.Y., Jung M.W., Ha S.D., Hong H.S., Huh K., Kim S.U., Mook-Jung I. Neuroprotective effects of estrogen against beta-amyloid toxicity are mediated by estrogen receptors in cultured neuronal cells. Neurosci. Lett. 2001, 302:58-62.
67. Kim S., Liva S.M., Dalal M.A., Verity M.A., Voskuhl R.R. Estriol ameliorates autoimmune demyelinating disease: implications for multiple sclerosis. Neurology 1999, 52:1230-1280.
68. Kokiko O.N., Murashov A.K., Hoane M.R. Administration of raloxifene reduces sensorimotor and working memory deficits following traumatic brain injury. Behav. Brain Res. 2006, 170:233-240.
69. Kosaka Y., Quillinan N., Bond C., Traystman R., Hurn P., Herson P. GPER1/GPR30 activation improves neuronal survival following global cerebral ischemia induced by cardiac arrest in mice. Transl. Stroke Res. 2012, 3:500-507.
70. Krege J.H., Hodgin J.B., Couse J.F., Enmark E., Warner M., Mahler J.F., Sar M., Korach K.S., Gustafsson J.A., Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15677-15682.
71. Kritzer M.F. Regional, laminar, and cellular distribution of immunoreactivity for ER alpha and ER beta in the cerebral cortex of hormonally intact, adult male and female rats. Cereb. Cortex 2002, 12:116-128.
72. Kulkarni J., Gavrilidis E., Worsley R., Van Rheenen T., Hayes E. The role of estrogen in the treatment of men with schizophrenia. Int. J. Endocrinol. Metab. 2013, 11:129-136.
73. Kushwaha A.K., Vuddanda P.R., Karunanidhi P., Singh S.K., Singh S. Development and evaluation of solid lipid nanoparticles of raloxifene hydrochloride for enhanced bioavailability. Biomed. Res. Int. 2013, 2013:584549.
74. Lai K., Cui J., Ni S., Zhang Y., He J., Yao K. The effects of postmenopausal hormone use on cataract: a meta-analysis. PLOS ONE 2013, 8:e78647.
75. Launer L.J., Andersen K., Dewey M.E., Letenneur L., Ott A., Amaducci L.A., Brayne C., Copeland J.R., Dartigues J.F., Kragh- Sorensen P., Lobo A., Martinez-Lage J.M., Stijnen T., Hofman A. Rates and risk factors for dementia and Alzheimer's disease: results from EURODEM pooled analyses. EURODEM Incidence Research Group and Work Groups. European Studies of Dementia. Neurology 1999, 52:78-84.
76. Lee J.H., Jiang Y., Han D.H., Shin S.K., Choi W.H., Lee M.J. Targeting estrogen receptors for the treatment of Alzheimer's disease. Mol. Neurobiol. 2014, 49:39-49.
77. Leung Y.K., Mak P., Hassan S., Ho S.M. Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signaling. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13162-13167.
78. Lewandowski S., Kalita K., Kaczmarek L. Estrogen receptor beta. Potential functional significance of a variety of mRNA isoforms. FEBS Lett. 2002, 524:1-5.
79. Lewis D.K., Johnson A.B., Stohlgren S., Harms A., Sohrabji F. Effects of estrogen receptor agonists on the regulation of the inflammatory response in astrocytes from young adult and middle-aged female rats. J. Neuroimmunol. 2008, 195:47-59.
80. Leygue E., Dotzlaw H., Lu B., Glor C., Watson P.H., Murphy L.C. Estrogen receptor beta: mine is longer than yours?. J. Clin. Endocrinol. Metab. 1998, 83:3754-3755.
81. 2+ exchange in spinal cord white matter injury at physiological temperature. J. Neurophysiol. 2000, 84:1116-1119.
82. Littleton-Kearney M.T., Ostrowski N.L., Cox D.A., Rossberg M.I., Hurn P.D. Selective estrogen receptor modulators: tissue actions and potential for CNS protection. CNS Drug Rev. 2002, 8:309-330.
