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Reviews in the Neurosciences

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Volume 25, Issue 2 (Apr 2014)


Possible roles of astrocytes in estrogen neuroprotection during cerebral ischemia

Cuifen Wang
  • Department of Physiology, Medical School of Southeast University, Nanjing, Jiangsu Province, China
  • Center for Diagnostic Nanosystems, Marshall University, Huntington, WV 25755, USA
/ Chao Jie
  • Department of Physiology, Medical School of Southeast University, Nanjing, Jiangsu Province, China
/ Xiaoniu Dai
  • Corresponding author
  • Department of Physiology, Medical School of Southeast University, Nanjing, Jiangsu Province, China
  • Email:
Published Online: 2014-02-22 | DOI: https://doi.org/10.1515/revneuro-2013-0055


17β-Estradiol (E2), one of female sex hormones, has well-documented neuroprotective effects in a variety of clinical and experimental disorders of the central cerebral ischemia, including stroke and neurodegenerative diseases. The cellular mechanisms that underlie these protective effects of E2 are uncertain because a number of different cell types express estrogen receptors in the central nervous system. Astrocytes are the most abundant cells in the central nervous system and provide structural and nutritive support of neurons. They interact with neurons by cross-talk, both physiologically and pathologically. Proper astrocyte function is particularly important for neuronal survival under ischemic conditions. Dysfunction of astrocytes resulting from ischemia significantly influences the responses of other brain cells to injury. Recent studies demonstrate that estrogen receptors are expressed in astrocytes, indicating that E2 may exert multiple regulatory actions on astrocytes. Cerebral ischemia induced changes in the expression of estrogen receptors in astrocytes. In the present review, we summarize the data in support of possible roles for astrocytes in the mediation of neuroprotection by E2 against cerebral ischemia.

Keywords: astrocytes; cerebral ischemia; estrogen receptors; neuroprotection; 17β-estradiol


  • Acs, P., Kipp, M., Norkute, A., Johann, S., Clarner, T., Braun, A., Berente, Z., Komoly, S., and Beyer, C. (2009). 17β-estradiol and progesterone prevent cuprizone provoked demyelination of corpus callosum in male mice. Glia 57, 807–814. [Crossref]

  • Al-Bader, M.D., Malatiali, S.A., and Redzic, Z.B. (2011). Expression of estrogen receptor α and β in rat astrocytes in primary culture: effects of hypoxia and glucose deprivation. Physiol. Res. 60, 951–960.

  • Albanito, L., Madeo, A., Lappano, R., Vivacqua, A., Rago, V., Carpino, A., Oprea, T.I., Prossnitz, E.R., Musti, A.M., Ando, S., et al. (2007). G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17β-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res. 67, 1859–1866. [Crossref]

  • Alkayed, N.J., Harukuni, I., Kimes, A.S., London, E.D., Traystman, R.J., and Hurn, P.D. (1998). Gender-linked brain injury in experimental stroke. Stroke 29, 159–165; discussion 166. [Crossref]

  • Alkayed, N.J., Murphy, S.J., Traystman, R.J., Hurn, P.D., and Miller, V.M. (2000). Neuroprotective effects of female gonadal steroids in reproductively senescent female rats. Stroke 31, 161–168. [Crossref] [PubMed]

  • Al Sweidi, S., Sanchez, M.G., Bourque, M., Morissette, M., Dluzen, D., and Di Paolo, T. (2012). Oestrogen receptors and signalling pathways: implications for neuroprotective effects of sex steroids in Parkinson’s disease. J. Neuroendocrinol. 24, 48–61. [Crossref]

  • Araujo, G.W., Beyer, C., and Arnold, S. (2008). Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes. J. Neuroendocrinol. 20, 930–941. [Crossref]

  • Arevalo, M.A., Santos-Galindo, M., Bellini, M.J., Azcoitia, I., and Garcia-Segura, L.M. (2010). Actions of estrogens on glial cells: implications for neuroprotection. Biochim. Biophys. Acta 1800, 1106–1112.

  • Arimoto, J.M., Wong, A., Rozovsky, I., Lin, S.W., Morgan, T.E., and Finch, C.E. (2013). Age increase of estrogen receptor-α (ERα) in cortical astrocytes impairs neurotrophic support in male and female rats. Endocrinology 154, 2101–2113.

  • Arnold, S., de Araujo, G.W., and Beyer, C. (2008). Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones. J. Mol. Endocrinol. 41, 289–300. [Crossref]

  • Attwell, D., Buchan, A.M., Charpak, S., Lauritzen, M., Macvicar, B.A., and Newman, E.A. (2010). Glial and neuronal control of brain blood flow. Nature 468, 232–243.

  • Ayus, J.C., Achinger, S.G., and Arieff, A. (2008). Brain cell volume regulation in hyponatremia: role of sex, age, vasopressin, and hypoxia. Am. J. Physiol. Renal. Physiol. 295, F619–F624.

  • Azcoitia, I., Sierra, A., and Garcia-Segura, L.M. (1999). Localization of estrogen receptor β-immunoreactivity in astrocytes of the adult rat brain. Glia 26, 260–267. [Crossref] [PubMed]

  • Azcoitia, I., Santos-Galindo, M., Arevalo, M.A., and Garcia-Segura, L.M. (2010). Role of astroglia in the neuroplastic and neuroprotective actions of estradiol. Eur. J. Neurosci. 32, 1995–2002. [Crossref] [PubMed]

  • Barreto, G., Veiga, S., Azcoitia, I., Garcia-Segura, L.M., and Garcia-Ovejero, D. (2007). Testosterone decreases reactive astroglia and reactive microglia after brain injury in male rats: role of its metabolites, oestradiol and dihydrotestosterone. Eur. J. Neurosci. 25, 3039–3046. [Crossref] [PubMed]

  • Barreto, G., Santos-Galindo, M., Diz-Chaves, Y., Pernia, O., Carrero, P., Azcoitia, I., and Garcia-Segura, L.M. (2009). Selective estrogen receptor modulators decrease reactive astrogliosis in the injured brain: effects of aging and prolonged depletion of ovarian hormones. Endocrinology 150, 5010–5015.

