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Review Article

Neuroprotective and Neurorestorative Effects of Epo and VEGF: Perspectives for New Therapeutic Approaches to Neurological Diseases

Author(s): Mónica E. Ureña-Guerrero*, José L. Castañeda-Cabral, Martha C. Rivera-Cervantes, Rafael J. Macias-Velez, José J. Jarero-Basulto, Graciela Gudiño-Cabrera and Carlos Beas-Zárate

Volume 26, Issue 12, 2020

Page: [1263 - 1276] Pages: 14

DOI: 10.2174/1381612826666200114104342

Price: $65

Abstract

Background: Erythropoietin (Epo) and vascular endothelial growth factor (VEGF) are two vasoactive molecules with essential trophic effects for brain development. The expression and secretion of both molecules increase in response to neuronal damage and they exert protective and restorative effects, which may also be accompanied by adverse side effects.

Objective: We review the most relevant evidence on the neuroprotective and neurorestorative effects of Epo and VEGF in three of the most frequent neurological disorders, namely, stroke, epilepsy and Alzheimer's disease, to develop new therapeutic approaches.

Methods: Several original scientific manuscripts and reviews that have discussed the evidence in critical way, considering both the beneficial and adverse effects of Epo and VEGF in the selected neurological disorders, were analysed. In addition, throughout this review, we propose several considerations to take into account in the design of therapeutic approaches based on Epo and VEGF signalling.

Results: Although the three selected disorders are triggered by different mechanisms, they evolve through similar processes: excitotoxicity, oxidative stress, neuroinflammation, neuronal death, glial reactivity and vascular remodelling. Epo and VEGF exert neuroprotective and neurorestorative effects by acting on these processes due to their pleiotropism. In general, the evidence shows that both Epo and VEGF reduce neuronal death but that at the vascular level, their effects are contradictory.

Conclusion: Because the Epo and VEGF signalling pathways are connected in several ways, we conclude that more experimental studies, primarily studies designed to thoroughly assess the functional interactions between Epo and VEGF in the brain under both physiological and pathophysiological conditions, are needed.

Keywords: Erythropoietin, VEGF, neuroprotection, neurorestoration, therapeutics, excitotoxicity.

