Neuronal Excitability in Epileptogenic Zones Regulated by the Wnt/ Β-Catenin Pathway

Author(s): Carmen Rubio, Elisa Taddei, Jorge Acosta, Verónica Custodio, Carlos Paz*

Journal Name: CNS & Neurological Disorders - Drug Targets
(Formerly Current Drug Targets - CNS & Neurological Disorders)

Volume 19 , Issue 1 , 2020

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Graphical Abstract:


Abstract:

Epilepsy is a neurological disorder that involves abnormal and recurrent neuronal discharges, producing epileptic seizures. Recently, it has been proposed that the Wnt signaling pathway is essential for the central nervous system development and function because it modulates important processes such as hippocampal neurogenesis, synaptic clefting, and mitochondrial regulation. Wnt/β- catenin signaling regulates changes induced by epileptic seizures, including neuronal death. Several genetic studies associate Wnt/β-catenin signaling with neuronal excitability and epileptic activity. Mutations and chromosomal defects underlying syndromic or inherited epileptic seizures have been identified. However, genetic factors underlying the susceptibility of an individual to develop epileptic seizures have not been fully studied yet. In this review, we describe the genes involved in neuronal excitability in epileptogenic zones dependent on the Wnt/β-catenin pathway.

Keywords: Wnt/β-catenin, neuronal excitability, epileptogenesis, genetic signaling, hippocampal formation, neurotransmitter secretion.

[1]
World Health Organization [Internet]. 2019. Epilepsy Fact Sheet; 2019 June 20 [cited 2019 Nov 21] Available from: https://www.who.int/en/news-room/fact-sheets/detail/epilepsy
[2]
Beghi, E.; Giussani, G.; Nichols, E. et al.Global, regional, and national burden of epilepsy, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol., 2019, 18(4), 357-375.
[http://dx.doi.org/10.1016/S1474-4422(18)30454-X] [PMID: 30773428]
[3]
Téllez-Zenteno, J.F.; Hernández-Ronquillo, L. A review of the epidemiology of temporal lobe epilepsy. Epilepsy Res. Treat., 2012, 2012630853
[http://dx.doi.org/10.1155/2012/630853] [PMID: 22957234]
[4]
Mergenthaler, P.; Lindauer, U.; Dienel, G.A.; Meisel, A. Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci., 2013, 36(10), 587-597.
[http://dx.doi.org/10.1016/j.tins.2013.07.001] [PMID: 23968694]
[5]
Logan, C.Y.; Nusse, R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol., 2004, 20(1), 781-810.
[http://dx.doi.org/10.1146/annurev.cellbio.20.010403.113126] [PMID: 15473860]
[6]
Nishimura, T.; Schwarzer, C.; Gasser, E.; Kato, N.; Vezzani, A.; Sperk, G. Altered expression of GABA(A) and GABA(B) receptor subunit mRNAs in the hippocampus after kindling and electrically induced status epilepticus. Neuroscience, 2005, 134(2), 691-704.
[http://dx.doi.org/10.1016/j.neuroscience.2005.04.013] [PMID: 15951123]
[7]
Li, H.; Kraus, A.; Wu, J.; Huguenard, J.R.; Fisher, R.S. Selective changes in thalamic and cortical GABAA receptor subunits in a model of acquired absence epilepsy in the rat. Neuropharmacology, 2006, 51(1), 121-128.
[http://dx.doi.org/10.1016/j.neuropharm.2006.03.003] [PMID: 16678865]
[8]
Pitkänen, A.; Sutula, T.P. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol., 2002, 1(3), 173-181.
[http://dx.doi.org/10.1016/S1474-4422(02)00073-X] [PMID: 12849486]
[9]
Nusse, R.; Varmus, H.E. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell, 1982, 31(1), 99-109.