  • Boada, M., Antunez, C., Lopez-Arrieta, J., Caruz, A., Moreno-Rey, C., Ramirez-Lorca, R., Moron, F. J., Hernandez, I., Mauleon, A., Rosende-Roca, M., et al. (2012). Estrogen receptor α gene variants are associated with Alzheimer’s disease. Neurobiol. Aging 33, 198. e115–198.e124. [PubMed]

  • Boix, R., del Barrio, J.L., Saz, P., Rene, R., Manubens, J.M., Lobo, A., Gascon, J., de Arce, A., Diaz-Guzman, J., Bergareche, A., et al. (2006). Stroke prevalence among the Spanish elderly: an analysis based on screening surveys. BMC Neurol. 6, 36. [Crossref]

  • Bologa, C.G., Revankar, C.M., Young, S.M., Edwards, B.S., Arterburn, J.B., Kiselyov, A.S., Parker, M.A., Tkachenko, S.E., Savchuck, N.P., Sklar, L.A., et al. (2006). Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2, 207–212. [Crossref]

  • Bondar, G., Kuo, J., Hamid, N., and Micevych, P. (2009). Estradiol-induced estrogen receptor – a trafficking. J. Neurosci. 29, 15323–15330. [Crossref]

  • Bourque, M., Dluzen, D.E., and Di Paolo, T. (2012). Signaling pathways mediating the neuroprotective effects of sex steroids and SERMs in Parkinson’s disease. Front. Neuroendocrinol. 33, 169–178. [PubMed] [Crossref]

  • Brailoiu, E., Dun, S.L., Brailoiu, G.C., Mizuo, K., Sklar, L.A., Oprea, T.I., Prossnitz, E.R., and Dun, N.J. (2007). Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 193, 311–321.

  • Brann, D.W., Dhandapani, K., Wakade, C., Mahesh, V.B., and Khan, M.M. (2007). Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids 72, 381–405. [PubMed] [Crossref]

  • Brann, D., Raz, L., Wang, R., Vadlamudi, R., and Zhang, Q. (2012). Oestrogen signalling and neuroprotection in cerebral ischaemia. J. Neuroendocrinol. 24, 34–47. [Crossref]

  • Brinton, R.D. (2008). The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci. 31, 529–537. [PubMed] [Crossref]

  • Brown, C.M., Suzuki, S., Jelks, K.A., and Wise, P.M. (2009). Estradiol is a potent protective, restorative, and trophic factor after brain injury. Semin. Reprod. Med. 27, 240–249. [Crossref] [PubMed]

  • Cambiasso, M.J., Colombo, J.A., and Carrer, H.F. (2000). Differential effect of oestradiol and astroglia-conditioned media on the growth of hypothalamic neurons from male and female rat brains. Eur. J. Neurosci. 12, 2291–2298. [PubMed] [Crossref]

  • Carlstrom, L., Ke, Z.J., Unnerstall, J.R., Cohen, R.S., and Pandey, S.C. (2001). Estrogen modulation of the cyclic AMP response element-binding protein pathway. Effects of long-term and acute treatments. Neuroendocrinology 74, 227–243. [PubMed] [Crossref]

  • Carswell, H.V., Macrae, I.M., Gallagher, L., Harrop, E., and Horsburgh, K.J. (2004). Neuroprotection by a selective estrogen receptor β agonist in a mouse model of global ischemia. Am. J. Physiol. Heart Circ. Physiol. 287, H1501–H1504.

  • Carswell, H.V., Dominiczak, A.F., Garcia-Segura, L.M., Harada, N., Hutchison, J.B., and Macrae, I.M. (2005). Brain aromatase expression after experimental stroke: topography and time course. J. Steroid Biochem. Mol. Biol. 96, 89–91. [Crossref]

  • Cerciat, M., Unkila, M., Garcia-Segura, L.M., and Arevalo, M.A. (2010). 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 58, 93–102.

  • Chaban, V.V., Lakhter, A.J., and Micevych, P. (2004). A membrane estrogen receptor mediates intracellular calcium release in astrocytes. Endocrinology 145, 3788–3795. [PubMed] [Crossref]

  • Cheong, R.Y., Kwakowsky, A., Barad, Z., Porteous, R., Herbison, A.E., and Abraham, I.M. (2012). Estradiol acts directly and indirectly on multiple signaling pathways to phosphorylate cAMP-response element binding protein in GnRH neurons. Endocrinology 153, 3792–3803.

  • Cho, J., Kim, D., Lee, S., and Lee, Y. (2005). Cobalt chloride-induced estrogen receptor α down-regulation involves hypoxia-inducible factor-1α in MCF-7 human breast cancer cells. Mol. Endocrinol. 19, 1191–1199. [Crossref] [PubMed]

  • Christian, C.A., Glidewell-Kenney, C., Jameson, J.L., and Moenter, S.M. (2008). Classical estrogen receptor α signaling mediates negative and positive feedback on gonadotropin-releasing hormone neuron firing. Endocrinology 149, 5328–5334.

  • Cimarosti, H., Jones, N.M., O’Shea, R.D., Pow, D.V., Salbego, C., and Beart, P.M. (2005). Hypoxic preconditioning in neonatal rat brain involves regulation of excitatory amino acid transporter 2 and estrogen receptor α. Neurosci. Lett. 385, 52–57.

  • Coleman, K.M., Dutertre, M., El-Gharbawy, A., Rowan, B.G., Weigel, N.L., and Smith, C.L. (2003). Mechanistic differences in the activation of estrogen receptor-α (ER α)- and ER β-dependent gene expression by cAMP signaling pathway(s). J. Biol. Chem. 278, 12834–12845.