« Previous Next »
[1]
Buemi M, Cavallaro E, Floccari F, et al. The pleiotropic effects of erythropoietin in the central nervous system. J Neuropathol Exp Neurol 2003; 62(3): 228-36.
[http://dx.doi.org/10.1093/jnen/62.3.228] [PMID: 12638727]
[2]
Tipoe GL, Lau TY, Nanji AA, Fung ML. Expression and functions of vasoactive substances regulated by hypoxia-inducible factor-1 in chronic hypoxemia. Cardiovasc Hematol Agents Med Chem 2006; 4(3): 199-218.
[http://dx.doi.org/10.2174/187152506777698290] [PMID: 16842206]
[3]
Jacobson LO, Goldwasser E, Fried W, Plzak L. Role of the kidney in erythropoiesis. Nature 1957; 179(4560): 633-4.
[http://dx.doi.org/10.1038/179633a0] [PMID: 13418752]
[4]
Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983; 219(4587): 983-5.
[http://dx.doi.org/10.1126/science.6823562] [PMID: 6823562]
[5]
Newton SS, Fournier NM, Duman RS. Vascular growth factors in neuropsychiatry. Cell Mol Life Sci 2013; 70(10): 1739-52.
[http://dx.doi.org/10.1007/s00018-013-1281-9] [PMID: 23475069]
[6]
Shibuya M. VEGF-VEGFR signals in health and disease. Biomol Ther (Seoul) 2014; 22(1): 1-9.
[http://dx.doi.org/10.4062/biomolther.2013.113] [PMID: 24596615]
[7]
Wenger RH. Mammalian oxygen sensing, signalling and gene regulation. J Exp Biol 2000; 203(Pt 8): 1253-63.
[PMID: 10729275]
[8]
Fan X, Heijnen CJ, van der Kooij MA, Groenendaal F, van Bel F. The role and regulation of hypoxia-inducible factor-1alpha expression in brain development and neonatal hypoxic-ischemic brain injury. Brain Res Brain Res Rev 2009; 62(1): 99-108.
[http://dx.doi.org/10.1016/j.brainresrev.2009.09.006] [PMID: 19786048]
[9]
Ott C, Martens H, Hassouna I, et al. Widespread expression of erythropoietin receptor in brain and its induction by injury. Mol Med 2015; 21(1): 803-15.
[http://dx.doi.org/10.2119/molmed.2015.00192] [PMID: 26349059]
[10]
Wittko-Schneider IM, Schneider FT, Plate KH. Brain homeostasis: VEGF receptor 1 and 2-two unequal brothers in mind. Cell Mol Life Sci 2013; 70(10): 1705-25.
[http://dx.doi.org/10.1007/s00018-013-1279-3] [PMID: 23475067]
[11]
Martínez-Estrada OM, Rodríguez-Millán E, González-De Vicente E, Reina M, Vilaró S, Fabre M. Erythropoietin protects the in vitro blood-brain barrier against VEGF-induced permeability. Eur J Neurosci 2003; 18(9): 2538-44.
[http://dx.doi.org/10.1046/j.1460-9568.2003.02987.x] [PMID: 14622154]
[12]
Noguchi CT, Asavaritikrai P, Teng R, Jia Y. Role of erythropoietin in the brain. Crit Rev Oncol Hematol 2007; 64(2): 159-71.
[http://dx.doi.org/10.1016/j.critrevonc.2007.03.001] [PMID: 17482474]
[13]
Brines M, Grasso G, Fiordaliso F, et al. Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. Proc Natl Acad Sci USA 2004; 101(41): 14907-12.
[http://dx.doi.org/10.1073/pnas.0406491101] [PMID: 15456912]
[14]
Ostrowski D, Heinrich R. Alternative erythropoietin receptors in the nervous system. J Clin Med 2018; 7(2)E24
[http://dx.doi.org/10.3390/jcm7020024] [PMID: 29393890]
[15]
Gonzalez FF, McQuillen P, Mu D, et al. Erythropoietin enhances long-term neuroprotection and neurogenesis in neonatal stroke. Dev Neurosci 2007; 29(4-5): 321-30.
[http://dx.doi.org/10.1159/000105473] [PMID: 17762200]
[16]
Sola A, Rogido M, Lee BH, Genetta T, Wen TC. Erythropoietin after focal cerebral ischemia activates the Janus kinase-signal transducer and activator of transcription signaling pathway and improves brain injury in postnatal day 7 rats. Pediatr Res 2005; 57(4): 481-7.
[http://dx.doi.org/10.1203/01.PDR.0000155760.88664.06] [PMID: 15718373]
[17]
Quelle FW, Wang D, Nosaka T, et al. Erythropoietin induces activation of Stat5 through association with specific tyrosines on the receptor that are not required for a mitogenic response. Mol Cell Biol 1996; 16(4): 1622-31.
[http://dx.doi.org/10.1128/MCB.16.4.1622] [PMID: 8657137]
[18]
Zhao W, Kitidis C, Fleming MD, Lodish HF, Ghaffari S. Erythropoietin stimulates phosphorylation and activation of GATA-1 via the PI3-kinase/AKT signaling pathway. Blood 2006; 107(3): 907-15.
[http://dx.doi.org/10.1182/blood-2005-06-2516] [PMID: 16204311]
[19]
Brines M, Cerami A. Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J Intern Med 2008; 264(5): 405-32.
[http://dx.doi.org/10.1111/j.1365-2796.2008.02024.x] [PMID: 19017170]
[20]
Wang L, Chopp M, Gregg SR, et al. Neural progenitor cells treated with EPO induce angiogenesis through the production of VEGF. J Cereb Blood Flow Metab 2008; 28(7): 1361-8.
[http://dx.doi.org/10.1038/jcbfm.2008.32] [PMID: 18414495]
[21]
Forostyak S, Jendelova P, Sykova E. The role of mesenchymal stromal cells in spinal cord injury, regenerative medicine and possible clinical applications. Biochimie 2013; 95(12): 2257-70.
[http://dx.doi.org/10.1016/j.biochi.2013.08.004] [PMID: 23994163]
[22]
Carelli S, Giallongo T, Gombalova Z, Merli D, Di Giulio AM, Gorio A. EPO-releasing neural precursor cells promote axonal regeneration and recovery of function in spinal cord traumatic injury. Restor Neurol Neurosci 2017; 35(6): 583-99.
[http://dx.doi.org/10.3233/RNN-170750] [PMID: 29172009]
[23]
Viviani B, Bartesaghi S, Corsini E, et al. Erythropoietin protects primary hippocampal neurons increasing the expression of brain-derived neurotrophic factor. J Neurochem 2005; 93(2): 412-21.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03033.x] [PMID: 15816864]
[24]
Gyetvai G, Hughes T, Wedmore F, et al. Erythropoietin increases myelination in oligodendrocytes: gene expression profiling reveals early induction of genes involved in lipid transport and metabolism. Front Immunol 2017; 8: 1394.
[http://dx.doi.org/10.3389/fimmu.2017.01394] [PMID: 29123527]
[25]
Greenberg DA, Jin K. Vascular endothelial growth factors (VEGFs) and stroke. Cell Mol Life Sci 2013; 70(10): 1753-61.
[http://dx.doi.org/10.1007/s00018-013-1282-8] [PMID: 23475070]
[26]
van Vliet EA, da Costa Araújo S, Redeker S, van Schaik R, Aronica E, Gorter JA. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007; 130(Pt 2): 521-34.
[http://dx.doi.org/10.1093/brain/awl318] [PMID: 17124188]
[27]
Iyer S, Acharya KR. Tying the knot: the cystine signature and molecular-recognition processes of the vascular endothelial growth factor family of angiogenic cytokines. FEBS J 2011; 278(22): 4304-22.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08350.x] [PMID: 21917115]
[28]