83. Liu H.B., Loo K.K., Palaszynski K., Ashouri J., Lubahn D.B., Voskuhl R.R. Estrogen receptor alpha mediates estrogen's immune protection in autoimmune disease. J. Immunol. 2003, 171:6936-6940.
84. Liu H.Y., Buenafe A.C., Matejuk A., Ito A., Zamora A., Dwyer J., Vandenbark A.A., Offner H. Estrogen inhibition of EAE involves effects on dendritic cell function. J. Neurosci. Res. 2002, 70:238-248.
85. Liu S.B., Zhang N., Guo Y.Y., Zhao R., Shi T.Y., Feng S.F., Wang S.Q., Yang Q., Li X.Q., Wu Y.M., Ma L., Hou Y., Xiong L.Z., Zhang W., Zhao M.G. G-protein-coupled receptor 30 mediates rapid neuroprotective effects of estrogen via depression of NR2B-containing NMDA receptors. J. Neurosci. 2012, 32:4887-4900.
86. Liu S.B., Zhao M.G. Neuroprotective effect of estrogen: role of nonsynaptic NR2B-containing NMDA receptors. Brain Res. Bull. 2013, 93:27-31.
87. Liu X.A., Zhu L.Q., Zhang Q., Shi H.R., Wang S.H., Wang Q., Wang J.Z. Estradiol attenuates tau hyperphosphorylation induced by upregulation of protein kinase-A. Neurochem. Res. 2008, 33:1811-1820.
88. Lubahn D.B., Moyer J.S., Golding T.S., Couse J.F., Korach K.S., Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11162-11166.
89. Luksha L., Kublickiene K. The role of estrogen receptor subtypes for vascular maintenance. Gynecol. Endocrinol. 2009, 25:82-95.
90. Lyons K.E., Hubble J.P., Troster A.I., Pahwa R., Koller W.C. Gender differences in Parkinson's disease. Clin. Neuropharmacol. 1998, 21:118-121.
91. Ma Y., Sullivan J.C., Schreihofer D.A. Dietary genistein and equol (4',7 isoflavandiol) reduce oxidative stress and protect rats against focal cerebral ischemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R871-R877.
92. Madak-Erdogan Z., Charn T.H., Jiang Y., Liu E.T., Katzenellenbogen J.A., Katzenellenbogen B.S. Integrative genomics of gene and metabolic regulation by estrogen receptors α and β, and their coregulators. Mol. Syst. Biol. 2013, 9:676.
93. Malinowska M., Wilkinson F.L., Langford-Smith K.J., Langford-Smith A., Brown J.R., Crawford B.E., Vanier M.T., Grynkiewicz G., Wynn R.F., Wraith J.E., Wegrzyn G., Bigger B.W. Genistein improves neuropathology and corrects behaviour in a mouse model of neurodegenerative metabolic disease. PLoS ONE 2010, 5:e14192.
94. Marder K., Tang M.X., Mejia H., Alfaro B., Cote L., Louis E., Groves J., Mayeux R. Risk of Parkinson's disease among first-degree relatives: a community-based study. Neurology 1996, 47:155-160.
95. McClean J., Nuñez J.L. 17α-Estradiol is neuroprotective in male and female rats in a model of early brain injury. Exp. Neurol. 2008, 210:41-50.
96. McCullough L.D., Alkayed N.J., Traystman R.J., Williams M.J., Hurn P.D. Postischemic estrogen reduces hypoperfusion and secondary ischemia after experimental stroke. Stroke 2001, 32:796-802.
97. McDonnell D.P. Selective estrogen receptor modulators (SERMs): a first step in the development of perfect hormone replacement therapy regimen. J. Soc. Gynecol. Investig. 2000, 7:S10-S15.
98. Mickley K.R., Dluzen D.E. Dose-response effects of estrogen and tamoxifen upon methamphetamine-induced behavioral responses and neurotoxicity of the nigrostriatal dopaminergic system in female mice. Neuroendocrinology 2004, 79:305-316.
99. Mills C.D., Xu G.Y., Johnson K.M., McAdoo D.J., Hulsebosch C.E. AIDA reduces glutamate release and attenuates mechanical allodynia after spinal cord injury. Neuroreport 2000, 11:3067-3070.