  • Cordeau, P. Jr., Lalancette-Hebert, M., Weng, Y.C., and Kriz, J. (2008). Live imaging of neuroinflammation reveals sex and estrogen effects on astrocyte response to ischemic injury. Stroke 39, 935–942. [PubMed] [Crossref]

  • Dai, X., Chen, L., and Sokabe, M. (2007). Neurosteroid estradiol rescues ischemia-induced deficit in the long-term potentiation of rat hippocampal CA1 neurons. Neuropharmacology 52, 1124–1138. [Crossref]

  • Dallas, M., Boycott, H.E., Atkinson, L., Miller, A., Boyle, J.P., Pearson, H.A., and Peers, C. (2007). Hypoxia suppresses glutamate transport in astrocytes. J. Neurosci. 27, 3946–3955. [Crossref]

  • De Butte-Smith, M., Gulinello, M., Zukin, R.S., and Etgen, A.M. (2009). Chronic estradiol treatment increases CA1 cell survival but does not improve visual or spatial recognition memory after global ischemia in middle-aged female rats. Horm. Behav. 55, 442–453. [Crossref]

  • Devarajan, A., Bourquard, N., Hama, S., Navab, M., Grijalva, V.R., Morvardi, S., Clarke, C.F., Vergnes, L., Reue, K., Teiber, J.F., et al. (2011). Paraoxonase 2 deficiency alters mitochondrial function and exacerbates the development of atherosclerosis. Antioxid. Redox Signal 14, 341–351.

  • Dhandapani, K.M., Wade, F.M., Mahesh, V.B., and Brann, D.W. (2005). Astrocyte-derived transforming growth factor-β mediates the neuroprotective effects of 17β-estradiol: involvement of nonclassical genomic signaling pathways. Endocrinology 146, 2749–2759. [Crossref]

  • Dodel, R.C., Du, Y., Bales, K.R., Gao, F., and Paul, S.M. (1999). Sodium salicylate and 17β-estradiol attenuate nuclear transcription factor NF-κB translocation in cultured rat astroglial cultures following exposure to amyloid Aβ(1-40) and lipopolysaccharides. J. Neurochem. 73, 1453–1460.

  • Donzelli, A., Braida, D., Finardi, A., Capurro, V., Valsecchi, A.E., Colleoni, M., and Sala, M. (2010). Neuroprotective effects of genistein in Mongolian gerbils: estrogen receptor-β involvement. J. Pharmacol. Sci. 114, 158–167.

  • Dubal, D.B. and Wise, P.M. (2002). Estrogen and neuroprotection: from clinical observations to molecular mechanisms. Dialogues Clin. Neurosci. 4, 149–161. [PubMed]

  • Dubal, D.B., Zhu, H., Yu, J., Rau, S.W., Shughrue, P.J., Merchenthaler, I., Kindy, M.S., and Wise, P.M. (2001). Estrogen receptor α, not β, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. USA 98, 1952–1957.

  • Dubal, D.B., Rau, S.W., Shughrue, P.J., Zhu, H., Yu, J., Cashion, A.B., Suzuki, S., Gerhold, L.M., Bottner, M.B., Dubal, S.B., et al. (2006). Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERα in estradiol-mediated protection against delayed cell death. Endocrinology 147, 3076–3084. [PubMed] [Crossref]

  • Dugan, L.L. and Kim-Han, J.S. (2004). Astrocyte mitochondria in in vitro models of ischemia. J. Bioenerg. Biomembr. 36, 317–321. [Crossref]

  • Eichner, L.J. and Giguere, V. (2011). Estrogen related receptors (ERRs): a new dawn in transcriptional control of mitochondrial gene networks. Mitochondrion 11, 544–552. [Crossref] [PubMed]

  • Elzer, J.G., Muhammad, S., Wintermantel, T.M., Regnier- Vigouroux, A., Ludwig, J., Schutz, G., and Schwaninger, M. (2010). Neuronal estrogen receptor-α mediates neuroprotection by 17β-estradiol. J. Cereb. Blood Flow Metab. 30, 935–942.

  • Falkeborn, M., Persson, I., Terent, A., Adami, H.O., Lithell, H., and Bergstrom, R. (1993). Hormone replacement therapy and the risk of stroke. Follow-up of a population-based cohort in Sweden. Arch. Intern. Med. 153, 1201–1209.

  • Filardo, E.J., Quinn, J.A., Bland, K.I., and Frackelton, A.R. Jr. (2000). Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14, 1649–1660.

  • Fuente-Martin, E., Garcia-Caceres, C., Morselli, E., Clegg, D.J., Chowen, J.A., Finan, B., Brinton, R.D., and Tschop, M.H. (2013). Estrogen, astrocytes and the neuroendocrine control of metabolism. Rev. Endocr. Metab. Disord. 14, 331–338. [Crossref]

  • Funakoshi, T., Yanai, A., Shinoda, K., Kawano, M.M., and Mizukami, Y. (2006). G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem. Biophys. Res. Commun. 346, 904–910.

  • Galbiati, M., Martini, L., and Melcangi, R.C. (2002). Oestrogens, via transforming growth factor α, modulate basic fibroblast growth factor synthesis in hypothalamic astrocytes: in vitro observations. J. Neuroendocrinol. 14, 829–835. [Crossref]

  • Garcia-Ovejero, D., Veiga, S., Garcia-Segura, L.M., and Doncarlos, L.L. (2002). Glial expression of estrogen and androgen receptors after rat brain injury. J. Comp. Neurol. 450, 256–271.