[http://dx.doi.org/10.1016/0092-8674(82)90409-3] [PMID: 6297757]
[10]
Prud’homme, B.; Lartillot, N.; Balavoine, G.; Adoutte, A.; Vervoort, M. Phylogenetic analysis of the Wnt gene family. Insights from lophotrochozoan members. Curr. Biol., 2002, 12(16), 1395-1400.
[http://dx.doi.org/10.1016/S0960-9822(02)01068-0] [PMID: 12194820]
[11]
Hill, M. Embryology [Internet] Developmental Signals - Wnt. [cited 2019 Nov 21] Available from: https://embryology.med.unsw. edu.au/embryology/index.php/Developmental_Signals_-_Wnt
[12]
Wiese, K.E.; Nusse, R.; van Amerongen, R. Wnt signalling: conquering complexity. Development, 2018, 145(12)dev165902
[http://dx.doi.org/10.1242/dev.165902] [PMID: 29945986]
[13]
Budnik, V.; Salinas, P.C. Wnt signaling during synaptic development and plasticity. Curr. Opin. Neurobiol., 2011, 21(1), 151-9.
[http://dx.doi.org/10.1016/j.conb.2010.12.002] [PMID: 21239163]
[14]
Inestrosa, N.C.; Varela-Nallar, L. Wnt signaling in the nervous system and in Alzheimer’s disease. J. Mol. Cell Biol., 2014, 6(1), 64-74.
[http://dx.doi.org/10.1093/jmcb/mjt051] [PMID: 24549157]
[15]
Arrázola, M.S.; Silva-Alvarez, C.; Inestrosa, N.C. How the Wnt signaling pathway protects from neurodegeneration: the mitochondrial scenario. Front. Cell. Neurosci., 2015, 9, 166.
[http://dx.doi.org/10.3389/fncel.2015.00166] [PMID: 25999816]
[16]
Niehrs, C. The complex world of WNT receptor signalling. Nat. Rev. Mol. Cell Biol., 2012, 13(12), 767-779.
[http://dx.doi.org/10.1038/nrm3470] [PMID: 23151663]
[17]
Chien, A.J.; Conrad, W.H.; Moon, R.T. A Wnt survival guide: from flies to human disease. J. Invest. Dermatol., 2009, 129(7), 1614-1627.
[http://dx.doi.org/10.1038/jid.2008.445] [PMID: 19177135]
[18]
Angers, S.; Moon, R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol., 2009, 10(7), 468-477.
[http://dx.doi.org/10.1038/nrm2717] [PMID: 19536106]
[19]
Willert, K.; Jones, K.A. Wnt signaling: is the party in the nucleus? Genes Dev., 2006, 20(11), 1394-1404.
[http://dx.doi.org/10.1101/gad.1424006] [PMID: 16751178]
[20]
Yost, C.; Torres, M.; Miller, J.R.; Huang, E.; Kimelman, D.; Moon, R.T. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev., 1996, 10(12), 1443-1454.
[http://dx.doi.org/10.1101/gad.10.12.1443] [PMID: 8666229]
[21]
Aberle, H.; Bauer, A.; Stappert, J.; Kispert, A.; Kemler, R. β-catenin is a target for the ubiquitin-proteasome pathway. EMBO J., 1997, 16(13), 3797-3804.
[http://dx.doi.org/10.1093/emboj/16.13.3797] [PMID: 9233789]
[22]
Hart, M.J.; de los Santos, R.; Albert, I.N.; Rubinfeld, B.; Polakis, P. Downregulation of β-catenin by human Axin and its association with the APC tumor suppressor, β-catenin and GSK3 β. Curr. Biol., 1998, 8(10), 573-581.
[http://dx.doi.org/10.1016/S0960-9822(98)70226-X] [PMID: 9601641]
[23]
Deng, X.; Xie, Y.; Chen, Y. Effect of neuroinflammation on ABC Transporters: possible contribution to refractory epilepsy. CNS Neurol. Disord. Drug Targets, 2018, 17(10), 728-735.