100. Moosmann B., Behl C. The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8867-8872.
101. Mosquera L., Colón J.M., Santiago J.M., Torrado A.I., Meléndez M., Segarra A.C., Rodríguez-Orengo J.F., Miranda J.D. Tamoxifen and estradiol improved locomotor function and increased spared tissue in rats after spinal cord injury: their antioxidant effect and role of estrogen receptor alpha. Brain Res. 2014, 1561:11-22.
102. Murata T., Dietrich H.H., Xiang C., Dacey R.G. G protein-coupled estrogen receptor agonist improves cerebral microvascular function after hypoxia/reoxygenation injury in male and female rats. Stroke 2013, 44:779-785.
103. Nalbandian G., Kovats S. Understanding sex biases in immunity: effects of estrogen on the differentiation and function of antigen-presenting cells. Immunol. Res. 2005, 31:91-106.
104. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., Gustafsson J.A. Mechanisms of estrogen action. Physiol. Rev. 2001, 81:1535-1565.
105. Numakawa T., Matsumoto T., Numakawa Y., Richards M., Yamawaki S., Kunugi H. Protective action of neurotrophic factors and estrogen against oxidative stress-mediated neurodegeneration. J. Toxicol. 2011, 2011:405194.
106. Occhiuto F., Palumbo D.R., Samperi S., Zangla G., Pino A., De Pasquale R., Circosta C. The isoflavones mixture from Trifolium pratense L. protects HCN 1-A neurons from oxidative stress. Phytother. Res. 2009, 23:192-196.
107. Occhiuto F., Zangla G., Samperi S., Palumbo D.R., Pino A., De Pasquale R., Circosta C. The phytoestrogenic isoflavones from Trifolium pratense L. (Red clover) protects human cortical neurons from glutamate toxicity. Phytomedicine 2008, 15:676-682.
108. Ogawa S., Inoue S., Watanabe T., Orimo A., Hosoi T., Ouchi Y., Muramatsu M. Molecular cloning and characterization of human estrogen receptor betacx: a potential inhibitor of estrogen action in human. Nucleic Acids Res. 1998, 26:3505-3512.
109. Okamoto Y., Liu X., Suzuki N., Okamoto K., Kim H.J., Laxmi Y.R., Sayama K., Shibutani S. Equine estrogen-induced mammary tumors in rats. Toxicol. Lett. 2010, 193:224-228.
110. O'Neill K., Chen S., Diaz Brinton R. Impact of the selective estrogen receptor modulator, tamoxifen, on neuronal outgrowth and survival following toxic insults associated with aging and Alzheimer's disease. Exp. Neurol. 2004, 188:268-278.
111. Oostenbrink B.C., Pitera J.W., van Lipzig M.M., Meerman J.H., van Gunsteren W.F. Simulations of the estrogen receptor ligand-binding domain: affinity of natural ligands and xenoestrogens. J. Med. Chem. 2000, 43:4594-4605.
112. Palaszynski K.M., Liu H., Loo K.K., Voskuhl R.R. Estriol treatment ameliorates disease in males with experimental autoimmune encephalomyelitis: implications for multiple sclerosis. J. Neuroimmunol. 2004, 149:84-89.
113. Pang Z., Bondada V., Sengoku T., Siman R., Geddes J.W. Calpain facilitates the neuron death induced by 3-nitropropionic acid and contributes to the necrotic morphology. J. Neuropathol. Exp. Neurol. 2003, 62:633-643.
114. + T cells. Curr. Opin. Rheumatol. 2007, 19:414-420.
115. Petrone A.B., Gatson J.W., Simpkins J.W., Reed M.N. Non-feminizing estrogens: a novel neuroprotective therapy. Mol. Cell. Endocrinol. 2014, 389:40-47.
116. + regulatory T cell compartment. J. Immunol. 2004, 173:2227-2230.
117. Ragonese P., D'Amelio M., Salemi G., Aridon P., Gammino M., Epifanio A., Morgante L., Savettieri G. Risk of Parkinson disease in women: effect of reproductive characteristics. Neurology 2004, 62:2010-2014.