  • Garcia-Ovejero, D., Azcoitia, I., Doncarlos, L.L., Melcangi, R.C., and Garcia-Segura, L.M. (2005). Glia-neuron crosstalk in the neuroprotective mechanisms of sex steroid hormones. Brain Res. Brain Res. Rev. 48, 273–286. [Crossref]

  • Garcia-Segura, L.M. and McCarthy, M.M. (2004). Minireview: role of glia in neuroendocrine function. Endocrinology 145, 1082–1086. [Crossref]

  • Garcia-Segura, L.M., Luquin, S., Parducz, A., and Naftolin, F. (1994). Gonadal hormone regulation of glial fibrillary acidic protein immunoreactivity and glial ultrastructure in the rat neuroendocrine hypothalamus. Glia 10, 59–69. [Crossref]

  • Gingerich, S., Kim, G.L., Chalmers, J.A., Koletar, M.M., Wang, X., Wang, Y., and Belsham, D.D. (2010). Estrogen receptor α and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neuroscience 170, 54–66. [Crossref]

  • Giordano, G., Cole, T.B., Furlong, C.E., and Costa, L.G. (2011). Paraoxonase 2 (PON2) in the mouse central nervous system: a neuroprotective role? Toxicol. Appl. Pharmacol. 256, 369–378.

  • Giordano, G., Tait, L., Furlong, C.E., Cole, T.B., Kavanagh, T.J., and Costa, L.G. (2013). Gender differences in brain susceptibility to oxidative stress are mediated by levels of paraoxonase-2 expression. Free Radic. Biol. Med. 58, 98–108.

  • Giraud, S.N., Caron, C.M., Pham-Dinh, D., Kitabgi, P., and Nicot, A.B. (2010). Estradiol inhibits ongoing autoimmune neuroinflammation and NFκB-dependent CCL2 expression in reactive astrocytes. Proc. Natl. Acad. Sci. USA 107, 8416–8421. [Crossref]

  • Gould, E., Woolley, C.S., Frankfurt, M., and McEwen, B.S. (1990). Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10, 1286–1291.

  • Guevara, R., Gianotti, M., Oliver, J., and Roca, P. (2011). Age and sex-related changes in rat brain mitochondrial oxidative status. Exp. Gerontol. 46, 923–928. [PubMed] [Crossref]

  • Gulinello, M., Lebesgue, D., Jover-Mengual, T., Zukin, R.S., and Etgen, A.M. (2006). Acute and chronic estradiol treatments reduce memory deficits induced by transient global ischemia in female rats. Horm. Behav. 49, 246–260. [Crossref] [PubMed]

  • Guo, J., Duckles, S.P., Weiss, J.H., Li, X., and Krause, D.N. (2012). 17β-Estradiol prevents cell death and mitochondrial dysfunction by an estrogen receptor-dependent mechanism in astrocytes after oxygen-glucose deprivation/reperfusion. Free Radic. Biol. Med. 52, 2151–2160.

  • Hall, E.D., Pazara, K.E., and Linseman, K.L. (1991). Sex differences in postischemic neuronal necrosis in gerbils. J. Cereb. Blood Flow Metab. 11, 292–298. [PubMed]

  • Huppmann, S., Romer, S., Altmann, R., Obladen, M., and Berns, M. (2008). 17β-estradiol attenuates hyperoxia-induced apoptosis in mouse C8-D1A cell line. J. Neurosci. Res. 86, 3420–3426.

  • Iadecola, C. and Nedergaard, M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369–1376. [Crossref] [PubMed]

  • Inagaki, T., Kaneko, N., Zukin, R.S., Castillo, P.E., and Etgen, A.M. (2012). Estradiol attenuates ischemia-induced death of hippocampal neurons and enhances synaptic transmission in aged, long-term hormone-deprived female rats. PLoS One 7, e38018.

  • Ivanova, T., Karolczak, M., and Beyer, C. (2001). Estrogen stimulates the mitogen-activated protein kinase pathway in midbrain astroglia. Brain Res. 889, 264–269.

  • Ji, Y., Tang, B., and Traub, R.J. (2011). Spinal estrogen receptor α mediates estradiol-induced pronociception in a visceral pain model in the rat. Pain 152, 1182–1191.

  • Johann, S. and Beyer, C. (2013). Neuroprotection by gonadal steroid hormones in acute brain damage requires cooperation with astroglia and microglia J. Steroid Biochem. Mol. Biol. 137, 71–81. [Crossref]

  • Johann, S., Dahm, M., Kipp, M., Beyer, C., and Arnold, S. (2010). Oestrogen regulates mitochondrial respiratory chain enzyme transcription in the mouse spinal cord. J. Neuroendocrinol. 22, 926–935.

  • Jover-Mengual, T., Zukin, R.S., and Etgen, A.M. (2007). MAPK signaling is critical to estradiol protection of CA1 neurons in global ischemia. Endocrinology 148, 1131–1143. [Crossref]

  • Kalaitzidis, D. and Gilmore, T.D. (2005). Transcription factor cross-talk: the estrogen receptor and NF-kappaB. Trends Endocrinol. Metab. 16, 46–52.

  • Kanda, N. and Watanabe, S. (2003a). 17β-estradiol inhibits MCP-1 production in human keratinocytes. J. Invest. Dermatol. 120, 1058–1066.

  • Kanda, N. and Watanabe, S. (2003b). 17 β-estradiol inhibits oxidative stress-induced apoptosis in keratinocytes by promoting Bcl-2 expression. J. Invest. Dermatol. 121, 1500–1509.