Mac Gabhann F, Popel AS. Dimerization of VEGF receptors and implications for signal transduction: a computational study. Biophys Chem 2007; 128(2-3): 125-39.
[http://dx.doi.org/10.1016/j.bpc.2007.03.010] [PMID: 17442480]
[29]
Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 1989; 161(2): 851-8.
[http://dx.doi.org/10.1016/0006-291X(89)92678-8] [PMID: 2735925]
[30]
Dalpe G, Tarsitano M, Persico MG, Zheng H, Culotti J. C. elegans PVF-1 inhibits permissive UNC-40 signalling through CED-10 GTPase to position the male ray 1 sensillum. Development 2013; 140(19): 4020-30.
[http://dx.doi.org/10.1242/dev.095190] [PMID: 24004945]
[31]
Mondal BC, Shim J, Evans CJ, Banerjee U. Pvr expression regulators in equilibrium signal control and maintenance of Drosophila blood progenitors. eLife 2014; 3e03626
[http://dx.doi.org/10.7554/eLife.03626] [PMID: 25201876]
[32]
Heinrich R, Günther V, Miljus N. Erythropoietin-mediated neuroprotection in insects suggests a prevertebrate evolution of erythropoietin-like signaling. Vitam Horm 2017; 105: 181-96.
[http://dx.doi.org/10.1016/bs.vh.2017.02.004] [PMID: 28629517]
[33]
The top 10 causes of death. World Health Organization cited 2019 23 Augupdated 2018 May 23. Available from: https://www.who.int/ news-room/ eelifact-sheets/ detail/the-top-10-causes-of-deathhttps://www.who.int/
[34]
Ginsberg MD. The new language of cerebral ischemia. AJNR Am J Neuroradiol 1997; 18(8): 1435-45.
[PMID: 9296184]
[35]
Fernández-Gómez FJ, Hernández F, Argandoña L, Galindo MF, Segura T, Jordán J. Farmacología de la neuroprotección en el ictus isquémico agudo. Rev Neurol 2008; 47(5): 253-60.
[http://dx.doi.org/10.33588/rn.4705.2008250] [PMID: 18780272]
[36]
Parikh P, Juul SE. Neuroprotective strategies in neonatal brain injury. J Pediatr 2018; 192: 22-32.
[http://dx.doi.org/10.1016/j.jpeds.2017.08.031] [PMID: 29031859]
[37]
Millar LJ, 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]
[38]
Sahota P, Savitz SI. Investigational therapies for ischemic stroke: neuroprotection and neurorecovery. Neurotherapeutics 2011; 8(3): 434-51.
[http://dx.doi.org/10.1007/s13311-011-0040-6] [PMID: 21604061]
[39]
Detante O, Jaillard A, Moisan A, et al. Biotherapies in stroke. Rev Neurol (Paris) 2014; 170(12): 779-98.
[http://dx.doi.org/10.1016/j.neurol.2014.10.005] [PMID: 25459115]
[40]
Dirnagl U. Pathobiology of injury after stroke: the neurovascular unit and beyond. Ann N Y Acad Sci 2012; 1268: 21-5.
[http://dx.doi.org/10.1111/j.1749-6632.2012.06691.x] [PMID: 22994217]
[41]
Zhang ZG, Chopp M. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol 2009; 8(5): 491-500.
[http://dx.doi.org/10.1016/S1474-4422(09)70061-4] [PMID: 19375666]
[42]
Sharp FR, Bernaudin M. HIF1 and oxygen sensing in the brain. Nat Rev Neurosci 2004; 5(6): 437-48.
[http://dx.doi.org/10.1038/nrn1408] [PMID: 15152194]
[43]
Sirén AL, Fasshauer T, Bartels C, Ehrenreich H. Therapeutic potential of erythropoietin and its structural or functional variants in the nervous system. Neurotherapeutics 2009; 6(1): 108-27.
[http://dx.doi.org/10.1016/j.nurt.2008.10.041] [PMID: 19110203]
[44]
Brines ML, Ghezzi P, Keenan S, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 2000; 97(19): 10526-31.
[http://dx.doi.org/10.1073/pnas.97.19.10526] [PMID: 10984541]
[45]
Lapchak PA. Carbamylated erythropoietin to treat neuronal injury: new development strategies. Expert Opin Investig Drugs 2008; 17(8): 1175-86.
[http://dx.doi.org/10.1517/13543784.17.8.1175] [PMID: 18616414]
[46]
Erbayraktar S, Grasso G, Sfacteria A, et al. Asialoerythropoietin is a nonerythropoietic cytokine with broad neuroprotective activity in vivo. Proc Natl Acad Sci USA 2003; 100(11): 6741-6.
[http://dx.doi.org/10.1073/pnas.1031753100] [PMID: 12746497]
[47]
Muir KW, Lees KR. Excitatory amino acid antagonists for acute stroke. Cochrane Database Syst Rev 2003; (3): CD001244
[http://dx.doi.org/10.1002/14651858.CD001244] [PMID: 12917902]
[48]
Kobayashi S, Fukuma S, Ikenoue T, Fukuhara S, Kobayashi S. Effect of edaravone on neurological symptoms in real-world patients with acute ischemic stroke. Stroke 2019; 50(7): 1805-11.
[http://dx.doi.org/10.1161/STROKEAHA.118.024351] [PMID: 31164072]
[49]
Kleinig TJ, Vink R. Suppression of inflammation in ischemic and hemorrhagic stroke: therapeutic options. Curr Opin Neurol 2009; 22(3): 294-301.
[http://dx.doi.org/10.1097/WCO.0b013e32832b4db3] [PMID: 19434798]
[50]
Neuhaus AA, Couch Y, Hadley G, Buchan AM. Neuroprotection in stroke: the importance of collaboration and reproducibility. Brain 2017; 140(8): 2079-92.
[http://dx.doi.org/10.1093/brain/awx126] [PMID: 28641383]
[51]
Gutiérrez M, Merino JJ, Alonso de Leciñana M, Díez-Tejedor E. Cerebral protection, brain repair, plasticity and cell therapy in ischemic stroke. Cerebrovasc Dis 2009; 27(Suppl. 1): 177-86.
[http://dx.doi.org/10.1159/000200457] [PMID: 19342849]
[52]
Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 2003; 4(5): 399-415.
[http://dx.doi.org/10.1038/nrn1106] [PMID: 12728267]
[53]
Alnaeeli M, Wang L, Piknova B, Rogers H, Li X, Noguchi CT. Erythropoietin in brain development and beyond. Anat Res Int 2012; 2012953264
[http://dx.doi.org/10.1155/2012/953264] [PMID: 22567318]
[54]
Byts N, Sirén AL. Erythropoietin: a multimodal neuroprotective agent. Exp Transl Stroke Med 2009; 1: 4.
[http://dx.doi.org/10.1186/2040-7378-1-4] [PMID: 20142991]
[55]
George PM, Steinberg GK. novel stroke therapeutics: unraveling stroke pathophysiology and its impact on clinical treatments. Neuron 2015; 87(2): 297-309.
[http://dx.doi.org/10.1016/j.neuron.2015.05.041] [PMID: 26182415]
[56]
Dash PK, Mach SA, Moore AN. Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J Neurosci Res 2001; 63(4): 313-9.
[http://dx.doi.org/10.1002/1097-4547(20010215)63:4<313:AID-JNR1025>3.0.CO;2-4] [PMID: 11170181]
[57]
Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 2002; 52(6): 802-13.
[http://dx.doi.org/10.1002/ana.10393] [PMID: 12447935]
[58]
Komitova M, Perfilieva E, Mattsson B, Eriksson PS, Johansson BB. Effects of cortical ischemia and postischemic environmental enrichment on hippocampal cell genesis and differentiation in the adult rat. J Cereb Blood Flow Metab 2002; 22(7): 852-60.
[http://dx.doi.org/10.1097/00004647-200207000-00010] [PMID: 12142570]
[59]
