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Current Neuropharmacology

Editor-in-Chief

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

Review Article

Neuroprotective Role of Hypothermia in Hypoxic-ischemic Brain Injury: Combined Therapies using Estrogen

Author(s): Nicolás Toro-Urrego*, Diego Julián Vesga-Jiménez , María Inés Herrera, Juan Pablo Luaces and Francisco Capani

Volume 17, Issue 9, 2019

Page: [874 - 890] Pages: 17

DOI: 10.2174/1570159X17666181206101314

Price: $65

Abstract

Hypoxic-ischemic brain injury is a complex network of factors, which is mainly characterized by a decrease in levels of oxygen concentration and blood flow, which lead to an inefficient supply of nutrients to the brain. Hypoxic-ischemic brain injury can be found in perinatal asphyxia and ischemic-stroke, which represent one of the main causes of mortality and morbidity in children and adults worldwide. Therefore, knowledge of underlying mechanisms triggering these insults may help establish neuroprotective treatments. Selective Estrogen Receptor Modulators and Selective Tissue Estrogenic Activity Regulators exert several neuroprotective effects, including a decrease of reactive oxygen species, maintenance of cell viability, mitochondrial survival, among others. However, these strategies represent a traditional approach of targeting a single factor of pathology without satisfactory results. Hence, combined therapies, such as the administration of therapeutic hypothermia with a complementary neuroprotective agent, constitute a promising alternative. In this sense, the present review summarizes the underlying mechanisms of hypoxic-ischemic brain injury and compiles several neuroprotective strategies, including Selective Estrogen Receptor Modulators and Selective Tissue Estrogenic Activity Regulators, which represent putative agents for combined therapies with therapeutic hypothermia.

Keywords: Hypoxic-ischemic brain injury, neuroprotective treatments, selective estrogen receptor modulators, selective tissue estrogenic activity regulators, therapeutic hypothermia, combined therapies.

Graphical Abstract
[1]
Bélanger, M.; Allaman, I.; Magistretti, P.J. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab., 2011, 14(6), 724-738.
[http://dx.doi.org/10.1016/j.cmet.2011.08.016] [PMID: 22152301]
[2]
Allaman, I.; Bélanger, M.; Magistretti, P.J. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci., 2011, 34(2), 76-87.
[http://dx.doi.org/10.1016/j.tins.2010.12.001] [PMID: 21236501]
[3]
Dwyer, D.S.; Vannucci, S.J.; Simpson, I.A. Expression, regulation, and functional role of glucose transporters (GLUTs) in brain. Int. Rev. Neurobiol., 2002, 51, 159-188.
[http://dx.doi.org/10.1016/S0074-7742(02)51005-9] [PMID: 12420359]
[4]
Vavilis, T.; Delivanoglou, N.; Aggelidou, E.; Stamoula, E.; Mellidis, K.; Kaidoglou, A.; Cheva, A.; Pourzitaki, C.; Chatzimeletiou, K.; Lazou, A.; Albani, M.; Kritis, A. Oxygen-glucose deprivation (OGD) modulates the unfolded protein response (UPR) and inflicts autophagy in a PC12 Hypoxia cell line model. Cell. Mol. Neurobiol., 2016, 36(5), 701-712.
[5]
Salvador, E.; Burek, M.; Förster, C.Y. Stretch and/or oxygen glucose deprivation (OGD) in an in vitro traumatic brain injury (TBI) model induces calcium alteration and inflammatory cascade. Front. Cell. Neurosci., 2015, 9, 323.
[http://dx.doi.org/10.3389/fncel.2015.00323] [PMID: 26347611]
[6]
Tian, T.; Zeng, J.; Zhao, G.; Zhao, W.; Gao, S.; Liu, L. Neuroprotective effects of orientin on oxygen-glucose deprivation/reperfusion-induced cell injury in primary culture of rat cortical neurons. Exp. Biol. Med. (Maywood), 2017, 243(1), 78-86.
[http://dx.doi.org/10.1177/1535370217737983] [PMID: 29073777]
[7]
Yang, X.; Zheng, T.; Hong, H.; Cai, N.; Zhou, X.; Sun, C.; Wu, L.; Liu, S.; Zhao, Y.; Zhu, L.; Fan, M.; Zhou, X.; Jin, F. Neuroprotective effects of Ginkgo Biloba extract and ginkgolide B against oxygen-glucose deprivation/reoxygenation and Gglucose injury in a new in vitro multicellular network model. Front. Med., 2018, 12(3), 307-318.
[8]
Mozaffarian, D.; Benjamin, E.J.; Go, A.S.; Arnett, D.K.; Blaha, M.J.; Cushman, M.; de Ferranti, S.; Després, J-P.; Fullerton, H.J.; Howard, V.J. Heart disease and stroke statistics—2015 update. Circulation, 2015, 131(4), e29-e322.
[9]
Northington, F.J.; Chavez-Valdez, R.; Martin, L.J. Neuronal cell death in neonatal hypoxia-ischemia. Ann. Neurol., 2011, 69(5), 743-758.
[http://dx.doi.org/10.1002/ana.22419] [PMID: 21520238]
[10]
Arevalo, M.A.; Santos-Galindo, M.; Lagunas, N.; Azcoitia, I.; Garcia-Segura, L.M. Selective estrogen receptor modulators as brain therapeutic agents. J. Mol. Endocrinol., 2011, 46(1), R1-R9.
[11]
Ávila, R.M.; Garcia-Segura, L. M.; Cabezas, R.; Torrente, D.; Capani, F.; Gonzalez, J.; Barreto, G. E. Tibolone protects T98G cells from glucose deprivation., J. Steroid Biochem. Mol. Biol., 2014, 144(PART B), 294-303.
[12]
Garzón, D.; Cabezas, R.; Vega, N.; Ávila-Rodriguez, M.; Gonzalez, J.; Gómez, R.M.; Echeverria, V.; Aliev, G.; Barreto, G.E. Novel approaches in astrocyte protection: From experimental methods to computational approaches. J. Mol. Neurosci., 2016, 58(4), 483-492.
[http://dx.doi.org/10.1007/s12031-016-0719-6] [PMID: 26803310]
[13]
Cilio, M.R.; Ferriero, D.M. Synergistic neuroprotective therapies with hypothermia. Semin. Fetal Neonatal Med., 2010, 15(5), 293-298.
[http://dx.doi.org/10.1016/j.siny.2010.02.002] [PMID: 20207600]
[14]
Berger, H.R.; Brekke, E.; Widerøe, M.; Morken, T.S. Neuroprotective Treatments after perinatal hypoxic-ischemic brain injury evaluated with magnetic resonance spectroscopy. Dev. Neurosci., 2017, 39(1-4), 36-48.
[http://dx.doi.org/10.1159/000472709] [PMID: 28448965]
[15]
Fleiss, B.; Gressens, P. Tertiary mechanisms of brain damage: a new hope for treatment of cerebral palsy? Lancet Neurol., 2012, 11(6), 556-566.
[http://dx.doi.org/10.1016/S1474-4422(12)70058-3] [PMID: 22608669]
[16]
Li, B.; Concepcion, K.; Meng, X.; Zhang, L. Brain-immune interactions in perinatal hypoxic-ischemic brain injury. Prog. Neurobiol., 2017, 159, 50-68.
[http://dx.doi.org/10.1016/j.pneurobio.2017.10.006] [PMID: 29111451]
[17]
Chen, X.; Guo, C.; Kong, J. Oxidative stress in neurodegenerative diseases. Neural Regen. Res., 2012, 7(5), 376-385.
[PMID: 25774178]
[18]
Berger, H.R.; Brekke, E.; Widerøe, M.; Morken, T.S. Neuroprotective treatments after perinatal hypoxic-ischemic brain injury evaluated with magnetic resonance spectroscopy. Dev. Neurosci., 2017, 39(1-4), 36-48.
[http://dx.doi.org/10.1159/000472709] [PMID: 28448965]
[19]
Wu, Q.; Chen, W.; Sinha, B.; Tu, Y.; Manning, S.; Thomas, N.; Zhou, S.; Jiang, H.; Ma, H.; Kroessler, D.A.; Yao, J.; Liz, Z.; Inder, T.E.; Wang, X. Neuroprotective agents for neonatal hypoxic-ischemic brain injury. Drug Discov. Today, 2015, 20(11), 1372-1381.