  • Kipp, M., Karakaya, S., Johann, S., Kampmann, E., Mey, J., and Beyer, C. (2007). Oestrogen and progesterone reduce lipopolysaccharide-induced expression of tumour necrosis factor-α and interleukin-18 in midbrain astrocytes. J. Neuroendocrinol. 19, 819–822. [Crossref]

  • Kuo, J., Hamid, N., Bondar, G., Prossnitz, E.R., and Micevych, P. (2010). Membrane estrogen receptors stimulate intracellular calcium release and progesterone synthesis in hypothalamic astrocytes. J. Neurosci. 30, 12950–12957. [Crossref]

  • Kuppers, E., Ivanova, T., Karolczak, M., Lazarov, N., Fohr, K., and Beyer, C. (2001). Classical and nonclassical estrogen action in the developing midbrain. Horm. Behav. 40, 196–202. [PubMed] [Crossref]

  • Kwakowsky, A., Cheong, R.Y., Herbison, A.E., and Abraham, I.M. (2013). Non-classical effects of estradiol on cAMP responsive element binding protein phosphorylation in gonadotropin-releasing hormone neurons: mechanisms and role. Front. Neuroendocrinol. [PubMed]

  • Lang, J.T. and McCullough, L.D. (2008). Pathways to ischemic neuronal cell death: are sex differences relevant? J. Transl. Med. 6, 33. [Crossref]

  • Lebesgue, D., Chevaleyre, V., Zukin, R.S., and Etgen, A.M. (2009). Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids 74, 555–561. [PubMed] [Crossref]

  • Lebesgue, D., Traub, M., De Butte-Smith, M., Chen, C., Zukin, R.S., Kelly, M.J., and Etgen, A.M. (2010). Acute administration of non-classical estrogen receptor agonists attenuates ischemia-induced hippocampal neuron loss in middle-aged female rats. PLoS One 5, e8642.

  • Lee, E.S., Sidoryk, M., Jiang, H., Yin, Z., and Aschner, M. (2009). Estrogen and tamoxifen reverse manganese-induced glutamate transporter impairment in astrocytes. J. Neurochem. 110, 530–544. [Crossref]

  • Lee, E., Sidoryk-Wegrzynowicz, M., Wang, N., Webb, A., Son, D.S., Lee, K., and Aschner, M. (2012). GPR30 regulates glutamate transporter GLT-1 expression in rat primary astrocytes. J. Biol. Chem. 287, 26817–26828.

  • Lewis, D.K., Johnson, A.B., Stohlgren, S., Harms, A., and Sohrabji, F. (2008). Effects of estrogen receptor agonists on regulation of the inflammatory response in astrocytes from young adult and middle-aged female rats. J. Neuroimmunol. 195, 47–59.

  • Liu, M., Hurn, P.D., Roselli, C.E., and Alkayed, N.J. (2007). Role of P450 aromatase in sex-specific astrocytic cell death. J. Cereb. Blood Flow Metab. 27, 135–141.

  • Loram, L.C., Sholar, P.W., Taylor, F.R., Wiesler, J.L., Babb, J.A., Strand, K.A., Berkelhammer, D., Day, H.E., Maier, S.F., and Watkins, L.R. (2012). Sex and estradiol influence glial pro-inflammatory responses to lipopolysaccharide in rats. Psychoneuroendocrinology 37, 1688–1699. [PubMed] [Crossref]

  • Lu, A., Ran, R.Q., Clark, J., Reilly, M., Nee, A., and Sharp, F.R. (2002). 17-β-estradiol induces heat shock proteins in brain arteries and potentiates ischemic heat shock protein induction in glia and neurons. J. Cereb. Blood Flow Metab. 22, 183–195.

  • Martinez, L. and de Lacalle, S. (2007). Astrocytic reaction to a lesion, under hormonal deprivation. Neurosci. Lett. 415, 190–193.

  • Mateos, L., Persson, T., Katoozi, S., Gil-Bea, F.J., and Cedazo-Minguez, A. (2012). Estrogen protects against amyloid-β toxicity by estrogen receptor α-mediated inhibition of Daxx translocation. Neurosci. Lett. 506, 245–250.

  • Matsuda, K., Sakamoto, H., Mori, H., Hosokawa, K., Kawamura, A., Itose, M., Nishi, M., Prossnitz, E.R., and Kawata, M. (2008). Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci. Lett. 441, 94–99.

  • McAsey, M.E., Cady, C., Jackson, L.M., Li, M., Randall, S., Nathan, B.P., and Struble, R.G. (2006). Time course of response to estradiol replacement in ovariectomized mice: brain apolipoprotein E and synaptophysin transiently increase and glial fibrillary acidic protein is suppressed. Exp. Neurol. 197, 197–205. [PubMed] [Crossref]

  • McCarthy, J.B., Barker-Gibb, A.L., Alves, S.E., and Milner, T.A. (2002). TrkA immunoreactive astrocytes in dendritic fields of the hippocampal formation across estrous. Glia 38, 36–44. [Crossref] [PubMed]

  • McCullough, L.D., Blizzard, K., Simpson, E.R., Oz, O.K., and Hurn, P.D. (2003). Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection. J. Neurosci. 23, 8701–8705.

  • McCullough, L.D., Zeng, Z., Blizzard, K.K., Debchoudhury, I., and Hurn, P.D. (2005). Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J. Cereb. Blood Flow Metab. 25, 502–512. [PubMed]

  • McEwen, B. (2000). Neuronal and cognitive effects of oestrogens. Introduction. Novartis Found. Symp. 230, 1–6.

  • McEwen, B., Akama, K., Alves, S., Brake, W.G., Bulloch, K., Lee, S., Li, C., Yuen, G., and Milner, T.A. (2001). Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc. Natl. Acad. Sci. USA 98, 7093–7100. [Crossref]

  • McKenna, N.J. and O’Malley, B.W. (2002). Minireview: nuclear receptor coactivators – an update. Endocrinology 143, 2461–2465.

  • Melcangi, R.C., Magnaghi, V., Galbiati, M., and Martini, L. (2001). Formation and effects of neuroactive steroids in the central and peripheral nervous system. Int. Rev. Neurobiol. 46, 145–176. [Crossref] [PubMed]

  • Merchenthaler, I., Dellovade, T.L., and Shughrue, P.J. (2003). Neuroprotection by estrogen in animal models of global and focal ischemia. Ann. N.Y. Acad. Sci. 1007, 89–100.