Komitova M, Mattsson B, Johansson BB, Eriksson PS. Enriched environment increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of stroke-lesioned adult rats. Stroke 2005; 36(6): 1278-82.
[http://dx.doi.org/10.1161/01.STR.0000166197.94147.59] [PMID: 15879324]
[60]
Bernaudin M, Marti HH, Roussel S, et al. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 1999; 19(6): 643-51.
[http://dx.doi.org/10.1097/00004647-199906000-00007] [PMID: 10366194]
[61]
Shingo T, Sorokan ST, Shimazaki T, Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 2001; 21(24): 9733-43.
[http://dx.doi.org/10.1523/JNEUROSCI.21-24-09733.2001] [PMID: 11739582]
[62]
Iwai M, Cao G, Yin W, Stetler RA, Liu J, Chen J. Erythropoietin promotes neuronal replacement through revascularization and neurogenesis after neonatal hypoxia/ischemia in rats. Stroke 2007; 38(10): 2795-803.
[http://dx.doi.org/10.1161/STROKEAHA.107.483008] [PMID: 17702962]
[63]
Woitke F, Ceanga M, Rudolph M, et al. Adult hippocampal neurogenesis poststroke: More new granule cells but aberrant morphology and impaired spatial memory. PLoS One 2017; 12(9)e0183463
[http://dx.doi.org/10.1371/journal.pone.0183463] [PMID: 28910298]
[64]
Scharfman HE, Hen R. Neuroscience. Is more neurogenesis always better? Science 2007; 315(5810): 336-8.
[http://dx.doi.org/10.1126/science.1138711] [PMID: 17234934]
[65]
Chong ZZ, Kang JQ, Maiese K. Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation 2002; 106(23): 2973-9.
[http://dx.doi.org/10.1161/01.CIR.0000039103.58920.1F] [PMID: 12460881]
[66]
Ribatti D, Vacca A, Roccaro AM, Crivellato E, Presta M. Erythropoietin as an angiogenic factor. Eur J Clin Invest 2003; 33(10): 891-6.
[http://dx.doi.org/10.1046/j.1365-2362.2003.01245.x] [PMID: 14511361]
[67]
Wei L, Erinjeri JP, Rovainen CM, Woolsey TA. Collateral growth and angiogenesis around cortical stroke. Stroke 2001; 32(9): 2179-84.
[http://dx.doi.org/10.1161/hs0901.094282] [PMID: 11546914]
[68]
Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004; 35(7): 1732-7.
[http://dx.doi.org/10.1161/01.STR.0000132196.49028.a4] [PMID: 15178821]
[69]
Nakano M, Satoh K, Fukumoto Y, et al. Important role of erythropoietin receptor to promote VEGF expression and angiogenesis in peripheral ischemia in mice. Circ Res 2007; 100(5): 662-9.
[http://dx.doi.org/10.1161/01.RES.0000260179.43672.fe] [PMID: 17293480]
[70]
Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J Neurosci 2006; 26(50): 13007-16.
[http://dx.doi.org/10.1523/JNEUROSCI.4323-06.2006] [PMID: 17167090]
[71]
Geiseler SJ, Morland C. The janus face of VEGF in stroke. Int J Mol Sci 2018; 19(5): 1-20.
[http://dx.doi.org/10.3390/ijms19051362] [PMID: 29734653]
[72]
Croll SD, Ransohoff RM, Cai N, et al. VEGF-mediated inflammation precedes angiogenesis in adult brain. Exp Neurol 2004; 187(2): 388-402.
[http://dx.doi.org/10.1016/j.expneurol.2004.02.010] [PMID: 15144865]
[73]
Zan L, Zhang X, Xi Y, et al. Src regulates angiogenic factors and vascular permeability after focal cerebral ischemia-reperfusion. Neuroscience 2014; 262: 118-28.
[http://dx.doi.org/10.1016/j.neuroscience.2013.12.060] [PMID: 24412374]
[74]
Jickling GC, Liu D, Stamova B, et al. Hemorrhagic transformation after ischemic stroke in animals and humans. J Cereb Blood Flow Metab 2014; 34(2): 185-99.
[http://dx.doi.org/10.1038/jcbfm.2013.203] [PMID: 24281743]
[75]
Zhang ZG, Zhang L, Tsang W, et al. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 2002; 22(4): 379-92.
[http://dx.doi.org/10.1097/00004647-200204000-00002] [PMID: 11919509]
[76]
Marti HJ, Bernaudin M, Bellail A, et al. Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am J Pathol 2000; 156(3): 965-76.
[http://dx.doi.org/10.1016/S0002-9440(10)64964-4] [PMID: 10702412]
[77]
Han T, Yan J, Chen H, et al. HIF-1α contributes to tube malformation of human lymphatic endothelial cells by upregulating VEGFR-3. Int J Oncol 2019; 54(1): 139-51.
[PMID: 30431105]
[78]
Wang Y, Kilic E, Kilic U, et al. VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena. Brain 2005; 128(Pt 1): 52-63.
[http://dx.doi.org/10.1093/brain/awh325] [PMID: 15509618]
[79]
Bry M, Kivelä R, Leppänen VM, Alitalo K. Vascular endothelial growth factor-B in physiology and disease. Physiol Rev 2014; 94(3): 779-94.
[http://dx.doi.org/10.1152/physrev.00028.2013] [PMID: 24987005]
[80]
Li X, Kumar A, Zhang F, Lee C, Tang Z. Complicated life, complicated VEGF-B. Trends Mol Med 2012; 18(2): 119-27.
[http://dx.doi.org/10.1016/j.molmed.2011.11.006] [PMID: 22178229]
[81]
Sun Y, Jin K, Childs JT, Xie L, Mao XO, Greenberg DA. Increased severity of cerebral ischemic injury in vascular endothelial growth factor-B-deficient mice. J Cereb Blood Flow Metab 2004; 24(10): 1146-52.
[http://dx.doi.org/10.1097/01.WCB.0000134477.38980.38] [PMID: 15529014]
[82]
Sun Y, Jin K, Childs JT, Xie L, Mao XO, Greenberg DA. Vascular endothelial growth factor-B (VEGFB) stimulates neurogenesis: evidence from knockout mice and growth factor administration. Dev Biol 2006; 289(2): 329-35.
[http://dx.doi.org/10.1016/j.ydbio.2005.10.016] [PMID: 16337622]
[83]
Pitkänen A, Sutula TP. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 2002; 1(3): 173-81.
[http://dx.doi.org/10.1016/S1474-4422(02)00073-X] [PMID: 12849486]
[84]
Kobylarek D, Iwanowski P, Lewandowska Z, et al. Advances in the potential biomarkers of epilepsy. Front Neurol 2019; 10: 685.
[http://dx.doi.org/10.3389/fneur.2019.00685] [PMID: 31312171]
[85]
Sloviter RS, Bumanglag AV. Defining “epileptogenesis” and identifying “antiepileptogenic targets” in animal models of acquired temporal lobe epilepsy is not as simple as it might seem. Neuropharmacology 2013; 69: 3-15.
[http://dx.doi.org/10.1016/j.neuropharm.2012.01.022] [PMID: 22342985]
[86]
Devinsky O, Vezzani A, O’Brien TJ, et al. Epilepsy. Nat Rev Dis Primers 2018; 4: 18024.
[http://dx.doi.org/10.1038/nrdp.2018.24] [PMID: 29722352]
[87]
Sutula TP, Hagen J, Pitkänen A. Do epileptic seizures damage the brain? Curr Opin Neurol 2003; 16(2): 189-95.
[http://dx.doi.org/10.1097/00019052-200304000-00012] [PMID: 12644748]
[88]
Noebels JL, Avoli M, Rogawski M, Olsen R, Delgado-Escueta AV. “Jasper’s basic mechanisms of the epilepsies” workshop. Epilepsia 2010; 51(Suppl. 5): 1-5.
[http://dx.doi.org/10.1111/j.1528-1167.2010.02792.x] [PMID: 21208201]
[89]