[20]
Leaw, B.; Nair, S.; Lim, R.; Thornton, C.; Mallard, C.; Hagberg, H. Mitochondria, bioenergetics and excitotoxicity: New therapeutic targets in perinatal brain injury. Front. Cell. Neurosci., 2017, 11, 199.
[http://dx.doi.org/10.3389/fncel.2017.00199] [PMID: 28747873]
[21]
Descloux, C.; Ginet, V.; Clarke, P.G.H.; Puyal, J.; Truttmann, A.C. Neuronal death after perinatal cerebral hypoxia-ischemia: Focus on autophagy-mediated cell death. Int. J. Dev. Neurosci., 2015, 45, 75-85.
[http://dx.doi.org/10.1016/j.ijdevneu.2015.06.008] [PMID: 26225751]
[22]
Weber, J.T. Altered calcium signaling following traumatic brain injury. Front. Pharmacol., 2012, 3, 60.
[http://dx.doi.org/10.3389/fphar.2012.00060] [PMID: 22518104]
[23]
Ouyang, Y-B.; Giffard, R.G. Cellular neuroprotective mechanisms in cerebral ischemia: Bcl-2 family proteins and protection of mitochondrial function. Cell Calcium, 2004, 36(3-4), 303-311.
[http://dx.doi.org/10.1016/j.ceca.2004.02.015] [PMID: 15261486]
[24]
Wang, C.; Youle, R.J. The role of mitochondria in apoptosis*. Annu. Rev. Genet., 2009, 43, 95-118.
[http://dx.doi.org/10.1146/annurev-genet-102108-134850] [PMID: 19659442]
[25]
Jacobson, J.; Duchen, M.R. Mitochondrial oxidative stress and cell death in astrocytes--requirement for stored Ca2+ and sustained opening of the permeability transition pore. J. Cell Sci., 2002, 115(Pt 6), 1175-1188.
[PMID: 11884517]
[26]
Kadenbach, B.; Hüttemann, M.; Arnold, S.; Lee, I.; Bender, E. Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic. Biol. Med., 2000, 29(3-4), 211-221.
[http://dx.doi.org/10.1016/S0891-5849(00)00305-1] [PMID: 11035249]
[27]
Kagan, V.E.; Chu, C.T.; Tyurina, Y.Y.; Cheikhi, A.; Bayir, H. Cardiolipin asymmetry, oxidation and signaling. Chem. Phys. Lipids, 2014, 179, 64-69.
[http://dx.doi.org/10.1016/j.chemphyslip.2013.11.010] [PMID: 24300280]
[28]
Paradies, G.; Petrosillo, G.; Paradies, V.; Ruggiero, F.M. Role of cardiolipin peroxidation and Ca2+ in mitochondrial dysfunction and disease. Cell Calcium, 2009, 45(6), 643-650.
[http://dx.doi.org/10.1016/j.ceca.2009.03.012] [PMID: 19368971]
[29]
Millar, L.J.; Shi, L.; Hoerder-Suabedissen, A.; Molnár, Z. Neonatal hypoxia ischaemia: Mechanisms, models, and therapeutic challenges. Front. Cell. Neurosci., 2017, 11, 78.
[http://dx.doi.org/10.3389/fncel.2017.00078] [PMID: 28533743]
[30]
Rocha-Ferreira, E.; Hristova, M. Antimicrobial peptides and complement in neonatal hypoxia-ischemia induced brain damage. Front. Immunol., 2015, 6, 56.
[http://dx.doi.org/10.3389/fimmu.2015.00056] [PMID: 25729383]
[31]
Ziemka-Nalecz, M.; Jaworska, J.; Zalewska, T. Insights into the neuroinflammatory responses after neonatal hypoxia-ischemia. J. Neuropathol. Exp. Neurol., 2017, 76(8), 644-654.
[http://dx.doi.org/10.1093/jnen/nlx046] [PMID: 28789477]
[32]
Lee, W.L.A.; Michael-Titus, A.T.; Shah, D.K. Hypoxic-ischaemic encephalopathy and the blood-brain barrier in neonates. Dev. Neurosci., 2017, 39(1-4), 49-58.
[http://dx.doi.org/10.1159/000467392] [PMID: 28434009]
[33]
Paternotte, E.; Gaucher, C.; Labrude, P.; Stoltz, J.F.; Menu, P. Review: Behaviour of endothelial cells faced with hypoxia. Biomed. Mater. Eng., 2008, 18(4-5), 295-299.
[PMID: 19065037]
[34]
Bélanger, M.; Magistretti, P.J. The role of astroglia in neuroprotection. Dialogues Clin. Neurosci., 2009, 11(3), 281-295.
[PMID: 19877496]
[35]
Karki, P.; Webb, A.; Zerguine, A.; Choi, J.; Son, D.S.; Lee, E. Mechanism of raloxifene-induced upregulation of glutamate transporters in rat primary astrocytes. Glia, 2014, 62(8), 1270-1283.
[http://dx.doi.org/10.1002/glia.22679] [PMID: 24782323]
[36]
Guillamón-Vivancos, T.; Gómez-Pinedo, U.; Matías-Guiu, J. Astrocitos En Las enfermedades neurodegenerativas (I): Función y caracterización molecular. Neurologia, 2015, 30(2), 119-129.
[http://dx.doi.org/10.1016/j.nrl.2012.12.007] [PMID: 23465689]
[37]
Fuller, S.; Steele, M.; Münch, G. Activated astroglia during chronic inflammation in Alzheimer’s disease--do they neglect their neurosupportive roles? Mutat. Res., 2010, 690(1-2), 40-49.
[http://dx.doi.org/10.1016/j.mrfmmm.2009.08.016] [PMID: 19748514]
[38]
Romero, J.; Muñiz, J.; Logica, T.T.; Holubiec, M.; González, J.; Barreto, G.E.; Guelman, L.; Lillig, C.H.; Blanco, E.; Capani, F. Dual role of astrocytes in perinatal asphyxia injury and neuroprotection. Neurosci. Lett., 2014, 565, 42-46.
[http://dx.doi.org/10.1016/j.neulet.2013.10.046] [PMID: 24172702]
[39]
Lee, K.M.; MacLean, A.G. New advances on glial activation in health and disease. World J. Virol., 2015, 4(2), 42-55.
[http://dx.doi.org/10.5501/wjv.v4.i2.42] [PMID: 25964871]
[40]
Sullivan, S.M.; Björkman, S.T.; Miller, S.M.; Colditz, P.B.; Pow, D.V. Morphological changes in white matter astrocytes in response to hypoxia/ischemia in the neonatal pig. Brain Res., 2010, 1319, 164-174.
[http://dx.doi.org/10.1016/j.brainres.2010.01.010] [PMID: 20079338]
[41]
Hirayama, Y.; Koizumi, S. Astrocytes and ischemic tolerance. Neurosci. Res., 2018, 126, 53-59.
[42]
Sofroniew, M.V. Astrocyte barriers to neurotoxic inflammation. Nat. Rev. Neurosci., 2015, 16(5), 249-263.
[http://dx.doi.org/10.1038/nrn3898]
[43]
Rice, J.E., III; Vannucci, R.C.; Brierley, J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol., 1981, 9(2), 131-141.
[http://dx.doi.org/10.1002/ana.410090206] [PMID: 7235629]
[44]
Derrick, M.; Drobyshevsky, A.; Ji, X.; Tan, S. A model of cerebral palsy from fetal hypoxia-ischemia. Stroke, 2007, 38(2)(Suppl.), 731-735.
[http://dx.doi.org/10.1161/01.STR.0000251445.94697.64] [PMID: 17261727]
[45]
Kida, H.; Nomura, S.; Shinoyama, M.; Ideguchi, M.; Owada, Y.; Suzuki, M. The effect of hypothermia therapy on cortical laminar disruption following ischemic injury in neonatal mice. PLoS One, 2013, 8(7), e68877.
[http://dx.doi.org/10.1371/journal.pone.0068877] [PMID: 23894362]
[46]
Lin, E.P.; Miles, L.; Hughes, E.A.; McCann, J.C.; Vorhees, C.V.; McAuliffe, J.J.; Loepke, A.W. A combination of mild hypothermia and sevoflurane affords long-term protection in a modified neonatal mouse model of cerebral hypoxia-ischemia. Anesth. Analg., 2014, 119(5), 1158-1173.