  • Micevych, P., Bondar, G., and Kuo, J. (2010). Estrogen actions on neuroendocrine glia. Neuroendocrinology 91, 211–222. [Crossref] [PubMed]

  • Miller, N.R., Jover, T., Cohen, H.W., Zukin, R.S., and Etgen, A.M. (2005). Estrogen can act via estrogen receptor α and β to protect hippocampal neurons against global ischemia-induced cell death. Endocrinology 146, 3070–3079. [PubMed] [Crossref]

  • 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., et al. (2003). Immunolocalization of estrogen receptor β in the mouse brain: comparison with estrogen receptor α. Endocrinology 144, 2055–2067. [Crossref] [PubMed]

  • Mong, J.A., Nunez, J.L., and McCarthy, M.M. (2002). GABA mediates steroid-induced astrocyte differentiation in the neonatal rat hypothalamus. J. Neuroendocrinol. 14, 45–55. [Crossref]

  • Morissette, M., Le Saux, M., D’Astous, M., Jourdain, S., Al Sweidi, S., Morin, N., Estrada-Camarena, E., Mendez, P., Garcia-Segura, L.M., and Di Paolo, T. (2008). Contribution of estrogen receptors α and β to the effects of estradiol in the brain. J. Steroid Biochem. Mol. Biol. 108, 327–338. [Crossref]

  • Murata, T., Dietrich, H.H., Xiang, C., and Dacey, R.G. Jr. (2013). G protein-coupled estrogen receptor agonist improves cerebral microvascular function after hypoxia/reoxygenation injury in male and female rats. Stroke 44, 779–785. [Crossref]

  • Murphy, S.J., McCullough, L.D., and Smith, J.M. (2004). Stroke in the female: role of biological sex and estrogen. ILAR J. 45, 147–159. [PubMed] [Crossref]

  • Nedergaard, M., Ransom, B., and Goldman, S.A. (2003). New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 26, 523–530. [PubMed] [Crossref]

  • Nilsson, S., Makela, S., Treuter, E., Tujague, M., Thomsen, J., Andersson, G., Enmark, E., Pettersson, K., Warner, M., and Gustafsson, J.A. (2001). Mechanisms of estrogen action. Physiol. Rev. 81, 1535–1565. [PubMed]

  • Panatier, A., Theodosis, D.T., Mothet, J.P., Touquet, B., Pollegioni, L., Poulain, D.A., and Oliet, S.H. (2006). Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775–784. [Crossref] [PubMed]

  • Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S., and Haydon, P.G. (1994). Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747.

  • Pawlak, J., Brito, V., Kuppers, E., and Beyer, C. (2005). Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen. Brain. Res. Mol. Brain Res. 138, 1–7. [Crossref]

  • Pellerin, L. and Magistretti, P.J. (2004). Neuroenergetics: calling upon astrocytes to satisfy hungry neurons. Neuroscientist 10, 53–62. [Crossref] [PubMed]

  • Perea, G., Navarrete, M., and Araque, A. (2009). Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32, 421–431. [Crossref] [PubMed]

  • Perez, S.E., Chen, E.Y., and Mufson, E.J. (2003). Distribution of estrogen receptor α and β immunoreactive profiles in the postnatal rat brain. Brain Res. Dev. Brain Res. 145, 117–139. [Crossref] [PubMed]

  • Prencipe, M., Ferretti, C., Casini, A.R., Santini, M., Giubilei, F., and Culasso, F. (1997). Stroke, disability, and dementia: results of a population survey. Stroke 28, 531–536. [PubMed] [Crossref]

  • Rao, S.P. and Sikdar, S.K. (2006). Astrocytes in 17β-estradiol treated mixed hippocampal cultures show attenuated calcium response to neuronal activity. Glia 53, 817–826. [Crossref]

  • Revankar, C.M., Cimino, D.F., Sklar, L.A., Arterburn, J.B., and Prossnitz, E.R. (2005). A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307, 1625–1630.

  • Roof, R.L., and Hall, E.D. (2000). Estrogen-related gender difference in survival rate and cortical blood flow after impact-acceleration head injury in rats. J. Neurotrauma 17, 1155–1169. [Crossref]

  • Roquer, J., Campello, A.R., and Gomis, M. (2003). Sex differences in first-ever acute stroke. Stroke 34, 1581–1585. [Crossref] [PubMed]

  • Rozovsky, I., Wei, M., Stone, D.J., Zanjani, H., Anderson, C.P., Morgan, T.E., and Finch, C.E. (2002). Estradiol (E2) enhances neurite outgrowth by repressing glial fibrillary acidic protein expression and reorganizing laminin. Endocrinology 143, 636–646.

  • Rutkowsky, J.M., Wallace, B.K., Wise, P.M., and O’Donnell, M.E. (2011). Effects of estradiol on ischemic factor-induced astrocyte swelling and AQP4 protein abundance. Am. J. Physiol. Cell Physiol. 301, C204–C212.

  • Sampei, K., Goto, S., Alkayed, N.J., Crain, B.J., Korach, K.S., Traystman, R.J., Demas, G.E., Nelson, R.J., and Hurn, P.D. (2000). Stroke in estrogen receptor-α-deficient mice. Stroke 31, 738–743; discussion 744. [Crossref]

  • Santos-Galindo, M., Acaz-Fonseca, E., Bellini, M.J., and Garcia-Segura, L.M. (2011). Sex differences in the inflammatory response of primary astrocytes to lipopolysaccharide. Biol. Sex Differ. 2, 7.

  • Sawada, M., Alkayed, N.J., Goto, S., Crain, B.J., Traystman, R.J., Shaivitz, A., Nelson, R.J., and Hurn, P.D. (2000). Estrogen receptor antagonist ICI182,780 exacerbates ischemic injury in female mouse. J. Cereb. Blood Flow Metab. 20, 112–118.