[http://dx.doi.org/10.2174/1871527317666180828121820] [PMID: 30152292]
[24]
Lazarowski, A.; Czornyj, L.; Lubienieki, F.; Girardi, E.; Vazquez, S.; D’Giano, C. ABC transporters during epilepsy and mechanisms underlying multidrug resistance in refractory epilepsy. Epilepsia, 2007, 48(Suppl. 5), 140-149.
[http://dx.doi.org/10.1111/j.1528-1167.2007.01302.x] [PMID: 17910594]
[25]
Liu, L.; Wan, W.; Xia, S.; Kalionis, B.; Li, Y. Dysfunctional Wnt/β-catenin signaling contributes to blood-brain barrier breakdown in Alzheimer’s disease. Neurochem. Int., 2014, 75, 19-25.
[http://dx.doi.org/10.1016/j.neuint.2014.05.004] [PMID: 24859746]
[26]
Li, X.T.; Ma, W.; Wang, X.B. Notoginsenoside R1 promotes the growth of neonatal rat cortical neurons via the Wnt/β-catenin signaling pathway. CNS Neurol. Disord. Drug Targets, 2018, 17(7), 547-556.
[http://dx.doi.org/10.2174/1871527317666180711093538] [PMID: 29992896]
[27]
Yan, S.; Li, Z.; Li, H.; Arancio, O.; Zhang, W. Notoginsenoside R1 increases neuronal excitability and ameliorates synaptic and memory dysfunction following amyloid elevation. Sci. Rep., 2014, 4(1), 6352.
[http://dx.doi.org/10.1038/srep06352] [PMID: 25213453]
[28]
Zang, K.; Zhang, Y.; Hu, J.; Wang, Y. The large conductance calcium- and voltage-activated potassium channel (BK) and epilepsy. CNS Neurol. Disord. Drug Targets, 2018, 17(4), 248-254.
[http://dx.doi.org/10.2174/1871527317666180404104055] [PMID: 29623857]
[29]
Zhu, Y.; Zhang, S.; Feng, Y.; Xiao, Q.; Cheng, J.; Tao, J. The Yin and Yang of BK channels in epilepsy. CNS Neurol. Disord. Drug Targets, 2018, 17(4), 272-279.
[http://dx.doi.org/10.2174/1871527317666180213142403] [PMID: 29437015]
[30]
Velázquez-Marrero, C.; Burgos, A.; García, J.O. Alcohol Regulates BK surface expression via Wnt/β-catenin signaling. J. Neurosci., 2016, 36(41), 10625-10639.
[http://dx.doi.org/10.1523/JNEUROSCI.0491-16.2016] [PMID: 27733613]
[31]
Clevers, H.; Nusse, R. Wnt/β-catenin signaling and disease. Cell, 2012, 149(6), 1192-1205.
[http://dx.doi.org/10.1016/j.cell.2012.05.012] [PMID: 22682243]
[32]
MacDonald, B.T.; Tamai, K.; He, X. Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell, 2009, 17(1), 9-26.
[http://dx.doi.org/10.1016/j.devcel.2009.06.016] [PMID: 19619488]
[33]
Routledge, D.; Scholpp, S. Mechanisms of intercellular Wnt transport. Development, 2019, 146(10)dev176073
[http://dx.doi.org/10.1242/dev.176073] [PMID: 31092504]
[34]
Xiao, Q.; Chen, Z.; Jin, X.; Mao, R.; Chen, Z. The many postures of noncanonical Wnt signaling in development and diseases. Biomed. Pharmacother., 2017, 93, 359-369.
[http://dx.doi.org/10.1016/j.biopha.2017.06.061] [PMID: 28651237]
[35]
Inoki, K.; Zhu, T.; Guan, K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell, 2003, 115(5), 577-590.
[http://dx.doi.org/10.1016/S0092-8674(03)00929-2] [PMID: 14651849]
[36]
Inoki, K.; Ouyang, H.; Zhu, T. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell, 2006, 126(5), 955-968.