118. Rakkestad K.E., Sørvik I.B., Overby G.R., Debernard K.A., Mathisen G.H., Paulsen R.E. 17α-Estradiol down-regulates glutathione synthesis in serum deprived PC-12 cells. Free Radic. Res. 2014, 48:1170-1178.
119. Ramsey T.L., Risinger K.E., Jernigan S.C., Mattingly K.A., Klinge C.M. Estrogen receptor beta isoforms exhibit differences in ligand-activated transcriptional activity in an estrogen response element sequence-dependent manner. Endocrinology 2004, 145:149-160.
120. Ray S.K., Hogan E.L., Banik N.L. Calpain in the pathophysiology of spinal cord injury: neuroprotection with calpain inhibitors. Brain Res. Rev. 2003, 42:169-185.
121. Ray S.K., Samantaray S., Smith J.A., Matzelle D.D., Das A., Banik N.L. Inhibition of cysteine proteases in acute and chronic spinal cord injury. Neurotherapeutics 2011, 8:180-186.
122. Rimbach G., Boesch-Saadatmandi C., Frank J., Fuchs D., Wenzel U., Daniel H., Hall W.L., Weinberg P.D. Dietary isoflavones in the prevention of cardiovascular disease - a molecular perspective. Food Chem. Toxicol. 2008, 46:1308-1319.
123. Rivest S. Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 2009, 9:429-439.
124. Roof R.L., Hall E.D. Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J. Neurotrauma 2000, 17:367-388.
125. Rzemieniec J., Litwa E., Wnuk A., Lason W., Gołas A., Krzeptowski W., Kajta M. Neuroprotective action of raloxifene against hypoxia-induced damage in mouse hippocampal cells depends on ERα but not ERβ or GPR30 signalling. J. Steroid Biochem. Mol. Biol. 2014, 10.1016/j.jsbmb.2014.05.005.
126. Saiyed M., Riker W.K. Cholinergic and anticholinergic drug effects on survival during hypoxia: significant gender differences. J. Pharmacol. Exp. Ther. 1993, 264:1146-1153.
127. Saji S., Omoto Y., Shimizu C., Warner M., Hayashi Y., Horiguchi S., Watanabe T., Hayashi S., Gustafsson J.A., Toi M. Expression of estrogen receptor (ER) (beta)cx protein in ER(alpha)-positive breast cancer: specific correlation with progesterone receptor. Cancer Res. 2002, 62:4849-4853.
128. Samantaray S., Sribnick E.A., Das A., Thakore N.P., Matzelle D., Yu S.P., Ray S.K., Wei L., Banik N.L. Neuroprotective efficacy of estrogen in experimental spinal cord injury in rats. Ann. N. Y. Acad. Sci. 2010, 1199:90-94.
129. Saunders-Pullman R., Gordon-Elliott J., Parides M., Fahn S., Saunders H.R., Bressman S. The effect of estrogen replacement on early Parkinson's disease. Neurology 1999, 52:1417-1421.
130. Savaskan E., Olivieri G., Meier F., Ravid R., Muller-Spahn F. Hippocampal estrogen beta-receptor immunoreactivity is increased in Alzheimer's disease. Brain Res. 2001, 908:113-119.
131. +. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:840-845.
132. Schreihofer D.A., Ma Y. Estrogen receptors and ischemic neuroprotection: who, what, where, and when?. Brain Res. 2013, 1514:107-122.
133. Schreihofer D.A., Redmond L. Soy phytoestrogens are neuroprotective against stroke-like injury in vitro. Neuroscience 2009, 158:602-609.
134. Schultz J.R., Petz L.N., Nardulli A.M. Cell- and ligand-specific regulation of promoters containing activator protein-1 and Sp1 sites by estrogen receptors α and β. J. Biol. Chem. 2005, 280:347-354.
135. Schupf N., Lee J.H., Wei M., Pang D., Chace C., Cheng R., Zigman W.B., Tycko B., Silverman W. Estrogen receptor-alpha variants increase risk of Alzheimer's disease in women with Down syndrome. Dement. Geriatr. Cogn. Disord. 2008, 25:476-482.
136. Session D.R., Pearlstone M.M., Jewelewicz R., Kelly A.C. Estrogens and Parkinson's disease. Med. Hypotheses 1994, 42:280-282.