  • Schwarz, J.M. and Bilbo, S.D. (2012). Sex, glia, and development: interactions in health and disease. Horm. Behav. 62, 243–253. [PubMed] [Crossref]

  • Selvamani, A. and Sohrabji, F. (2010a). Reproductive age modulates the impact of focal ischemia on the forebrain as well as the effects of estrogen treatment in female rats. Neurobiol. Aging 31, 1618–1628. [Crossref] [PubMed]

  • Selvamani, A. and Sohrabji, F. (2010b). The neurotoxic effects of estrogen on ischemic stroke in older female rats is associated with age-dependent loss of insulin-like growth factor-1. J. Neurosci. 30, 6852–6861. [Crossref]

  • Shughrue, P.J. and Merchenthaler, I. (2000). Estrogen is more than just a “sex hormone”: novel sites for estrogen action in the hippocampus and cerebral cortex. Front. Neuroendocrinol. 21, 95–101. [Crossref] [PubMed]

  • Shughrue, P.J., Lane, M.V., and Merchenthaler, I. (1997). Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J. Comp. Neurol. 388, 507–525.

  • Sims, N.R. and Muyderman, H. (2010). Mitochondria, oxidative metabolism and cell death in stroke. Biochim. Biophys. Acta 1802, 80–91.

  • Singer, C.A., Figueroa-Masot, X.A., Batchelor, R.H., and Dorsa, D.M. (1999). The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J. Neurosci. 19, 2455–2463.

  • Singh, M., Setalo, G. Jr., Guan, X., Frail, D.E., and Toran-Allerand, C.D. (2000). Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-α knock-out mice. J. Neurosci. 20, 1694–1700.

  • Smith, C.C. and McMahon, L.L. (2006). Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J. Neurosci. 26, 8517–8522.

  • Sohrabji, F., Miranda, R.C., and Toran-Allerand, C.D. (1995). Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92, 11110–11114. [Crossref]

  • Somjen, G.G. (1988). Nervenkitt: notes on the history of the concept of neuroglia. Glia 1, 2–9. [Crossref] [PubMed]

  • Spence, R.D., Hamby, M.E., Umeda, E., Itoh, N., Du, S., Wisdom, A.J., Cao, Y., Bondar, G., Lam, J., Ao, Y., et al. (2011). Neuroprotection mediated through estrogen receptor-α in astrocytes. Proc. Natl. Acad. Sci. USA 108, 8867–8872. [Crossref]

  • Stirone, C., Duckles, S.P., and Krause, D.N. (2003). Multiple forms of estrogen receptor-α in cerebral blood vessels: regulation by estrogen. Am. J. Physiol. Endocrinol. Metab. 284, E184–E192.

  • Sundar Boyalla, S., Barbara Victor, M., Roemgens, A., Beyer, C., and Arnold, S. (2011). Sex- and brain region-specific role of cytochrome c oxidase in 1-methyl-4-phenylpyridinium-mediated astrocyte vulnerability. J. Neurosci. Res. 89, 2068–2082. [Crossref]

  • Suuronen, T., Ojala, J., Hyttinen, J.M., Kaarniranta, K., Thornell, A., Kyrylenko, S., Salminen, A. (2008). Regulation of ER α signaling pathway in neuronal HN10 cells: role of protein acetylation and Hsp90. Neurochem. Res. 33, 1768–1775.

  • Suzuki, S., Brown, C.M., Dela Cruz, C.D., Yang, E., Bridwell, D.A., and Wise, P.M. (2007). Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions. Proc. Natl. Acad. Sci. USA 104, 6013–6018. [Crossref]

  • Takano, T., Oberheim, N., Cotrina, M.L., and Nedergaard, M. (2009). Astrocytes and ischemic injury. Stroke 40, S8–S12. [PubMed]

  • Tan, X.J., Dai, Y.B., Wu, W.F., Kim, H.J., Barros, R.P., Richardson, T.I., Yaden, B.C., Warner, M., McKinzie, D.L., Krishnan, V., et al. (2012). Reduction of dendritic spines and elevation of GABAergic signaling in the brains of mice treated with an estrogen receptor β ligand. Proc. Natl. Acad. Sci. USA 109, 1708–1712. [Crossref]

  • Tapia-Gonzalez, S., Carrero, P., Pernia, O., Garcia-Segura, L.M., and Diz-Chaves, Y. (2008). Selective oestrogen receptor (ER) modulators reduce microglia reactivity in vivo after peripheral inflammation: potential role of microglial ERs. J. Endocrinol. 198, 219–230.

  • Tasker, J.G., Oliet, S.H., Bains, J.S., Brown, C.H., and Stern, J.E. (2012). Glial regulation of neuronal function: from synapse to systems physiology. J. Neuroendocrinol. 24, 566–576. [Crossref]

  • Tenenbaum, M., Azab, A.N., and Kaplanski, J. (2007). Effects of estrogen against LPS-induced inflammation and toxicity in primary rat glial and neuronal cultures. J. Endotoxin Res. 13, 158–166. [Crossref]

  • Tomas-Camardiel, M., Venero, J.L., Herrera, A.J., De Pablos, R.M., Pintor-Toro, J.A., Machado, A., and Cano, J. (2005). Blood-brain barrier disruption highly induces aquaporin-4 mRNA and protein in perivascular and parenchymal astrocytes: protective effect by estradiol treatment in ovariectomized animals. J. Neurosci. Res. 80, 235–246. [Crossref]

  • Toung, T.J., Chen, T.Y., Littleton-Kearney, M.T., Hurn, P.D., and Murphy, S.J. (2004). Effects of combined estrogen and progesterone on brain infarction in reproductively senescent female rats. J. Cereb. Blood Flow Metab. 24, 1160–1166. [PubMed]

  • Turgeon, J.L., Carr, M.C., Maki, P.M., Mendelsohn, M.E., and Wise, P.M. (2006). Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: insights from basic science and clinical studies. Endocr. Rev. 27, 575–605. [PubMed] [Crossref]

  • Vegeto, E., Belcredito, S., Ghisletti, S., Meda, C., Etteri, S., and Maggi, A. (2006). The endogenous estrogen status regulates microglia reactivity in animal models of neuroinflammation. Endocrinology 147, 2263–2272. [Crossref] [PubMed]

  • Wappler, E.A., Felszeghy, K., Szilagyi, G., Gal, A., Skopal, J., Mehra, R.D., Nyakas, C., and Nagy, Z. (2010). Neuroprotective effects of estrogen treatment on ischemia-induced behavioural deficits in ovariectomized gerbils at different ages. Behav. Brain Res. 209, 42–48.