[http://dx.doi.org/10.1213/ANE.0000000000000262] [PMID: 24878681]
[47]
Reddy, K.; Mallard, C.; Guan, J.; Marks, K.; Bennet, L.; Gunning, M.; Gunn, A.; Gluckman, P.; Williams, C. Maturational change in the cortical response to hypoperfusion injury in the fetal sheep. Pediatr. Res., 1998, 43(5), 674-682.
[http://dx.doi.org/10.1203/00006450-199805000-00017] [PMID: 9585015]
[48]
Domnguez, R.; Zitting, M.; Liu, Q.; Patel, A.; Babadjouni, R.; Hodis, D.M.; Chow, R.H.; Mack, W.J. Estradiol protects white matter of male C57BL6J mice against experimental chronic cerebral hypoperfusion. J. Stroke Cerebrovasc. Dis., 2018, 27(7), 1743-1751.
[49]
Derrick, M.; Drobyshevsky, A.; Ji, X.; Chen, L.; Yang, Y.; Ji, H.; Silverman, R.B.; Tan, S. Hypoxia-ischemia causes persistent movement deficits in a perinatal rabbit model of cerebral palsy: assessed by a new swim test. Int. J. Dev. Neurosci., 2009, 27(6), 549-557.
[http://dx.doi.org/10.1016/j.ijdevneu.2009.06.008] [PMID: 19573586]
[50]
Traudt, C.M.; McPherson, R.J.; Bauer, L.A.; Richards, T.L.; Burbacher, T.M.; McAdams, R.M.; Juul, S.E. Concurrent erythropoietin and hypothermia treatment improve outcomes in a term nonhuman primate model of perinatal asphyxia. Dev. Neurosci., 2013, 35(6), 491-503.
[http://dx.doi.org/10.1159/000355460] [PMID: 24192275]
[51]
Anju, T.R.; Paulose, C.S. Amelioration of hypoxia-induced striatal 5-HT(2A) receptor, 5-HT transporter and HIF1 alterations by glucose, oxygen and epinephrine in neonatal rats. Neurosci. Lett., 2011, 502(3), 129-132.
[http://dx.doi.org/10.1016/j.neulet.2011.05.236] [PMID: 21683764]
[52]
Anju, T.R.; Paulose, C.S. Striatal cholinergic functional alterations in hypoxic neonatal rats: role of glucose, oxygen, and epinephrine resuscitation. Biochem. Cell Biol., 2013, 91(5), 350-356.
[http://dx.doi.org/10.1139/bcb-2012-0102] [PMID: 24032686]
[53]
Rodriguez-Alvarez, N.; Jimenez-Mateos, E.M.; Dunleavy, M.; Waddington, J.L.; Boylan, G.B.; Henshall, D.C. Effects of hypoxia-induced neonatal seizures on acute hippocampal injury and later-life seizure susceptibility and anxiety-related behavior in mice. Neurobiol. Dis., 2015, 83, 100-114.
[http://dx.doi.org/10.1016/j.nbd.2015.08.023] [PMID: 26341542]
[54]
Sampath, D.; Shmueli, D.; White, A.M.; Raol, Y.H. Flupirtine effectively prevents development of acute neonatal seizures in an animal model of global hypoxia. Neurosci. Lett., 2015, 607, 46-51.
[http://dx.doi.org/10.1016/j.neulet.2015.09.005] [PMID: 26365409]
[55]
Helmy, M.M.; Tolner, E.A.; Vanhatalo, S.; Voipio, J.; Kaila, K. Brain alkalosis causes birth asphyxia seizures, suggesting therapeutic strategy. Ann. Neurol., 2011, 69(3), 493-500.
[http://dx.doi.org/10.1002/ana.22223] [PMID: 21337602]
[56]
Herrera, M.I.; Udovin, L.D.; Toro-Urrego, N.; Kusnier, C.F.; Luaces, J.P.; Capani, F. Palmitoylethanolamide ameliorates hippocampal damage and behavioral dysfunction after perinatal asphyxia in the immature rat brain. Front. Neurosci., 2018, 12, 145.
[http://dx.doi.org/10.3389/fnins.2018.00145] [PMID: 29662433]
[57]
Herrera, M.I.; Otero-Losada, M.; Udovin, L.D.; Kusnier, C.; Kölliker-Frers, R.; de Souza, W.; Capani, F. Could perinatal asphyxia induce a synaptopathy? new highlights from an experimental model. Neural Plast., 2017, 20173436943.
[http://dx.doi.org/10.1155/2017/3436943] [PMID: 28326198]
[58]
Tan, W.K.M.; Williams, C.E.; Gunn, A.J.; Mallard, C.E.; Gluckman, P.D. Suppression of postischemic epileptiform activity with MK-801 improves neural outcome in fetal sheep. Ann. Neurol., 1992, 32(5), 677-682.
[http://dx.doi.org/10.1002/ana.410320511] [PMID: 1449248]
[59]
Gunn, A.J.; Gunn, T.R.; de Haan, H.H.; Williams, C.E.; Gluckman, P.D. Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J. Clin. Invest., 1997, 99(2), 248-256.
[http://dx.doi.org/10.1172/JCI119153] [PMID: 9005993]
[60]
Mallard, E.C.; Williams, C.E.; Johnston, B.M.; Gluckman, P.D. Increased vulnerability to neuronal damage after umbilical cord occlusion in fetal sheep with advancing gestation. Am. J. Obstet. Gynecol., 1994, 170(1 Pt 1), 206-214.
[http://dx.doi.org/10.1016/S0002-9378(94)70409-0] [PMID: 8296824]
[61]
Thoresen, M.; Penrice, J.; Lorek, A.; Cady, E.B.; Wylezinska, M.; Kirkbride, V.; Cooper, C.E.; Brown, G.C.; Edwards, A.D.; Wyatt, J.S. Mild hypothermia after severe transient hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr. Res., 1995, 37(5), 667-670.
[http://dx.doi.org/10.1203/00006450-199505000-00019] [PMID: 7603788]
[62]
Laptook, A.R.; Hassan, A.; Peterson, J.; Corbett, R.J.; Nunnally, R.L. Effects of repeated ischemia on cerebral blood flow and brain energy metabolism. NMR Biomed., 1988, 1(2), 74-79.
[http://dx.doi.org/10.1002/nbm.1940010204] [PMID: 3275028]
[63]
Gressens, P.; Marret, S.; Evrard, P. Developmental spectrum of the excitotoxic cascade induced by ibotenate: A model of hypoxic insults in fetuses and neonates. Neuropathol. Appl. Neurobiol., 2018, 22(6), 498-502.
[64]
Baud, O.; Daire, J-L.; Dalmaz, Y.; Fontaine, R.H.; Krueger, R.C.; Sebag, G.; Evrard, P.; Gressens, P.; Verney, C. Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol., 2004, 14(1), 1-10.
[http://dx.doi.org/10.1111/j.1750-3639.2004.tb00492.x] [PMID: 14997932]
[65]
Sheldon, R.A.; Chuai, J.; Ferriero, D.M. A rat model for hypoxic-ischemic brain damage in very premature infants. Biol. Neonate, 1996, 69(5), 327-341.
[http://dx.doi.org/10.1159/000244327] [PMID: 8790911]
[66]
Back, S.A.; Han, B.H.; Luo, N.L.; Chricton, C.A.; Xanthoudakis, S.; Tam, J.; Arvin, K.L.; Holtzman, D.M. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci., 2002, 22(2), 455-463.
[http://dx.doi.org/10.1523/JNEUROSCI.22-02-00455.2002] [PMID: 11784790]
[67]
Yang, D.; Sun, Y-Y.; Bhaumik, S.K.; Li, Y.; Baumann, J.M.; Lin, X.; Zhang, Y.; Lin, S-H.; Dunn, R.S.; Liu, C-Y.; Shie, F.S.; Lee, Y.H.; Wills-Karp, M.; Chougnet, C.A.; Kallapur, S.G.; Lewkowich, I.P.; Lindquist, D.M.; Murali-Krishna, K.; Kuan, C.Y. Blocking lymphocyte trafficking with FTY720 prevents inflammation-sensitized hypoxic-ischemic brain injury in newborns. J. Neurosci., 2014, 34(49), 16467-16481.