Feast A, Martinian L, Liu J, Catarino CB, Thom M, Sisodiya SM. Investigation of hypoxia-inducible factor-1α in hippocampal sclerosis: a postmortem study. Epilepsia 2012; 53(8): 1349-59.
[http://dx.doi.org/10.1111/j.1528-1167.2012.03591.x] [PMID: 22812626]
[90]
Li J, Jiang G, Chen Y, et al. Altered expression of hypoxia-Inducible factor-1α participates in the epileptogenesis in animal models. Synapse 2014; 68(9): 402-9.
[http://dx.doi.org/10.1002/syn.21752] [PMID: 24889205]
[91]
Yang J, He F, Meng Q, Sun Y, Wang W, Wang C. Inhibiting HIF-1α decreases expression of TNF-α and caspase-3 in specific brain regions exposed kainic acid-induced status epilepticus. Cell Physiol Biochem 2016; 38(1): 75-82.
[http://dx.doi.org/10.1159/000438610] [PMID: 26741705]
[92]
Li Y, Chen J, Zeng T, Lei D, Chen L, Zhou D. Expression of HIF-1α and MDR1/P-glycoprotein in refractory mesial temporal lobe epilepsy patients and pharmacoresistant temporal lobe epilepsy rat model kindled by coriaria lactone. Neurol Sci 2014; 35(8): 1203-8.
[http://dx.doi.org/10.1007/s10072-014-1681-0] [PMID: 24590840]
[93]
Chin K, Yu X, Beleslin-Cokic B, et al. Production and processing of erythropoietin receptor transcripts in brain. Brain Res Mol Brain Res 2000; 81(1-2): 29-42.
[http://dx.doi.org/10.1016/S0169-328X(00)00157-1] [PMID: 11000476]
[94]
Merelli A, Ramos AJ, Lazarowski A, Auzmendi J. Convulsive stress mimics brain hypoxia and promotes the p-glycoprotein (p-gp) and erythropoietin receptor overexpression. recombinant human erythropoietin effect on P-gp activity. Front Neurosci 2019; 13: 750.
[http://dx.doi.org/10.3389/fnins.2019.00750] [PMID: 31379495]
[95]
Collino M, Thiemermann C, Cerami A, Brines M. Flipping the molecular switch for innate protection and repair of tissues: Long-lasting effects of a non-erythropoietic small peptide engineered from erythropoietin. Pharmacol Ther 2015; 151: 32-40.
[http://dx.doi.org/10.1016/j.pharmthera.2015.02.005] [PMID: 25728128]
[96]
Henshall DC, Simon RP. Epilepsy and apoptosis pathways. J Cereb Blood Flow Metab 2005; 25(12): 1557-72.
[http://dx.doi.org/10.1038/sj.jcbfm.9600149] [PMID: 15889042]
[97]
Maiese K, Li F, Chong ZZ. Erythropoietin in the brain: can the promise to protect be fulfilled? Trends Pharmacol Sci 2004; 25(11): 577-83.
[http://dx.doi.org/10.1016/j.tips.2004.09.006] [PMID: 15491780]
[98]
Brines M, Cerami A. Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci 2005; 6(6): 484-94.
[http://dx.doi.org/10.1038/nrn1687] [PMID: 15928718]
[99]
Morishita E, Masuda S, Nagao M, Yasuda Y, Sasaki R. Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience 1997; 76(1): 105-16.
[http://dx.doi.org/10.1016/S0306-4522(96)00306-5 ] [PMID: 8971763]
[100]
Kondo A, Shingo T, Yasuhara T, et al. Erythropoietin exerts anti-epileptic effects with the suppression of aberrant new cell formation in the dentate gyrus and upregulation of neuropeptide Y in seizure model of rats. Brain Res 2009; 1296: 127-36.
[http://dx.doi.org/10.1016/j.brainres.2009.08.025] [PMID: 19695235]
[101]
Jun Y, JiangTao X, YuanGui H, et al. Erythropoietin pre-treatment prevents cognitive impairments following status epilepticus in rats. Brain Res 2009; 1282: 57-66.
[http://dx.doi.org/10.1016/j.brainres.2009.05.062] [PMID: 19497315]
[102]
Nadam J, Navarro F, Sanchez P, et al. Neuroprotective effects of erythropoietin in the rat hippocampus after pilocarpine-induced status epilepticus. Neurobiol Dis 2007; 25(2): 412-26.
[http://dx.doi.org/10.1016/j.nbd.2006.10.009] [PMID: 17166730]
[103]
Jing M, Shingo T, Yasuhara T, et al. The combined therapy of intrahippocampal transplantation of adult neural stem cells and intraventricular erythropoietin-infusion ameliorates spontaneous recurrent seizures by suppression of abnormal mossy fiber sprouting. Brain Res 2009; 1295: 203-17.
[http://dx.doi.org/10.1016/j.brainres.2009.07.079] [PMID: 19646969]
[104]
Han W, Song X, He R, et al. VEGF regulates hippocampal neurogenesis and reverses cognitive deficits in immature rats after status epilepticus through the VEGF R2 signaling pathway. Epilepsy Behav 2017; 68: 159-67.
[http://dx.doi.org/10.1016/j.yebeh.2016.12.007] [PMID: 28193596]
[105]
Lange C, Storkebaum E, de Almodóvar CR, Dewerchin M, Carmeliet P. Vascular endothelial growth factor: a neurovascular target in neurological diseases. Nat Rev Neurol 2016; 12(8): 439-54.
[http://dx.doi.org/10.1038/nrneurol.2016.88] [PMID: 27364743]
[106]
McCloskey DP, Croll SD, Scharfman HE. Depression of synaptic transmission by vascular endothelial growth factor in adult rat hippocampus and evidence for increased efficacy after chronic seizures. J Neurosci 2005; 25(39): 8889-97.
[http://dx.doi.org/10.1523/JNEUROSCI.2577-05.2005] [PMID: 16192378]
[107]
Lenzer-Fanara JR, Li T, Salerni EA, Payen F, Croll SD. VEGF treatment during status epilepticus attenuates long-term seizure-associated alterations in astrocyte morphology Epilepsy Behav 2017; 70(Pt A): 33-44.
[http://dx.doi.org/10.1016/j.yebeh.2017.02.019] [PMID: 28410463]
[108]
Kou ZW, Mo JL, Wu KW, et al. Vascular endothelial growth factor increases the function of calcium-impermeable AMPA receptor GluA2 subunit in astrocytes via activation of protein kinase C signaling pathway. Glia 2019; 67(7): 1344-58.
[http://dx.doi.org/10.1002/glia.23609] [PMID: 30883902]
[109]
Vazquez-Valls E, Flores-Soto ME, Chaparro-Huerta V, et al. HIF-1α expression in the hippocampus and peripheral macrophages after glutamate-induced excitotoxicity. J Neuroimmunol 2011; 238(1-2): 12-8.
[http://dx.doi.org/10.1016/j.jneuroim.2011.06.001] [PMID: 21807419]
[110]
Castañeda-Cabral JL, Beas-Zarate C, Gudiño-Cabrera G, Ureña-Guerrero ME. Glutamate neonatal excitotoxicity modifies VEGF-A, VEGF-B, VEGFR-1 and VEGFR-2 Protein expression profiles during postnatal development of the cerebral cortex and hippocampus of male rats. J Mol Neurosci 2017; 63(1): 17-27.
[http://dx.doi.org/10.1007/s12031-017-0952-7] [PMID: 28755050]
[111]
Nicoletti JN, Shah SK, McCloskey DP, et al. Vascular endothelial growth factor is up-regulated after status epilepticus and protects against seizure-induced neuronal loss in hippocampus. Neuroscience 2008; 151(1): 232-41.
[http://dx.doi.org/10.1016/j.neuroscience.2007.09.083] [PMID: 18065154]
[112]
Nicoletti JN, Lenzer J, Salerni EA, et al. Vascular endothelial growth factor attenuates status epilepticus-induced behavioral impairments in rats. Epilepsy Behav 2010; 19(3): 272-7.