  • Wilson, M.E., Dubal, D.B., and Wise, P.M. (2000). Estradiol protects against injury-induced cell death in cortical explant cultures: a role for estrogen receptors. Brain Res. 873, 235–242.

  • Wu, D.C., Xiao, X.Q., Ng, A.K., Chen, P.M., Chung, W., Lee, N.T., Carlier, P.R., Pang, Y.P., Yu, A.C., and Han, Y.F. (2000). Protection against ischemic injury in primary cultured mouse astrocytes by bis(7)-tacrine, a novel acetylcholinesterase inhibitor [corrected]. Neurosci. Lett. 288, 95–98.

  • Wu, T.W., Wang, J.M., Chen, S., and Brinton, R.D. (2005). 17β-estradiol induced Ca2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 135, 59–72.

  • Xu, Z.C., Chwang, W., Li, X., Chen, X., and He, P. (1999). Gender difference in dopamine concentration and postischemic neuronal damage in neostriatum after unilateral dopamine depletion. Exp. Neurol. 158, 182–191.

  • Yang, S.H., Liu, R., Perez, E.J., Wang, X., and Simpkins, J.W. (2005). Estrogens as protectants of the neurovascular unit against ischemic stroke. Curr. Drug Targets CNS Neurol. Disord. 4, 169–177.

  • Yi, J.M., Kwon, H.Y., Cho, J.Y., and Lee, Y.J. (2009). Estrogen and hypoxia regulate estrogen receptor α in a synergistic manner. Biochem. Biophys. Res. Commun. 378, 842–846.

  • Zhang, J.Q., Cai, W.Q., Zhou, D.S., and Su, B.Y. (2002a). Distribution and differences of estrogen receptor β immunoreactivity in the brain of adult male and female rats. Brain Res. 935, 73–80.

  • Zhang, L., Li, B., Zhao, W., Chang, Y.H., Ma, W., Dragan, M., Barker, J.L., Hu, Q., and Rubinow, D.R. (2002b). Sex-related differences in MAPKs activation in rat astrocytes: effects of estrogen on cell death. Brain Res. Mol. Brain Res. 103, 1–11. [Crossref] [PubMed]

  • Zhang, Q.G., Raz, L., Wang, R., Han, D., De Sevilla, L., Yang, F., Vadlamudi, R.K., and Brann, D.W. (2009). Estrogen attenuates ischemic oxidative damage via an estrogen receptor α-mediated inhibition of NADPH oxidase activation. J. Neurosci. 29, 13823–13836. [Crossref]

  • Zhang, B., Subramanian, S., Dziennis, S., Jia, J., Uchida, M., Akiyoshi, K., Migliati, E., Lewis, A.D., Vandenbark, A.A., Offner, H., et al. (2010). Estradiol and G1 reduce infarct size and improve immunosuppression after experimental stroke. J. Immunol. 184, 4087–4094.

  • Zhang, Q.G., Han, D., Wang, R.M., Dong, Y., Yang, F., Vadlamudi, R.K., and Brann, D.W. (2011). C terminus of Hsc70-interacting protein (CHIP)-mediated degradation of hippocampal estrogen receptor-α and the critical period hypothesis of estrogen neuroprotection. Proc. Natl. Acad. Sci. USA 108, E617–E624. [Crossref]

  • Zhao, L. and Brinton, R.D. (2007). Estrogen receptor α and β differentially regulate intracellular Ca2+ dynamics leading to ERK phosphorylation and estrogen neuroprotection in hippocampal neurons. Brain Res. 1172, 48–59.

About the article

Cuifen Wang

Cuifen Wang is taking her post-doc research at School of Pharmacy, Marshall University, West Virginia, USA. She is skilled in neural degenerative diseases with immunohistochemistry and fluorescence microscopy in brain tissues and employs a variety of biochemical and molecular biological techniques to develop new chemicals against cerebral diseases.

Chao Jie

Jie Chao is a professor at Department of Physiology at the Medical School of Southeast University, Nanjing, China. He got his PhD from University of Kansas Medical Center. He has ample experience with the technique of intravital microscopy, as well as molecular biologic techniques in neuroscience and respiration physiology. He is first-author or correspond-author of more than 20 peer-reviewed papers of his field. The primary objective of Jie’s laboratory is to explore, in vivo and in vitro, molecular and cellular mechanisms underlying the inflammation of silicosis.

Xiaoniu Dai

Xiaoniu Dai is a lecture at the Department of Physiology at the Medical School of Southeast University, Nanjing, China. He got his PhD from the Medical School of Nagoya University, Japan. His research interest is primarily in learning-memory mechanisms with focus on the effects of neurosteroids on synaptic transmission and synaptic plasticity by using electrophysiological techniques, including whole cell patch clamping and field excitatory postsynaptic potentials (fEPSPs) recording from brain slice.

Corresponding author: Xiaoniu Dai, Department of Physiology, Medical School of Southeast University, Nanjing, Jiangsu Province, China, e-mail:

Received: 2013-11-18

Accepted: 2014-01-29

Published Online: 2014-02-22

Published in Print: 2014-04-01

Citation Information: Reviews in the Neurosciences, ISSN (Online) 2191-0200, ISSN (Print) 0334-1763, DOI: https://doi.org/10.1515/revneuro-2013-0055. Export Citation

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