[68]
Sheldon, R.A.; Jiang, X.; Francisco, C.; Christen, S.; Vexler, Z.S.; Täuber, M.G.; Ferriero, D.M. Manipulation of antioxidant pathways in neonatal murine brain. Pediatr. Res., 2004, 56(4), 656-662.
[http://dx.doi.org/10.1203/01.PDR.0000139413.27864.50] [PMID: 15295091]
[69]
Doverhag, C.; Hedtjärn, M.; Poirier, F.; Mallard, C.; Hagberg, H.; Karlsson, A.; Sävman, K. Galectin-3 contributes to neonatal hypoxic-ischemic brain injury. Neurobiol. Dis., 2010, 38(1), 36-46.
[http://dx.doi.org/10.1016/j.nbd.2009.12.024] [PMID: 20053377]
[70]
Ek, C.J.; D’Angelo, B.; Baburamani, A.A.; Lehner, C.; Leverin, A-L.; Smith, P.L.; Nilsson, H.; Svedin, P.; Hagberg, H.; Mallard, C. Brain barrier properties and cerebral blood flow in neonatal mice exposed to cerebral hypoxia-ischemia. J. Cereb. Blood Flow Metab., 2015, 35(5), 818-827.
[http://dx.doi.org/10.1038/jcbfm.2014.255] [PMID: 25627141]
[71]
Hagberg, H.; Mallard, C.; Ferriero, D.M.; Vannucci, S.J.; Levison, S.W.; Vexler, Z.S.; Gressens, P. The role of inflammation in perinatal brain injury. Nat. Rev. Neurol., 2015, 11(4), 192-208.
[http://dx.doi.org/10.1038/nrneurol.2015.13] [PMID: 25686754]
[72]
Renolleau, S.; Aggoun-Zouaoui, D.; Ben-Ari, Y.; Charriaut-Marlangue, C. A model of transient unilateral focal ischemia with reperfusion in the P7 neonatal rat: morphological changes indicative of apoptosis. Stroke, 1998, 29(7), 1454-1460.
[http://dx.doi.org/10.1161/01.STR.29.7.1454] [PMID: 9660403]
[73]
Derugin, N.; Ferriero, D.M.; Vexler, Z.S. Neonatal reversible focal cerebral ischemia: a new model. Neurosci. Res., 1998, 32(4), 349-353.
[http://dx.doi.org/10.1016/S0168-0102(98)00096-0] [PMID: 9950062]
[74]
Fernández-López, D.; Faustino, J.; Daneman, R.; Zhou, L.; Lee, S.Y.; Derugin, N.; Wendland, M.F.; Vexler, Z.S. Blood-brain barrier permeability is increased after acute adult stroke but not neonatal stroke in the rat. J. Neurosci., 2012, 32(28), 9588-9600.
[http://dx.doi.org/10.1523/JNEUROSCI.5977-11.2012] [PMID: 22787045]
[75]
Faustino, J.V.; Wang, X.; Johnson, C.E.; Klibanov, A.; Derugin, N.; Wendland, M.F.; Vexler, Z.S. Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J. Neurosci., 2011, 31(36), 12992-13001.
[http://dx.doi.org/10.1523/JNEUROSCI.2102-11.2011] [PMID: 21900578]
[76]
Mu, D.; Jiang, X.; Sheldon, R.A.; Fox, C.K.; Hamrick, S.E.G.; Vexler, Z.S.; Ferriero, D.M. Regulation of hypoxia-inducible factor 1alpha and induction of vascular endothelial growth factor in a rat neonatal stroke model. Neurobiol. Dis., 2003, 14(3), 524-534.
[http://dx.doi.org/10.1016/j.nbd.2003.08.020] [PMID: 14678768]
[77]
Woo, M-S.; Wang, X.; Faustino, J.V.; Derugin, N.; Wendland, M.F.; Zhou, P.; Iadecola, C.; Vexler, Z.S. Genetic deletion of CD36 enhances injury after acute neonatal stroke. Ann. Neurol., 2012, 72(6), 961-970.
[http://dx.doi.org/10.1002/ana.23727] [PMID: 23280844]
[78]
Elkordy, A.; Mishima, E.; Niizuma, K.; Akiyama, Y.; Fujimura, M.; Tominaga, T.; Abe, T. Stress-induced tRNA cleavage and tiRNA generation in rat neuronal PC12 cells. J. Neurochem., 2018, 146(5), 560-569.
[http://dx.doi.org/10.1111/jnc.14321] [PMID: 29431851]
[79]
Chen, Y.; Zhang, J.; Zhang, X.Y. 2-NBDG as a marker for detecting glucose uptake in reactive astrocytes exposed to oxygen-glucose deprivation in vitro. J. Mol. Neurosci., 2015, 55(1), 126-130.
[http://dx.doi.org/10.1007/s12031-014-0385-5] [PMID: 25091860]
[80]
Cui, X.; Fu, Z.; Wang, M.; Nan, X.; Zhang, B. Pitavastatin treatment induces neuroprotection through the BDNF-TrkB signalling pathway in cultured cerebral neurons after oxygen-glucose deprivation. Neurol. Res., 2018, 40(5), 391-397.
[81]
Dong, Y-F.; Guo, R-B.; Ji, J.; Cao, L-L.; Zhang, L.; Chen, Z-Z.; Huang, J-Y.; Wu, J.; Lu, J.; Sun, X-L. S1PR3 is essential for phosphorylated fingolimod to protect Astrocytes against oxygen-glucose deprivation-induced neuroinflammation via inhibiting TLR2/4-NFκB signalling. J. Cell. Mol. Med., 2018, 22(6), 3159-3166.
[82]
Feng, S-J.; Zhang, X-Q.; Li, J-T.; Dai, X-M.; Zhao, F. miRNA-223 regulates ischemic neuronal injury by targeting the type 1 insulin-like growth factor receptor (IGF1R). Folia Neuropathol., 2018, 56(1), 49-57.
[http://dx.doi.org/10.5114/fn.2018.74659] [PMID: 29663740]
[83]
Guo, M.; Wang, X.; Zhao, Y.; Yang, Q.; Ding, H.; Dong, Q.; Chen, X.; Cui, M. Ketogenic diet improves brain ischemic tolerance and inhibits NLRP3 inflammasome activation by preventing Drp1-mediated mitochondrial fission and endoplasmic reticulum Stress. Front. Mol. Neurosci., 2018, 11, 86.
[http://dx.doi.org/10.3389/fnmol.2018.00086] [PMID: 29662437]
[84]
He, W.; Liu, Y.; Tian, X. Rosuvastatin improves neurite outgrowth of cortical neurons against oxygen-glucose deprivation via Notch1-mediated mitochondrial biogenesis and functional improvement. Front. Cell. Neurosci., 2018, 12, 6.
[http://dx.doi.org/10.3389/fncel.2018.00006] [PMID: 29387001]
[85]
Kim, M.; Jung, K.; Kim, I-S.; Lee, I-S.; Ko, Y.; Shin, J.E.; Park, K.I. TNF-α induces human neural progenitor cell survival after oxygen-glucose deprivation by activating the NF-κB pathway. Exp. Mol. Med., 2018, 50(4), 14.
[http://dx.doi.org/10.1038/s12276-018-0033-1] [PMID: 29622770]
[86]
Li, Y.; Zhao, Y.; Cheng, M.; Qiao, Y.; Wang, Y.; Xiong, W.; Yue, W. Suppression of microRNA-144-3p attenuates oxygen-glucose deprivation/reoxygenation-induced neuronal injury by promoting Brg1/Nrf2/ARE signaling. J. Biochem. Mol. Toxicol., 2018, 32(4), e22044.
[http://dx.doi.org/10.1002/jbt.22044] [PMID: 29457851]
[87]
Wang, K.; Zhu, Y. Dexmedetomidine protects against oxygen-glucose deprivation/reoxygenation injury-induced apoptosis via the p38 MAPK/ERK signalling pathway. J. Int. Med. Res., 2018, 46(2), 675-686.
[http://dx.doi.org/10.1177/0300060517734460] [PMID: 29210287]
[88]
Weng, Y.; Lin, J.; Liu, H.; Wu, H.; Yan, Z.; Zhao, J. AMPK activation by Tanshinone IIA protects neuronal cells from oxygen-glucose deprivation. Oncotarget, 2017, 9(4), 4511-4521.