[http://dx.doi.org/10.1016/j.yebeh.2010.07.011] [PMID: 20801723]
[113]
Morin-Brureau M, Lebrun A, Rousset MC, et al. Epileptiform activity induces vascular remodeling and zonula occludens 1 downregulation in organotypic hippocampal cultures: role of VEGF signaling pathways. J Neurosci 2011; 31(29): 10677-88.
[http://dx.doi.org/10.1523/JNEUROSCI.5692-10.2011] [PMID: 21775611]
[114]
Nikitidou L, Kanter-Schlifke I, Dhondt J, Carmeliet P, Lambrechts D, Kokaia M. VEGF receptor-2 (Flk-1) overexpression in mice counteracts focal epileptic seizures. PLoS One 2012; 7(7)e40535
[http://dx.doi.org/10.1371/journal.pone.0040535] [PMID: 22808185]
[115]
Cho KO, Kim JY, Jeong KH, Lee MY, Kim SY. Increased expression of vascular endothelial growth factor-C and vascular endothelial growth factor receptor-3 after pilocarpine-induced status epilepticus in mice. Korean J Physiol Pharmacol 2019; 23(4): 281-9.
[http://dx.doi.org/10.4196/kjpp.2019.23.4.281] [PMID: 31297012]
[116]
Park H, Choi SH, Kong MJ, Kang TC. Dysfunction of 67-kDa laminin receptor disrupts BBB integrity via Impaired dystrophin/AQP4 complex and p38 MAPK/VEGF activation following status epilepticus. Front Cell Neurosci 2019; 13: 236.
[http://dx.doi.org/10.3389/fncel.2019.00236] [PMID: 31178701]
[117]
Rigau V, Morin M, Rousset MC, et al. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 2007; 130(Pt 7): 1942-56.
[http://dx.doi.org/10.1093/brain/awm118] [PMID: 17533168]
[118]
Sun FJ, Wei YJ, Li S, et al. Elevated expression of VEGF-C and its receptors, VEGFR-2 and VEGFR-3, in patients with mesial temporal lobe epilepsy. J Mol Neurosci 2016; 59(2): 241-50.
[http://dx.doi.org/10.1007/s12031-016-0714-y] [PMID: 26798047]
[119]
Castañeda-Cabral JL, Beas-Zárate C, Rocha-Arrieta LL, et al. Increased protein expression of VEGF-A, VEGF-B, VEGF-C and their receptors in the temporal neocortex of pharmacoresistant temporal lobe epilepsy patients. J Neuroimmunol 2019; 328: 68-72.
[http://dx.doi.org/10.1016/j.jneuroim.2018.12.007] [PMID: 30597392]
[120]
Tolosa L, Mir M, Asensio VJ, Olmos G, Lladó J. Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J Neurochem 2008; 105(4): 1080-90.
[http://dx.doi.org/10.1111/j.1471-4159.2007.05206.x] [PMID: 18182045]
[121]
Zhang Z, Yu D, Yin D, Wang Z. Activation of PI3K/mTOR signaling pathway contributes to induction of vascular endothelial growth factor by hCG in bovine developing luteal cells. Anim Reprod Sci 2011; 125(1-4): 42-8.
[http://dx.doi.org/10.1016/j.anireprosci.2011.03.002] [PMID: 21477953]
[122]
Benini R, Roth R, Khoja Z, Avoli M, Wintermark P. Does angiogenesis play a role in the establishment of mesial temporal lobe epilepsy? Int J Dev Neurosci 2016; 49: 31-6.
[http://dx.doi.org/10.1016/j.ijdevneu.2016.01.001] [PMID: 26773167]
[123]
Kim JE, Kang TC. TRPC3- and ETB receptor-mediated PI3K/AKT activation induces vasogenic edema formation following status epilepticus.Brain Res 2017. 1672-58-64.
[124]
Ndode-Ekane XE, Hayward N, Gröhn O, Pitkänen A. Vascular changes in epilepsy: functional consequences and association with network plasticity in pilocarpine-induced experimental epilepsy. Neuroscience 2010; 166(1): 312-32.
[http://dx.doi.org/10.1016/j.neuroscience.2009.12.002] [PMID: 20004712]
[125]
Devinsky O, Vezzani A, Najjar S, De Lanerolle NC, Rogawski MA. Glia and epilepsy: excitability and inflammation. Trends Neurosci 2013; 36(3): 174-84.
[http://dx.doi.org/10.1016/j.tins.2012.11.008] [PMID: 23298414]
[126]
Marchi N, Lerner-Natoli M. Cerebrovascular remodeling and epilepsy. Neuroscientist 2013; 19(3): 304-12.
[http://dx.doi.org/10.1177/1073858412462747] [PMID: 23072899]
[127]
Sweeney MD, Zhao Z, Montagne A, Nelson AR, Zlokovic BV. Blood-brain barrier: from physiology to disease and back. Physiol Rev 2019; 99(1): 21-78.
[http://dx.doi.org/10.1152/physrev.00050.2017] [PMID: 30280653]
[128]
Grabenstatter HL, Del Angel YC, Carlsen J, et al. The effect of STAT3 inhibition on status epilepticus and subsequent spontaneous seizures in the pilocarpine model of acquired epilepsy. Neurobiol Dis 2014; 62: 73-85.
[http://dx.doi.org/10.1016/j.nbd.2013.09.003] [PMID: 24051278]
[129]
Alonso-Nanclares L, DeFelipe J. Alterations of the microvascular network in the sclerotic hippocampus of patients with temporal lobe epilepsy. Epilepsy Behav 2014; 38: 48-52.
[http://dx.doi.org/10.1016/j.yebeh.2013.12.009] [PMID: 24406303]
[130]
Sun BL, Wang LH, Yang T, et al. Lymphatic drainage system of the brain: A novel target for intervention of neurological diseases. Prog Neurobiol 2018; 163-164: 118-43.
[http://dx.doi.org/10.1016/j.pneurobio.2017.08.007] [PMID: 28903061]
[131]
Selkoe DJ. Alzheimer’s disease results from the cerebral accumulation and cytotoxicity of amyloid β-protein. J Alzheimers Dis 2001; 3(1): 75-80.
[http://dx.doi.org/10.3233/JAD-2001-3111] [PMID: 12214075]
[132]
Shim JW, Madsen JR. VEGF Signaling in neurological disorders. Int J Mol Sci 2018; 19(1)E275
[http://dx.doi.org/10.3390/ijms19010275] [PMID: 29342116]
[133]
Subirós N, Del Barco DG, Coro-Antich RM. Erythropoietin: still on the neuroprotection road. Ther Adv Neurol Disorder 2012; 5(3): 161-73.
[http://dx.doi.org/10.1177/1756285611434926] [PMID: 22590480]
[134]
Juul SE, Yachnis AT, Rojiani AM, Christensen RD. Immunohistochemical localization of erythropoietin and its receptor in the developing human brain. Pediatr Dev Pathol 1999; 2(2): 148-58.
[http://dx.doi.org/10.1007/s100249900103] [PMID: 9949221]
[135]
Sirén AL, Knerlich F, Poser W, Gleiter CH, Brück W, Ehrenreich H. Erythropoietin and erythropoietin receptor in human ischemic/hypoxic brain. Acta Neuropathol 2001; 101(3): 271-6.
[http://dx.doi.org/10.1007/s004010000297] [PMID: 11307627]
[136]
Assaraf MI, Diaz Z, Liberman A, et al. Brain erythropoietin receptor expression in Alzheimer disease and mild cognitive impairment. J Neuropathol Exp Neurol 2007; 66(5): 389-98.
[http://dx.doi.org/10.1097/nen.0b013e3180517b28] [PMID: 17483696]
[137]
Chakraborty A, Chatterjee M, Twaalfhoven H, et al. Vascular Endothelial Growth Factor remains unchanged in cerebrospinal fluid of patients with Alzheimer’s disease and vascular dementia. Alzheimers Res Ther 2018; 10(1): 58.
[http://dx.doi.org/10.1186/s13195-018-0385-8] [PMID: 29933741]
[138]