137. Shao B., Cheng Y., Jin K. Estrogen, neuroprotection and neurogenesis after ischemic stroke. Curr. Drug Targets 2012, 13:188-198.
138. 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, 388:507-525.
139. Shughrue P.J., Merchenthaler I. Estrogen is more than just a "sex hormone": novel sites for estrogen action in the hippocampus and cerebral cortex. Front. Neuroendocrinol. 2000, 21:95-101.
140. Sicotte N.L., Liva S.M., Klutch R., Pfeiffer P., Bouvier S., Odesa S., Wu T.C., Voskuhl R.R. Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann. Neurol. 2002, 52:421-428.
141. Sierra A., Gottfried-Blackmore A., Milner T.A., McEwen B.S., Bulloch K. Steroid hormone receptor expression and function in microglia. Glia 2008, 56:659-674.
142. Singh N.P., Singh U.P., Nagarkatti P.S., Nagarkatti M. Prenatal exposure of mice to diethylstilbestrol disrupts T-cell differentiation by regulating Fas/Fas ligand expression through estrogen receptor element and nuclear factor-κB motifs. J. Pharmacol. Exp. Ther. 2012, 343:351-361.
143. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
144. Spencer J.L., Waters E.M., Romeo R.D., Wood G.E., Millner T.A., McEwen B.S. Uncovering the mechanism of estrogen effects on hippocampal function. Front. Neuroendocrinol. 2008, 29:219-237.
145. 2+ channels. Brain Res. 2009, 1276:159-170.
146. Sribnick E.A., Matzelle D.D., Ray S.K., Banik N.L. Estrogen as a prospective multi-active agent for the treatment of spinal cord injury. Brain and Spinal Cord Trauma 2009, p581-p598. Springer, New York. N.L. Banik, S.K. Ray (Eds.).
147. Sribnick E.A., Ray S.K., Banik N.L. Estrogen as a multi-active neuroprotective agent in traumatic injuries. Neurochem. Res. 2004, 29:2007-2014.
148. Sribnick E.A., Wingrave J.M., Matzelle D.D., Wilford G.G., Ray S.K., Banik N.L. Estrogen attenuated markers of inflammation and decreased lesion volume in acute spinal cord injury in rats. J. Neurosci. Res. 2005, 82:283-293.
149. 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.
150. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
151. Strijks E., Kremer J.A., Horstink M.W. Effects of female sex steroids on Parkinson's disease in postmenopausal women. Clin. Neuropharmacol. 1999, 22:93-97.
152. Subramanian S., Matejuk A., Zamora A., Vandenbark A.A., Offner H. Oral feeding with ethinyl estradiol suppresses and treats experimental autoimmune encephalomyelitis in SJL mice and inhibits the recruitment of inflammatory cells into the central nervous system. J. Immunol. 2003, 170:1548-1555.
153. Sun J., Meyers M.J., Fink B.E., Rajendran R., Katzenellenbogen A., Katzenellenbogen B.S. Novel ligands that function as selective estrogens or antiestrogens for estrogen receptor-α or estrogen receptor-β. Endocrinology 1999, 140:800-804.
154. Tian Z., Liu S.B., Wang Y.C., Li X.Q., Zheng L.H., Zhao M.G. Neuroprotective effects of formononetin against NMDA-induced apoptosis in cortical neurons. Phytother. Res. 2013, 10.1002/ptr.4928.
155. Vegeto E., Belcredito S., Etteri S., Ghisletti S., Brusadelli A., Meda C., Krust A., Dupont S., Ciana P., Chambon P., Maggi A. Estrogen receptor-α mediates the brain anti-inflammatory activity of estradiol. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9614-9619.
156. Vizi E.S., Kisfali M., Lorincz T. Role of nonsynaptic GluN2B-containing NMDA receptors in excitotoxicity: evidence that fluoxetine selectively inhibits these receptors and may have neuroprotective effects. Brain Res. Bull. 2013, 93:32-38.
157. Voskuhl R.R., Peterson R.S., Song B., Ao Y., Morales L.B.J., Tiwari-Woodruff S., Sofroniew M.V. Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J. Neurosci. 2009, 29:11511-11522.