[PMID: 29435120]
[89]
Yin, X.; Feng, L.; Ma, D.; Yin, P.; Wang, X.; Hou, S.; Hao, Y.; Zhang, J.; Xin, M.; Feng, J. Roles of astrocytic connexin-43, hemichannels, and gap junctions in oxygen-glucose deprivation/reperfusion injury induced neuroinflammation and the possible regulatory mechanisms of salvianolic acid B and carbenoxolone. J. Neuroinflamm, 2018, 15(1), 97.
[http://dx.doi.org/10.1186/s12974-018-1127-3] [PMID: 29587860]
[90]
Zhao, X.; Zhou, K-S.; Li, Z-H.; Nan, W.; Wang, J.; Xia, Y-Y.; Zhang, H-H. Knockdown of Ski decreased the reactive astrocytes proliferation in vitro induced by oxygen-glucose deprivation/reoxygenation. J. Cell. Biochem., 2018, 119(6), 4548-4558.
[http://dx.doi.org/10.1002/jcb.26597] [PMID: 29236326]
[91]
Zhou, T.; Lin, H.; Jiang, L.; Yu, T.; Zeng, C.; Liu, J.; Yang, Z. Mild hypothermia protects hippocampal neurons from oxygen-glucose deprivation injury through inhibiting caspase-3 activation. Cryobiology, 2018, 80, 55-61.
[92]
Bae, S.; Jeong, H.J.; Cha, H.J.; Kim, K.; Choi, Y.M.; An, I.S.; Koh, H.J.; Lim, D.J.; Lee, S.J.; An, S. The hypoxia-mimetic agent cobalt chloride induces cell cycle arrest and alters gene expression in U266 multiple myeloma cells. Int. J. Mol. Med., 2012, 30(5), 1180-1186.
[http://dx.doi.org/10.3892/ijmm.2012.1115] [PMID: 22941251]
[93]
Guo, M.; Song, L-P.; Jiang, Y.; Liu, W.; Yu, Y.; Chen, G-Q. Hypoxia-mimetic agents desferrioxamine and cobalt chloride induce leukemic cell apoptosis through different hypoxia-inducible factor-1α independent mechanisms. Apoptosis, 2006, 11(1), 67-77.
[http://dx.doi.org/10.1007/s10495-005-3085-3] [PMID: 16374551]
[94]
Al Okail, M.S. Cobalt chloride, a chemical inducer of hypoxia-inducible factor-1α in U251 human glioblastoma cell line. J. Saudi Chem. Soc., 2010, 14(2), 197-201.
[http://dx.doi.org/10.1016/j.jscs.2010.02.005]
[95]
Elstner, A.; Holtkamp, N.; von Deimling, A. Involvement of Hif-1 in desferrioxamine-induced invasion of glioblastoma cells. Clin. Exp. Metastasis, 2007, 24(1), 57-66.
[http://dx.doi.org/10.1007/s10585-007-9057-y] [PMID: 17357815]
[96]
Guo, C.; Hao, L-J.; Yang, Z-H.; Chai, R.; Zhang, S.; Gu, Y.; Gao, H-L.; Zhong, M-L.; Wang, T.; Li, J-Y.; Wang, Z.Y. Deferoxamine-mediated up-regulation of HIF-1α prevents dopaminergic neuronal death via the activation of MAPK family proteins in MPTP-treated mice. Exp. Neurol., 2016, 280, 13-23.
[97]
Hamrick, S.E.G.; McQuillen, P.S.; Jiang, X.; Mu, D.; Madan, A.; Ferriero, D.M. A role for hypoxia-inducible factor-1α in desferoxamine neuroprotection. Neurosci. Lett., 2005, 379(2), 96-100.
[http://dx.doi.org/10.1016/j.neulet.2004.12.080] [PMID: 15823423]
[98]
Hishikawa, T.; Ono, S.; Ogawa, T.; Tokunaga, K.; Sugiu, K.; Date, I. Effects of deferoxamine-activated hypoxia-inducible factor-1 on the brainstem after subarachnoid hemorrhage in rats. Neurosurgery, 2008, 62(1), 232-240.
[http://dx.doi.org/10.1227/01.NEU.0000311082.88766.33] [PMID: 18300912]
[99]
Jones, S.M.; Novak, A.E.; Elliott, J.P. The role of HIF in cobalt-induced ischemic tolerance. Neuroscience, 2013, 252, 420-430.
[http://dx.doi.org/10.1016/j.neuroscience.2013.07.060] [PMID: 23916558]
[100]
Li, L.; Yin, X.; Ma, N.; Lin, F.; Kong, X.; Chi, J.; Feng, Z. Desferrioxamine regulates HIF-1 alpha expression in neonatal rat brain after hypoxia-ischemia. Am. J. Transl. Res., 2014, 6(4), 377-383.
[PMID: 25075254]
[101]
Mehrabani, M.; Najafi, M.; Kamarul, T.; Mansouri, K.; Iranpour, M.; Nematollahi, M.H.; Ghazi-Khansari, M.; Sharifi, A.M. Deferoxamine preconditioning to restore impaired HIF-1α-mediated angiogenic mechanisms in adipose-derived stem cells from STZ-induced type 1 diabetic rats. Cell Prolif., 2015, 48(5), 532-549.
[http://dx.doi.org/10.1111/cpr.12209] [PMID: 26332145]
[102]
Mu, D.; Chang, Y.S.; Vexler, Z.S.; Ferriero, D.M. Hypoxia-inducible factor 1α and erythropoietin upregulation with deferoxamine salvage after neonatal stroke. Exp. Neurol., 2005, 195(2), 407-415.
[http://dx.doi.org/10.1016/j.expneurol.2005.06.001] [PMID: 16023639]
[103]
van der Kooij, M.A.; Groenendaal, F.; Kavelaars, A.; Heijnen, C.J.; van Bel, F. Combination of deferoxamine and erythropoietin: Therapy for hypoxia-ischemia-induced brain injury in the neonatal rat? Neurosci. Lett., 2009, 451(2), 109-113.
[http://dx.doi.org/10.1016/j.neulet.2008.12.013] [PMID: 19103262]
[104]
Zeng, H-L.; Zhong, Q.; Qin, Y-L.; Bu, Q-Q.; Han, X-A.; Jia, H-T.; Liu, H-W. Hypoxia-mimetic agents inhibit proliferation and alter the morphology of human umbilical cord-derived mesenchymal stem cells. BMC Cell Biol., 2011, 12(1), 32.
[http://dx.doi.org/10.1186/1471-2121-12-32] [PMID: 21827650]
[105]
Mallard, C.; Vexler, Z.S. Modeling ischemia in the immature brain: How translational are animal models? Stroke, 2015, 46(10), 3006-3011.
[http://dx.doi.org/10.1161/STROKEAHA.115.007776] [PMID: 26272384]
[106]
Wang, Z.; Guo, L.M.; Wang, Y.; Zhou, H.K.; Wang, S.C.; Chen, D.; Huang, J.F.; Xiong, K. Inhibition of HSP90α protects cultured neurons from oxygen-glucose deprivation induced necroptosis by decreasing RIP3 expression. J. Cell. Physiol., 2018, 233(6), 4864-4884.
[http://dx.doi.org/10.1002/jcp.26294] [PMID: 29334122]
[107]
Bordt, E.A. The importance of controlling in vitro oxygen tension to accurately model in vivo neurophysiology. Neurotoxicology, 2018, 66, 213-220.
[http://dx.doi.org/10.1016/j.neuro.2017.10.008] [PMID: 29102646]
[108]
Khan, M.; Khan, H.; Singh, I.; Singh, A.K. Hypoxia inducible factor-1 alpha stabilization for regenerative therapy in traumatic brain injury. Neural Regen. Res., 2017, 12(5), 696-701.
[http://dx.doi.org/10.4103/1673-5374.206632] [PMID: 28616019]
[109]
Semenza, G.L. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr. Opin. Genet. Dev., 1998, 8(5), 588-594.
[http://dx.doi.org/10.1016/S0959-437X(98)80016-6] [PMID: 9794818]
[110]
Ke, Q.; Costa, M. Hypoxia-inducible factor-1 (HIF-1). Mol. Pharmacol., 2006, 70(5), 1469-1480.
[111]
Huang, L.E.; Gu, J.; Schau, M.; Bunn, H.F. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA, 1998, 95(14), 7987-7992.