During MJ, Cao L. VEGF, a mediator of the effect of experience on hippocampal neurogenesis. Curr Alzheimer Res 2006; 3(1): 29-33.
[http://dx.doi.org/10.2174/156720506775697133] [PMID: 16472200]
[139]
Sopova K, Gatsiou K, Stellos K, Laske C. Dysregulation of neurotrophic and haematopoietic growth factors in Alzheimer’s disease: from pathophysiology to novel treatment strategies. Curr Alzheimer Res 2014; 11(1): 27-39.
[http://dx.doi.org/10.2174/1567205010666131120100743] [PMID: 24251394]
[140]
Castillo C, Fernández-Mendívil C, Buendia I, et al. Neuroprotective effects of EpoL against oxidative stress induced by soluble oligomers of Aβ peptide. Redox Biol 2019; 24: 101187
[http://dx.doi.org/10.1016/j.redox.2019.101187] [PMID: 30965198]
[141]
Ning B, Zhang A, Song H, et al. Recombinant human erythropoietin prevents motor neuron apoptosis in a rat model of cervical sub-acute spinal cord compression. Neurosci Lett 2011; 490(1): 57-62.
[http://dx.doi.org/10.1016/j.neulet.2010.12.025] [PMID: 21167907]
[142]
Zhu L, Wang HD, Yu XG, et al. Erythropoietin prevents zinc accumulation and neuronal death after traumatic brain injury in rat hippocampus: in vitro and in vivo studies. Brain Res 2009; 1289: 96-105.
[http://dx.doi.org/10.1016/j.brainres.2009.07.015] [PMID: 19615349]
[143]
Castillo C, Zaror S, Gonzalez M, et al. Neuroprotective effect of a new variant of Epo nonhematopoietic against oxidative stress. Redox Biol 2018; 14: 285-94.
[http://dx.doi.org/10.1016/j.redox.2017.09.010] [PMID: 28987867]
[144]
Chong ZZ, Li F, Maiese K. Erythropoietin requires NF-kappaB and its nuclear translocation to prevent early and late apoptotic neuronal injury during β-amyloid toxicity. Curr Neurovasc Res 2005; 2(5): 387-99.
[http://dx.doi.org/10.2174/156720205774962683] [PMID: 16375720]
[145]
Sepulveda FJ, Parodi J, Peoples RW, Opazo C, Aguayo LG. Synaptotoxicity of Alzheimer β amyloid can be explained by its membrane perforating property. PLoS One 2010; 5(7)e11820
[http://dx.doi.org/10.1371/journal.pone.0011820] [PMID: 20676404]
[146]
Sáez-Orellana F, Godoy PA, Bastidas CY, et al. ATP leakage induces P2XR activation and contributes to acute synaptic excitotoxicity induced by soluble oligomers of β-amyloid peptide in hippocampal neurons. Neuropharmacology 2016; 100: 116-23.
[http://dx.doi.org/10.1016/j.neuropharm.2015.04.005] [PMID: 25896766]
[147]
Maurice T, Lockhart BP, Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res 1996; 706(2): 181-93.
[http://dx.doi.org/10.1016/0006-8993(95)01032-7] [PMID: 8822355]
[148]
Salkovic-Petrisic M, Knezovic A, Hoyer S, Riederer P. What have we learned from the streptozotocin-induced animal model of sporadic Alzheimer’s disease, about the therapeutic strategies in Alzheimer’s research. J Neural Transm (Vienna) 2013; 120(1): 233-52.
[http://dx.doi.org/10.1007/s00702-012-0877-9] [PMID: 22886150]
[149]
Arabpoor Z, Hamidi G, Rashidi B, et al. Erythropoietin improves neuronal proliferation in dentate gyrus of hippocampal formation in an animal model of Alzheimer’s disease. Adv Biomed Res 2012; 1: 50.
[http://dx.doi.org/10.4103/2277-9175.100157] [PMID: 23326781]
[150]
Rodríguez Cruz Y, Strehaiano M, Rodríguez Obaya T, García Rodríguez JC, Maurice T. An intranasal formulation of erythropoietin (Neuro-EPO) prevents memory deficits and amyloid toxicity in the appswe transgenic mouse model of Alzheimer’s disease. J Alzheimers Dis 2017; 55(1): 231-48.
[http://dx.doi.org/10.3233/JAD-160500] [PMID: 27662300]
[151]
Maurice T, Mustafa MH, Desrumaux C, et al. Intranasal formulation of erythropoietin (EPO) showed potent protective activity against amyloid toxicity in the Aβ(2)(5)(-)(3)(5) non-transgenic mouse model of Alzheimer’s disease. J Psychopharmacol 2013; 27: 1044-57.
[http://dx.doi.org/10.1177/0269881113494939] [PMID: 23813967]
[152]
Sun ZK, Yang HQ, Pan J, et al. Protective effects of erythropoietin on tau phosphorylation induced by β-amyloid. J Neurosci Res 2008; 86(13): 3018-27.
[http://dx.doi.org/10.1002/jnr.21745] [PMID: 18512763]
[153]
Ehrenreich H, Aust C, Krampe H, et al. Erythropoietin: novel approaches to neuroprotection in human brain disease. Metab Brain Dis 2004; 19(3-4): 195-206.
[http://dx.doi.org/10.1023/B:MEBR.0000043969.96895.3c] [PMID: 15554415]
[154]
Almaguer-Melian W, Mercerón-Martínez D, Delgado-Ocaña S, Pavón-Fuentes N, Ledón N, Bergado JA. EPO induces changes in synaptic transmission and plasticity in the dentate gyrus of rats. Synapse 2016; 70(6): 240-52.
[http://dx.doi.org/10.1002/syn.21895] [PMID: 26860222]
[155]
Cevik B, Solmaz V, Yigitturk G, Cavusoğlu T, Peker G, Erbas O. Neuroprotective effects of erythropoietin on Alzheimer’s dementia model in rats. Adv Clin Exp Med 2017; 26(1): 23-9.
[http://dx.doi.org/10.17219/acem/61044] [PMID: 28397428]
[156]
Mattson MP. Pathways towards and away from Alzheimer’s disease. Nature 2004; 430(7000): 631-9.
[http://dx.doi.org/10.1038/nature02621] [PMID: 15295589]
[157]
Schipper HM. Astrocytes, brain aging, and neurodegeneration. Neurobiol Aging 1996; 17(3): 467-80.
[http://dx.doi.org/10.1016/0197-4580(96)00014-0] [PMID: 8725909]
[158]
Chong ZZ, Li F, Maiese K. Activating Akt and the brain’s resources to drive cellular survival and prevent inflammatory injury. Histol Histopathol 2005; 20(1): 299-315.
[PMID: 15578447]
[159]
Maiese K. Inflammatory glial cells of the nervous system: assistants or assassins? Curr Neurovasc Res 2005; 2(3): 187-8.
[http://dx.doi.org/10.2174/1567202054368380] [PMID: 16189907]
[160]
Hsiao K, Chapman P, Nilsen S, et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996; 274(5284): 99-102.
[http://dx.doi.org/10.1126/science.274.5284.99] [PMID: 8810256]
[161]
Biron KE, Dickstein DL, Gopaul R, Jefferies WA. Amyloid triggers extensive cerebral angiogenesis causing blood brain barrier permeability and hypervascularity in Alzheimer’s disease. PLoS One 2011; 6(8)e23789
[http://dx.doi.org/10.1371/journal.pone.0023789] [PMID: 21909359]
[162]
Biron KE, Dickstein DL, Gopaul R, Fenninger F, Jefferies WA. Cessation of neoangiogenesis in Alzheimer’s disease follows amyloid-β immunization. Sci Rep 2013; 3: 1354.
[http://dx.doi.org/10.1038/srep01354] [PMID: 23446889]
[163]
Armato U, Chakravarthy B, Pacchiana R, Whitfield JF. Alzheimer’s disease: an update of the roles of receptors, astrocytes and primary cilia (review). Int J Mol Med 2013; 31(1): 3-10.