[http://dx.doi.org/10.1016/j.cell.2006.06.055] [PMID: 16959574]
[37]
Inoki, K.; Li, Y.; Zhu, T.; Wu, J.; Guan, K.L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol., 2002, 4(9), 648-657.
[http://dx.doi.org/10.1038/ncb839] [PMID: 12172553]
[38]
Yamada, K.A. Calorie restriction and glucose regulation. Epilepsia, 2008, 49(Suppl. 8), 94-96.
[http://dx.doi.org/10.1111/j.1528-1167.2008.01847.x] [PMID: 19049600]
[39]
Oliva, C.A.; Montecinos-Oliva, C.; Inestrosa, N.C. Wnt signaling in the central nervous system: new insights in health and disease. Prog. Mol. Biol. Transl. Sci., 2018, 153, 81-130.
[http://dx.doi.org/10.1016/bs.pmbts.2017.11.018] [PMID: 29389523]
[40]
Yi, H.; Hu, J.; Qian, J.; Hackam, A.S. Expression of brain-derived neurotrophic factor is regulated by the Wnt signaling pathway. Neuroreport, 2012, 23(3), 189-194.
[http://dx.doi.org/10.1097/WNR.0b013e32834fab06] [PMID: 22198686]
[41]
Li, X.T.; Liang, Z.; Wang, T.T. Brain-derived neurotrophic factor promotes growth of neurons and neural stem cells possibly by triggering the phosphoinositide 3-Kinase/ AKT/Glycogen synthase Kinase-3β/β-catenin Pathway. CNS Neurol. Disord. Drug Targets, 2017, 16(7), 828-836.
[http://dx.doi.org/10.2174/1871527316666170518170422] [PMID: 28524001]
[42]
Russo, E.; Andreozzi, F.; Iuliano, R. Early molecular and behavioral response to lipopolysaccharide in the WAG/Rij rat model of absence epilepsy and depressive-like behavior, involves interplay between AMPK, AKT/mTOR pathways and neuroinflammatory cytokine release. Brain Behav. Immun., 2014, 42, 157-168.
[http://dx.doi.org/10.1016/j.bbi.2014.06.016] [PMID: 24998197]
[43]
Russo, E.; Citraro, R.; Donato, G. mTOR inhibition modulates epileptogenesis, seizures and depressive behavior in a genetic rat model of absence epilepsy. Neuropharmacology, 2013, 69, 25-36.
[http://dx.doi.org/10.1016/j.neuropharm.2012.09.019] [PMID: 23092918]
[44]
Danzer, S.C. Depression, stress, epilepsy and adult neurogenesis. Exp. Neurol., 2012, 233(1), 22-32.
[http://dx.doi.org/10.1016/j.expneurol.2011.05.023] [PMID: 21684275]
[45]
Scharfman, H.E.; Goodman, J.H.; Sollas, A.L. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J. Neurosci., 2000, 20(16), 6144-58.
[http://dx.doi.org/10.1523/JNEUROSCI.20-16-06144.2000] [PMID: 10934264]
[46]
Farías, G.G.; Vallés, A.S.; Colombres, M. Wnt-7a induces presynaptic colocalization of alpha 7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J. Neurosci., 2007, 27(20), 5313-5325.
[http://dx.doi.org/10.1523/JNEUROSCI.3934-06.2007] [PMID: 17507554]
[47]
Cerpa, W.; Godoy, J.A.; Alfaro, I. Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J. Biol. Chem., 2008, 283(9), 5918-27.
[http://dx.doi.org/10.1074/jbc.M705943200] [PMID: 18096705]
[48]
Davis, E.K.; Zou, Y.; Ghosh, A. Wnts acting through canonical and noncanonical signaling pathways exert opposite effects on hippocampal synapse formation. Neural Dev., 2008, 3(1), 32.