[http://dx.doi.org/10.1073/pnas.95.14.7987] [PMID: 9653127]
[112]
Wenger, R.H.; Gassmann, M. Oxygen(es) and the hypoxia-inducible factor-1. Biol. Chem., 1997, 378(7), 609-616.
[PMID: 9278140]
[113]
Wang, G.L.; Semenza, G.L. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood, 1993, 82(12), 3610-3615.
[PMID: 8260699]
[114]
Xia, M.; Huang, R.; Sun, Y.; Semenza, G.L.; Aldred, S.F.; Witt, K.L.; Inglese, J.; Tice, R.R.; Austin, C.P. Identification of chemical compounds that induce HIF-1α activity. Toxicol. Sci., 2009, 112(1), 153-163.
[http://dx.doi.org/10.1093/toxsci/kfp123] [PMID: 19502547]
[115]
Huang, B-W.; Miyazawa, M.; Tsuji, Y. Distinct regulatory mechanisms of the human ferritin gene by hypoxia and hypoxia mimetic cobalt chloride at the transcriptional and post-transcriptional levels. Cell. Signal., 2014, 26(12), 2702-2709.
[http://dx.doi.org/10.1016/j.cellsig.2014.08.018] [PMID: 25172425]
[116]
Müller, A.S.; Artner, M.; Janjić, K.; Edelmayer, M.; Kurzmann, C.; Moritz, A.; Agis, H. Synthetic clay-based hypoxia mimetic hydrogel for pulp regeneration: The impact on cell activity and release kinetics based on dental pulp-derived cells In Vitro. J. Endod., 2018, 44(8), 1263-1269.
[http://dx.doi.org/10.1016/j.joen.2018.04.010] [PMID: 29958677]
[117]
Yao, Q.; Liu, Y.; Tao, J.; Baumgarten, K.M.; Sun, H. Hypoxia-mimicking nanofibrous scaffolds promote endogenous bone regeneration. ACS Appl. Mater. Interfaces, 2016, 8(47), 32450-32459.
[http://dx.doi.org/10.1021/acsami.6b10538] [PMID: 27809470]
[118]
Ma, D.; Hossain, M.; Pettet, G.K.; Luo, Y.; Lim, T.; Akimov, S.; Sanders, R.D.; Franks, N.P.; Maze, M. Xenon preconditioning reduces brain damage from neonatal asphyxia in rats. J. Cereb. Blood Flow Metab., 2006, 26(2), 199-208.
[http://dx.doi.org/10.1038/sj.jcbfm.9600184] [PMID: 16034370]
[119]
Hu, Y.; Wang, Z.; Liu, Y.; Pan, S.; Zhang, H.; Fang, M.; Jiang, H.; Yin, J.; Zou, S.; Li, Z.; Zhang, H.; Lin, Z.; Xiao, J. Melatonin Reduces hypoxic-ischaemic (HI) induced autophagy and apoptosis: An in Vivo and in Vitro investigation in experimental models of neonatal HI brain injury. Neurosci. Lett., 2017, 653, 105-112.
[120]
Pabon, M.M.; Borlongan, C.V. Advances in the cell-based treatment of neonatal hypoxic-ischemic brain injury. Future Neurol., 2013, 8(2), 193-203.
[http://dx.doi.org/10.2217/fnl.12.85] [PMID: 23565051]
[121]
Liang, L.; Yang, J.; Jin, X. Cocktail Treatment, a Promising Strategy to Treat Acute Cerebral Ischemic Stroke? Med. Gas Res., 2016, 6(1), 33-38.http://www.medgasres.com/article.asp?issn=2045-9912;year=2016;volume=6;issue=1;spage=33;epage=38;aulast=Liang;t=5
[122]
Drury, P.P.; Gunn, E.R.; Bennet, L.; Gunn, A.J. Mechanisms of hypothermic neuroprotection. Clin. Perinatol., 2014, 41(1), 161-175.
[http://dx.doi.org/10.1016/j.clp.2013.10.005] [PMID: 24524453]
[123]
Liu, J.; Segal, M.R.; Kelly, M.J.S.; Pelton, J.G.; Kim, M.; James, T.L.; Litt, L. 13C NMR metabolomic evaluation of immediate and delayed mild hypothermia in cerebrocortical slices after oxygen-glucose deprivation. Anesthesiology, 2013, 119(5), 1120-1136.
[http://dx.doi.org/10.1097/ALN.0b013e31829c2d90] [PMID: 23748856]
[124]
Nakai, A.; Shibazaki, Y.; Taniuchi, Y.; Oya, A.; Asakura, H.; Kuroda, S.; Koshino, T.; Araki, T. Influence of mild hypothermia on delayed mitochondrial dysfunction after transient intrauterine ischemia in the immature rat brain. Brain Res. Dev. Brain Res., 2001, 128(1), 1-7.
[http://dx.doi.org/10.1016/S0165-3806(01)00138-9] [PMID: 11356256]
[125]
Jacobs, S.E.; Berg, M.; Hunt, R.; Tarnow-Mordi, W.O.; Inder, T.E.; Davis, P.G. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst. Rev., 2013, (1), CD003311.
[http://dx.doi.org/10.1002/14651858.CD003311.pub3] [PMID: 23440789]
[126]
Piironen, K.; Tiainen, M.; Mustanoja, S.; Kaukonen, K-M.; Meretoja, A.; Tatlisumak, T.; Kaste, M. Mild hypothermia after intravenous thrombolysis in patients with acute stroke: a randomized controlled trial. Stroke, 2014, 45(2), 486-491.
[http://dx.doi.org/10.1161/STROKEAHA.113.003180] [PMID: 24436240]
[127]
Gao, X.Y.; Huang, J.O.; Hu, Y.F.; Gu, Y.; Zhu, S.Z.; Huang, K.B.; Chen, J.Y.; Pan, S.Y. Combination of mild hypothermia with neuroprotectants has greater neuroprotective effects during oxygen-glucose deprivation and reoxygenation-mediated neuronal injury. Sci. Rep., 2014, 4, 7091.
[http://dx.doi.org/10.1038/srep07091] [PMID: 25404538]
[128]
Dubrovsky, B.O. Steroids, neuroactive steroids and neurosteroids in psychopathology. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2005, 29(2), 169-192.
[http://dx.doi.org/10.1016/j.pnpbp.2004.11.001] [PMID: 15694225]
[129]
Tuem, K.B.; Atey, T.M. Neuroactive steroids: Receptor interactions and responses. Front. Neurol., 2017, 8, 442.
[http://dx.doi.org/10.3389/fneur.2017.00442] [PMID: 28894435]
[130]
Rey, M.; Coirini, H. Synthetic neurosteroids on brain protection. Neural Regen. Res., 2015, 10(1), 17-21.
[http://dx.doi.org/10.4103/1673-5374.150640] [PMID: 25788907]
[131]
Lizcano, F.; Guzmán, G. Estrogen deficiency and the origin of obesity during menopause. Biomed Res. Int., 2014, 2014, 757461.
[132]
Zhao, L.; O’Neill, K.; Diaz, B.R. Selective estrogen receptor modulators (SERMs) for the brain: Current status and remaining challenges for developing neuroSERMs. Brain Res. Brain Res. Rev., 2005, 49(3), 472-493.
[http://dx.doi.org/10.1016/j.brainresrev.2005.01.009] [PMID: 16269315]
[133]
Paterni, I.; Granchi, C.; Katzenellenbogen, J.A.; Minutolo, F. Estrogen receptors alpha (ERα) and beta (ERβ): Subtype-selective ligands and clinical potential. Steroids, 2014, 90, 13-29.
[134]
Arevalo, M.A.; Azcoitia, I.; Garcia-Segura, L.M. The neuroprotective actions of oestradiol and oestrogen receptors. Nat. Rev. Neurosci., 2015, 16(1), 17-29.
[http://dx.doi.org/10.1038/nrn3856] [PMID: 25423896]
[135]
Shang, Y.; Hu, X.; DiRenzo, J.; Lazar, M.A.; Brown, M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell, 2000, 103(6), 843-852.
[136]
Safe, S.; Kim, K. Non classical genomic ER/Sp and ER/AP-1 signaling pathways. J. Mol. Endocrinol., 2008, 41(5), 263-275.
[http://dx.doi.org/10.1677/JME-08-0103] [PMID: 18772268]
[137]
Ruiz-Palmero, I.; Hernando, M.; Garcia-Segura, L.M.; Arevalo, M-A.G. G protein-coupled estrogen receptor is required for the neuritogenic mechanism of 17β-estradiol in developing hippocampal neurons. Mol. Cell. Endocrinol., 2013, 372(1-2), 105-115.