[http://dx.doi.org/10.3892/ijmm.2012.1162] [PMID: 23124509]
[164]
Sharma HS, Castellani RJ, Smith MA, Sharma A. The blood-brain barrier in Alzheimer’s disease: novel therapeutic targets and nanodrug delivery. Int Rev Neurobiol 2012; 102: 47-90.
[http://dx.doi.org/10.1016/B978-0-12-386986-9.00003-X] [PMID: 22748826]
[165]
Jantaratnotai N, Ryu JK, Schwab C, McGeer PL, McLarnon JG. Comparison of vascular perturbations in an aβ-injected animal model and in AD brain. Int J Alzheimers Dis 2011; 2011918280
[http://dx.doi.org/10.4061/2011/918280] [PMID: 21969915]
[166]
Dal Prà I, Whitfileld JF, Pacchiana R, et al. The amyloid-β42 proxy, amyloid-β(25-35), induces normal human cerebral astrocytes to produce amyloid-β42. J Alzheimers Dis 2011; 24(2): 335-47.
[http://dx.doi.org/10.3233/JAD-2011-101626] [PMID: 21258151]
[167]
Storkebaum E, Lambrechts D, Dewerchin M, et al. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 2005; 8(1): 85-92.
[http://dx.doi.org/10.1038/nn1360] [PMID: 15568021]
[168]
Krum JM, Mani N, Rosenstein JM. Angiogenic and astroglial responses to vascular endothelial growth factor administration in adult rat brain. Neuroscience 2002; 110(4): 589-604.
[http://dx.doi.org/10.1016/S0306-4522(01)00615-7] [PMID: 11934468]
[169]
Rosenstein JM, Mani N, Khaibullina A, Krum JM. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J Neurosci 2003; 23(35): 11036-44.
[http://dx.doi.org/10.1523/JNEUROSCI.23-35-11036.2003] [PMID: 14657160]
[170]
Rosenstein JM, Krum JM, Ruhrberg C. VEGF in the nervous system. Organogenesis 2010; 6(2): 107-14.
[http://dx.doi.org/10.4161/org.6.2.11687] [PMID: 20885857]
[171]
Oosthuyse B, Moons L, Storkebaum E, et al. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet 2001; 28(2): 131-8.
[http://dx.doi.org/10.1038/88842] [PMID: 11381259]
[172]
Sanchez A, Tripathy D, Luo J, Yin X, Martinez J, Grammas P. Neurovascular unit and the effects of dosage in VEGF toxicity: role for oxidative stress and thrombin. J Alzheimers Dis 2013; 34(1): 281-91.
[http://dx.doi.org/10.3233/JAD-121636] [PMID: 23202441]
[173]
Vazquez-Mellado MJ, Monjaras-Embriz V, Rocha-Zavaleta L. Erythropoietin, stem cell factor, and cancer cell migration. Vitam Horm 2017; 105: 273-96.
[http://dx.doi.org/10.1016/bs.vh.2017.02.008] [PMID: 28629522]
[174]
Siveen KS, Prabhu K, Krishnankutty R, et al. Vascular endothelial growth factor (vegf) signaling in tumour vascularization: potential and challenges. Curr Vasc Pharmacol 2017; 15(4): 339-51.
[http://dx.doi.org/10.2174/1570161115666170105124038] [PMID: 28056756]
[175]
Szenajch JM, Synowiec AE. [Erythropoietin and drug resistance in breast and ovarian cancers]. Ginekol Pol 2016; 87(4): 300-4.
[http://dx.doi.org/10.17772/gp/57817] [PMID: 27321103]
[176]
Puszko AK, Sosnowski P, Pułka-Ziach K, et al. Urea moiety as amide bond mimetic in peptide-like inhibitors of VEGF-A165/NRP-1 complex. Bioorg Med Chem Lett 2019; 29(17): 2493-7.
[http://dx.doi.org/10.1016/j.bmcl.2019.07.016] [PMID: 31326342]
[177]
Wang S, Park JK, Duh EJ. Novel targets against retinal angiogenesis in diabetic retinopathy. Curr Diab Rep 2012; 12(4): 355-63.
[http://dx.doi.org/10.1007/s11892-012-0289-0] [PMID: 22638940]
[178]
Funakoshi-Tago M, Moriwaki T, Ueda F, Tamura H, Kasahara T, Tago K. Phosphorylated CIS suppresses the Epo or JAK2 V617F mutant-triggered cell proliferation through binding to EpoR. Cell Signal 2017; 31: 41-57.
[http://dx.doi.org/10.1016/j.cellsig.2016.12.008] [PMID: 28038963]
[179]
Kim BR, Yoon K, Byun HJ, Seo SH, Lee SH, Rho SB. The anti-tumor activator sMEK1 and paclitaxel additively decrease expression of HIF-1α and VEGF via mTORC1-S6K/4E-BP-dependent signaling pathways. Oncotarget 2014; 5(15): 6540-51.
[http://dx.doi.org/10.18632/oncotarget.2119] [PMID: 25153728]
[180]
Liu J, Schenker M, Ghiasvand S, Berdichevsky Y. Kinase inhibitors with antiepileptic properties identified with a novel in vitro screening platform. Int J Mol Sci 2019; 20(10)E2502
[http://dx.doi.org/10.3390/ijms20102502] [PMID: 31117204]
[181]
Gągało I, Rusiecka I, Kocić I. Tyrosine kinase inhibitor as a new therapy for ischemic stroke and other neurologic diseases: is there any hope for a better outcome? Curr Neuropharmacol 2015; 13(6): 836-44.
[http://dx.doi.org/10.2174/1570159X13666150518235504] [PMID: 26630962]
[182]
Yuan R, Wang B, Lu W, Maeda Y, Dowling P. A distinct region in erythropoietin that induces immuno/inflammatory modulation and tissue protection. Neurotherapeutics 2015; 12(4): 850-61.
[http://dx.doi.org/10.1007/s13311-015-0379-1] [PMID: 26271954]
[183]
Ercan I, Tufekci KU, Karaca E, Genc S, Genc K. Peptide derivatives of erythropoietin in the treatment of neuroinflammation and neurodegeneration. Adv Protein Chem Struct Biol 2018; 112: 309-57.
[http://dx.doi.org/10.1016/bs.apcsb.2018.01.007] [PMID: 29680240]
[184]
Zhang X, Feng S, Liu J, et al. Novel small peptides derived from VEGF125-136: potential drugs for radioactive diagnosis and therapy in A549 tumor-bearing nude mice. Sci Rep 2017; 7(1): 4278.
[http://dx.doi.org/10.1038/s41598-017-04513-y] [PMID: 28655913]
[185]
Abdollahpour N, Soheili V, Saberi MR, Chamani J. Investigation of the interaction between human serum albumin and two drugs as binary and ternary systems. Eur J Drug Metab Pharmacokinet 2016; 41(6): 705-21.
[http://dx.doi.org/10.1007/s13318-015-0297-y] [PMID: 26328807]
[186]
Zolfagharzadeh M, Pirouzi M, Asoodeh A, Saberi MR, Chamani J. A comparison investigation of DNP-binding effects to HSA and HTF by spectroscopic and molecular modeling techniques. J Biomol Struct Dyn 2014; 32(12): 1936-52.
[http://dx.doi.org/10.1080/07391102.2013.843062] [PMID: 24125112]
[187]
Danesh N, Navaee Sedighi Z, Beigoli S, Sharifi-Rad A, Saberi MR, Chamani J. Determining the binding site and binding affinity of estradiol to human serum albumin and holo-transferrin: fluorescence spectroscopic, isothermal titration calorimetry and molecular modeling approaches. J Biomol Struct Dyn 2018; 36(7): 1747-63.
[http://dx.doi.org/10.1080/07391102.2017.1333460] [PMID: 28573922]
[188]
Juul SE, Pet GC. Erythropoietin and neonatal neuroprotection. Clin Perinatol 2015; 42(3): 469-81.
[http://dx.doi.org/10.1016/j.clp.2015.04.004] [PMID: 26250911]

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