158. Wang R., Tu J., Zhang Q., Zhang X., Zhu Y., Ma W., Cheng C., Brann D.W., Yang F. Genistein attenuates ischemic oxidative damage and behavioral deficits via eNOS/Nrf2/HO-1 signaling. Hippocampus 2013, 23:634-647.
159. 2 toxicity in human neuroblastoma SK-N-SH cells. Mol. Pharmacol. 2006, 70:395-404.
160. Warner M., Gustafsson J.A. Estrogen receptor β and liver X receptor β: biology and therapeutic potential in CNS diseases. Mol. Psychiatry 2014, 10.1038/mp.2014.23.
161. Watanabe Y., Littleton-Kearney M.T., Traystman R.J., Hurn P.D. Estrogen restores postischemic pial microvascular dilation. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H155-H160.
162. Watson C.S., Jeng Y.J., Kochukov M.Y. Nongenomic actions of estradiol compared with estrone and estriol in pituitary tumor cell signaling and proliferation. FASEB J. 2008, 22:3328-3336.
163. Wegrzyn G., Jakóbkiewicz-Banecka J., Gabig-Cimińska M., Piotrowska E., Narajczyk M., Kloska A., Malinowska M., Dziedzic D., Gołebiewska I., Moskot M., Wegrzyn A. Genistein: a natural isoflavone with a potential for treatment of genetic diseases. Biochem. Soc. Trans. 2010, 38:695-701.
164. Wingrave J.M., Sribnick E.A., Wilford G.G., Matzelle D.D., Mou J.A., Ray S.K., Hogan E.L., Banik N.L. Relatively low levels of calpain expression in juvenile rat correlate with less neuronal apoptosis after spinal cord injury. Exp. Neurol. 2004, 187:529-532.
165. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Liu Y. Estrogens: trophic and protective factors in the adult brain. Front. Neuroendocrinol. 2001, 22:33-66.
166. Witorsch R.J. Low-dose in utero effects of xenoestrogens in mice and their relevance to humans: an analytical review of the literature. Food Chem. Toxicol. 2002, 40:905-912.
167. Witorsch R.J. Endocrine disruptors: can biological effects and environmental risks be predicted?. Regul. Toxicol. Pharmacol. 2002, 36:118-130.
168. Wolf P.A. An overview of the epidemiology of stroke. Stroke 1990, 21:4-6.
169. Yang S.-H., Shi J., Day A.L., Simpkins J.W. Estradiol exerts neuroprotective effects when administered after ischemic insult. Stroke 2000, 31:745-750.
170. 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. J. Am. Med. Assoc. 2002, 288:2123-2129.
171. Zhang Y.-Q., Shi J., Rajakumar G., Day A.L., Simpkins J.W. Effects of gender and estradiol treatment on focal brain ischemia. Brain Res. 1998, 784:321-324.
172. 2+ dynamics leading to ERK phosphorylation and estrogen neuroprotection in hippocampal neurons. Brain Res. 2007, 1172:48-59.
173. Zhao L., Jin C., Mao Z., Gopinathan M.B., Rehder K., Brinton R.D. Design, synthesis, and estrogenic activity of a novel estrogen receptor modulator - a hybrid structure of 17β-estradiol and vitamin E in hippocampal neurons. J. Med. Chem. 2007, 50:4471-4481.
174. Zhao L., O'Neill K., Brinton R.D. Selective estrogen receptor modulators (SERMs) for the brain: current status and remaining challenges for developing NeuroSERMs. Brain Res. Rev. 2005, 49:472-493.
175. Zhao L., O'Neill K., Brinton R.D. Estrogenic agonist activity of ICI 182,780 (Faslodex) in hippocampal neurons: implications for basic science understanding of estrogen signaling and development of estrogen modulators with a dual therapeutic profile. J. Pharmacol. Exp. Ther. 2006, 319:1124-1132.
176. Ziehn M.O., Avedisian A.A., Dervin S.M., O'Dell T.J., Voskuhl R.R. Estriol preserves synaptic transmission in the hippocampus during autoimmune demyelinating disease. Lab. Invest. 2012, 92:1234-1245.