[http://dx.doi.org/10.1016/j.mce.2013.03.018] [PMID: 23545157]
[138]
Qiu, J.; Bosch, M.A.; Tobias, S.C.; Grandy, D.K.; Scanlan, T.S.; Ronnekleiv, O.K.; Kelly, M.J. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci., 2003, 23(29), 9529-9540.
[http://dx.doi.org/10.1523/JNEUROSCI.23-29-09529.2003] [PMID: 14573532]
[139]
Hammes, S.R.; Davis, P.J. Overlapping nongenomic and genomic actions of thyroid hormone and steroids. Best Pract. Res. Clin. Endocrinol. Metab., 2015, 29(4), 581-593.
[http://dx.doi.org/10.1016/j.beem.2015.04.001] [PMID: 26303085]
[140]
Harvey, B.J.; Condliffe, S.; Doolan, C.M. Sex and salt Hormones: Rapid effects in epithelia. News Physiol. Sci., 2001, 16, 174-177.
[141]
Simoncini, T.; Mannella, P.; Fornari, L.; Caruso, A.; Varone, G.; Genazzani, A.R. Genomic and non-genomic effects of estrogens on endothelial cells. Steroids, 2004, 69(8-9), 537-542.
[http://dx.doi.org/10.1016/j.steroids.2004.05.009] [PMID: 15288766]
[142]
Meldrum, D.R. G-protein-coupled receptor 30 mediates estrogen’s nongenomic effects after hemorrhagic shock and trauma. Am. J. Pathol., 2007, 170(4), 1148-1151.
[http://dx.doi.org/10.2353/ajpath.2007.070025] [PMID: 17392155]
[143]
Lösel, R.; Wehling, M. Nongenomic actions of steroid hormones. Nat. Rev. Mol. Cell Biol., 2003, 4(1), 46-56.
[http://dx.doi.org/10.1038/nrm1009] [PMID: 12511868]
[144]
Fernandez, S.M.; Lewis, M.C.; Pechenino, A.S.; Harburger, L.L.; Orr, P.T.; Gresack, J.E.; Schafe, G.E.; Frick, K.M. Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J. Neurosci., 2008, 28(35), 8660-8667.
[145]
Fan, L.; Zhao, Z.; Orr, P.T.; Chambers, C.H.; Lewis, M.C.; Frick, K.M. Nongenomic actions of steroid hormones. Nat. Rev. Mol. Cell Biol., 2003, 4(1), 46-56.
[146]
Hojo, Y.; Kawato, S. Neurosteroids in adult hippocampus of male and female rodents: Biosynthesis and actions of sex steroids. Front. Endocrinol. (Lausanne), 2018, 9(APR), 183.
[http://dx.doi.org/10.3389/fendo.2018.00183] [PMID: 29740398]
[147]
Tozzi, A.; de Iure, A.; Tantucci, M.; Durante, V.; Quiroga-Varela, A.; Giampà, C.; Di Mauro, M.; Mazzocchetti, P.; Costa, C.; Di Filippo, M.; Grassi, S.; Pettorossi, V.E.; Calabresi, P. Endogenous 17β-estradiol is required for activity-dependent long-term potentiation in the striatum: interaction with the dopaminergic system. Front. Cell. Neurosci., 2015, 9, 192.
[http://dx.doi.org/10.3389/fncel.2015.00192] [PMID: 26074768]
[148]
Pupo, M.; Maggiolini, M.; Musti, A.M. GPER mediates non-genomic effects of estrogen BT - estrogen receptors: Methods and protocols; eyster, K. M; York, S.N., Ed.; New York, NY, 2016, pp. 471-488.
[http://dx.doi.org/10.1007/978-1-4939-3127-9_37]
[149]
Lebesgue, D.; Chevaleyre, V.; Zukin, R.S.; Etgen, A.M. Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids, 2009, 74(7), 555-561.
[http://dx.doi.org/10.1016/j.steroids.2009.01.003] [PMID: 19428444]
[150]
Galbiati, M.; Martini, L.; Melcangi, R.C. Oestrogens, via transforming growth factor α, modulate basic fibroblast growth factor synthesis in hypothalamic astrocytes: in vitro observations. J. Neuroendocrinol., 2002, 14(10), 829-835.
[http://dx.doi.org/10.1046/j.1365-2826.2002.00852.x] [PMID: 12372008]
[151]
Karki, P.; Smith, K.; Johnson, J., Jr; Lee, E. Astrocyte-derived growth factors and estrogen neuroprotection: role of transforming growth factor-α in estrogen-induced upregulation of glutamate transporters in astrocytes. Mol. Cell. Endocrinol., 2014, 389(1-2), 58-64.
[http://dx.doi.org/10.1016/j.mce.2014.01.010] [PMID: 24447465]
[152]
Kirschner, P.B.; Henshaw, R.; Weise, J.; Trubetskoy, V.; Finklestein, S.; Schulz, J.B.; Beal, M.F. Basic fibroblast growth factor protects against excitotoxicity and chemical hypoxia in both neonatal and adult rats. J. Cereb. Blood Flow Metab., 1995, 15(4), 619-623.
[http://dx.doi.org/10.1038/jcbfm.1995.76] [PMID: 7790410]
[153]
Nozaki, K.; Finklestein, S.P.; Beal, M.F. Basic fibroblast growth factor protects against hypoxia-ischemia and NMDA neurotoxicity in neonatal rats. J. Cereb. Blood Flow Metab., 1993, 13(2), 221-228.
[http://dx.doi.org/10.1038/jcbfm.1993.27] [PMID: 8436614]
[154]
Herrera, M. I.; Mucci, S.; Barreto, G. E.; Kolliker-Frers, R.
Capani, F. Neuroprotection in hypoxic-Iischemic brain injury targeting Glial cells. Curr. Pharm. Des., 2017, 23(26), 3899-3906.
[155]
Gerstner, B.; Lee, J.; DeSilva, T.M.; Jensen, F.E.; Volpe, J.J.; Rosenberg, P.A. 17β-estradiol protects against hypoxic/ischemic white matter damage in the neonatal rat brain. J. Neurosci. Res., 2009, 87(9), 2078-2086.
[http://dx.doi.org/10.1002/jnr.22023] [PMID: 19224575]
[156]
Nuñez, J.; Yang, Z.; Jiang, Y.; Grandys, T.; Mark, I.; Levison, S.W. 17β-estradiol protects the neonatal brain from hypoxia-ischemia. Exp. Neurol., 2007, 208(2), 269-276.
[http://dx.doi.org/10.1016/j.expneurol.2007.08.020] [PMID: 17950281]
[157]
Barreto, G.; Saraceno, E.; Gonzalez, J.; Kolliker, R.; Castilla, R.; Capani, F. Neuroprotection with estradiol in experimental perinatal asphyxia: A new approach A2 - duncan, Kelli, A. B.T - Estrogen effects on traumatic brain injury; In: Academic Press: San Diego, 2015, pp. 113-124.
[http://dx.doi.org/10.1016/B978-0-12-801479-0.00008-5]
[158]
Charriaut-Marlangue, C.; Besson, V.C.; Baud, O. Sexually dimorphic outcomes after neonatal stroke and hypoxia-ischemia. Int. J. Mol. Sci., 2017, 19(1), E61.
[http://dx.doi.org/10.3390/ijms19010061] [PMID: 29278365]
[159]
Elzer, J.G.; Muhammad, S.; Wintermantel, T.M.; Regnier-Vigouroux, A.; Ludwig, J.; Schütz, G.; Schwaninger, M. Neuronal estrogen receptor-α mediates neuroprotection by 17β-estradiol. J. Cereb. Blood Flow Metab., 2010, 30(5), 935-942.
[http://dx.doi.org/10.1038/jcbfm.2009.258] [PMID: 20010956]
[160]
Toro-Urrego, N.; Garcia-Segura, L.M.; Echeverria, V.; Barreto, G.E. Testosterone protects mitochondrial function and regulates neuroglobin expression in astrocytic cells exposed to glucose deprivation. Front. Aging Neurosci., 2016, 8, 152.
[http://dx.doi.org/10.3389/fnagi.2016.00152] [PMID: 27445795]
[161]
Nelson, E.R.; Wardell, S.E.; McDonnell, D.P. The molecular mechanisms underlying the pharmacological actions of estrogens, SERMs and oxysterols: implications for the treatment and prevention of osteoporosis. Bone, 2013, 53(1), 42-50.
[http://dx.doi.org/10.1016/j.bone.2012.11.011] [PMID: 23168292]
[162]
Marín, F.; Barbancho, M.C. Action of selective estrogen receptor modulators (SERMs) through the classical mechanism of estrogen action. In: Selective Estrogen Receptor Modulators, 2006, pp. 71- 77.
[163]
Khan, M.M.; Wakade, C.; de Sevilla, L.; Brann, D.W. Selective estrogen receptor modulators (SERMs) enhance neurogenesis and spine density following focal cerebral ischemia. J. Steroid Biochem. Mol. Biol., 2015, 146, 38-47.
[http://dx.doi.org/10.1016/j.jsbmb.2014.05.001] [PMID: 24815952]
[164]
Lopez-Rodriguez, A. B.; Ávila-Rodriguez, M.; Vega-vela, N. E.; Capani, F.; Gonzalez, J.; Garciá-Segura, L. M.; Barreto, G. E. Estrogen Effects on Traumatic Brain Injury, 2015.
[165]
Gao, Y.; Wang, Z.; He, W.; Ma, W.; Ni, X. Mild hypothermia protects neurons against oxygen glucose deprivation via Poly (ADP-Ribose) signaling. J. Matern. Neonatal Med., 2017, 1-7.
[166]
Chakkarapani, E.; Dingley, J.; Liu, X.; Hoque, N.; Aquilina, K.; Porter, H.; Thoresen, M. Xenon enhances hypothermic neuroprotection in asphyxiated newborn pigs. Ann. Neurol., 2010, 68(3), 330-341.
[http://dx.doi.org/10.1002/ana.22016] [PMID: 20658563]
[167]
Kaneko, Y.; Tajiri, N.; Su, T-P.; Wang, Y.; Borlongan, C.V. Combination treatment of hypothermia and mesenchymal stromal cells amplifies neuroprotection in primary rat neurons exposed to hypoxic-ischemic-like injury in vitro: role of the opioid system. PLoS One, 2012, 7(10), e47583.
[http://dx.doi.org/10.1371/journal.pone.0047583] [PMID: 23077646]
[168]
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(5), 256-268.
[169]
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., 2015, 146, 26-37.
[http://dx.doi.org/10.1016/j.jsbmb.2014.05.005] [PMID: 24846829]
[170]
Rzemieniec, J.; Litwa, E.; Wnuk, A.; Lason, W.; Kajta, M. Bazedoxifene and raloxifene protect neocortical neurons undergoing hypoxia via targeting ERα and PPAR-γ. Mol. Cell. Endocrinol., 2018, 461, 64-78.
[http://dx.doi.org/10.1016/j.mce.2017.08.014] [PMID: 28859903]
[171]
Barreto, G.E.; Santos-Galindo, M.; Garcia-Segura, L.M. Selective estrogen receptor modulators regulate reactive microglia after penetrating brain injury. Front. Aging Neurosci., 2014, 6, 132.
[http://dx.doi.org/10.3389/fnagi.2014.00132] [PMID: 24999330]
[172]
Pinto-Almazán, R.; Calzada-Mendoza, C.C.; Campos-Lara, M.G.; Guerra-Araiza, C. Effect of chronic administration of estradiol, progesterone, and tibolone on the expression and phosphorylation of glycogen synthase kinase-3β and the microtubule-associated protein tau in the hippocampus and cerebellum of female rat. J. Neurosci. Res., 2012, 90(4), 878-886.
[http://dx.doi.org/10.1002/jnr.22808] [PMID: 22183707]
[173]
de Aguiar, R.B.; Dickel, O.E.; Cunha, R.W.; Monserrat, J.M.; Barros, D.M.; Martinez, P.E. Estradiol valerate and tibolone: effects upon brain oxidative stress and blood biochemistry during aging in female rats. Biogerontology, 2008, 9(5), 285-298.
[http://dx.doi.org/10.1007/s10522-008-9137-7] [PMID: 18386154]
[174]
Stark, J.; Varbiro, S.; Sipos, M.; Tulassay, Z.; Sara, L.; Adler, I.; Dinya, E.; Magyar, Z.; Szekacs, B.; Marczell, I.; Kloosterboer, H.J.; Racz, K.; Bekesi, G. Antioxidant effect of the active metabolites of tibolone. Gynecol. Endocrinol., 2015, 31(1), 31-35.
[175]
Crespo-Castrillo, A.; Yanguas-Casás, N.; Arevalo, M.A.; Azcoitia, I.; Barreto, G.E.; Garcia-Segura, L.M. The synthetic steroid tibolone decreases reactive gliosis and neuronal death in the cerebral cortex of female mice after a stab wound injury. Mol. Neurobiol., 2018, 55(11), 8651-8667.
[176]
Avila-Rodriguez, M.; Garcia-Segura, L.M.; Hidalgo-Lanussa, O.; Baez, E.; Gonzalez, J.; Barreto, G.E. Tibolone protects astrocytic cells from glucose deprivation through a mechanism involving estrogen receptor beta and the upregulation of neuroglobin expression. Mol. Cell. Endocrinol., 2016, 433, 35-46.
[http://dx.doi.org/10.1016/j.mce.2016.05.024] [PMID: 27250720]
[177]
Oh, J.S.; Kim, S.W.; Cho, H.J.; Kyong, Y.Y.; Oh, Y.M.; Choi, S.M.; Choi, K.H.; Park, K.N. Combination treatment with 17β-estradiol and therapeutic hypothermia for transient global cerebral ischemia in rats. Am. J. Emerg. Med., 2013, 31(1), 154-160.
[http://dx.doi.org/10.1016/j.ajem.2012.06.033] [PMID: 22980365]
[178]
Song, J.; Sun, H.; Xu, F.; Kang, W.; Gao, L.; Guo, J.; Zhang, Y.; Xia, L.; Wang, X.; Zhu, C. Recombinant human erythropoietin improves neurological outcomes in very preterm infants. Ann. Neurol., 2016, 80(1), 24-34.
[http://dx.doi.org/10.1002/ana.24677] [PMID: 27130143]
[179]
Robertson, N.J.; Faulkner, S.; Fleiss, B.; Bainbridge, A.; Andorka, C.; Price, D.; Powell, E.; Lecky-Thompson, L.; Thei, L.; Chandrasekaran, M.; Hristova, M.; Cady, E.B.; Gressens, P.; Golay, X.; Raivich, G. Melatonin augments hypothermic neuroprotection in a perinatal Asphyxia Model. Brain, 2013, 136(1), 90-105.
[180]
Kim, H.; Koo, Y.S.; Shin, M.J.; Kim, S.; Shin, Y.B.; Choi, B.T.; Yun, Y.J.; Lee, S.; Shin, H.K. Combination of constraint-induced movement therapy with electroacupuncture improves functional recovery following neonatal hypoxic-ischemic brain injury in rats. Biomed Res. Int., 2018, 8638294.
[http://dx.doi.org/10.1155/2018/8638294]
[181]
Jin, X.; Liu, J.; Liu, K.J.; Rosenberg, G.A.; Yang, Y.; Liu, W. Normobaric hyperoxia combined with minocycline provides greater neuroprotection than either alone in transient focal cerebral ischemia. Exp. Neurol., 2013, 240, 9-16.
[http://dx.doi.org/10.1016/j.expneurol.2012.11.018] [PMID: 23195595]
[182]
Nonaka, Y.; Shimazawa, M.; Yoshimura, S.; Iwama, T.; Hara, H. Combination effects of normobaric hyperoxia and edaravone on focal cerebral ischemia-induced neuronal damage in mice. Neurosci. Lett., 2008, 441(2), 224-228.
[http://dx.doi.org/10.1016/j.neulet.2008.06.033] [PMID: 18577423]
[183]
Nonaka, Y.; Koumura, A.; Hyakkoku, K.; Shimazawa, M.; Yoshimura, S.; Iwama, T.; Hara, H. Combination treatment with normobaric hyperoxia and cilostazol protects mice against focal cerebral ischemia-iInduced neuronal damage better than each treatment alone. J. Pharmacol. Exp. Ther., 2009, 330(1), 13-22.

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