[http://dx.doi.org/10.1186/1749-8104-3-32] [PMID: 18986540]
[49]
Avila, M.E.; Sepúlveda, F.J.; Burgos, C.F. Canonical Wnt3a modulates intracellular calcium and enhances excitatory neurotransmission in hippocampal neurons. J. Biol. Chem., 2010, 285(24), 18939-47.
[http://dx.doi.org/10.1074/jbc.M110.103028] [PMID: 20404321]
[50]
Cisternas, P.; Salazar, P.; Silva-Álvarez, C.; Barros, L.F.; Inestrosa, N.C. Activation of Wnt signaling in cortical neurons enhances glucose utilization through glycolysis. J. Biol. Chem., 2016, 291(50), 25950-25964.
[http://dx.doi.org/10.1074/jbc.M116.735373] [PMID: 27703002]
[51]
Rubio, C.; Rosiles-Abonce, A.; Trejo-Solis, C. Increase signaling of Wnt/β-catenin pathway and presence of apoptosis in cerebellum of kindled rats. CNS Neurol. Disord. Drug Targets, 2017, 16(7), 772-80.
[http://dx.doi.org/10.2174/1871527316666170117114513] [PMID: 28124605]
[52]
Pérez-Palma, E.; Andrade, V.; Caracci, M.O. Early transcriptional changes induced by Wnt/β-catenin signaling in hippocampal neurons. Neural Plast., 2016, 20164672841
[http://dx.doi.org/10.1155/2016/4672841] [PMID: 28116168]
[53]
Yntema, H.G.; van den Helm, B.; Kissing, J. A novel ribosomal S6-kinase (RSK4; RPS6KA6) is commonly deleted in patients with complex X-linked mental retardation. Genomics, 1999, 62(3), 332-343.
[http://dx.doi.org/10.1006/geno.1999.6004] [PMID: 10644430]
[54]
Carriere, A.; Ray, H.; Blenis, J.; Roux, P.P. The RSK factors of activating the Ras/MAPK signaling cascade. Front. Biosci., 2008, 13(13), 4258-4275.
[http://dx.doi.org/10.2741/3003] [PMID: 18508509]
[55]
Zeniou, M.; Ding, T.; Trivier, E.; Hanauer, A. Expression analysis of RSK gene family members: the RSK2 gene, mutated in Coffin-Lowry syndrome, is prominently expressed in brain structures essential for cognitive function and learning. Hum. Mol. Genet., 2002, 11(23), 2929-2940.
[http://dx.doi.org/10.1093/hmg/11.23.2929] [PMID: 12393804]
[56]
Zeniou-Meyer, M.; Liu, Y.; Béglé, A. The Coffin-Lowry syndrome-associated protein RSK2 is implicated in calcium-regulated exocytosis through the regulation of PLD1. Proc. Natl. Acad. Sci. USA, 2008, 105(24), 8434-9.
[http://dx.doi.org/10.1073/pnas.0710676105] [PMID: 18550821]
[57]
Yamada, T.; Yoshiyama, Y.; Kawaguchi, N. Expression of activating transcription factor-2 (ATF-2), one of the cyclic AMP response element (CRE) binding proteins, in Alzheimer disease and non-neurological brain tissues. Brain Res., 1997, 749(2), 329-334.
[http://dx.doi.org/10.1016/S0006-8993(96)01356-X] [PMID: 9138733]
[58]
Haze, K.; Yoshida, H.; Yanagi, H.; Yura, T.; Mori, K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell, 1999, 10(11), 3787-99.
[http://dx.doi.org/10.1091/mbc.10.11.3787] [PMID: 10564271]
[59]
Kezuka, D.; Tkarada-Iemata, M.; Hattori, T. Deletion of Atf6α enhances kainate-induced neuronal death in mice. Neurochem. Int., 2016, 92, 67-74.
[http://dx.doi.org/10.1016/j.neuint.2015.12.009] [PMID: 26724566]
[60]
Batten, S.R.; Matveeva, E.A.; Whiteheart, S.W.; Vanaman, T.C.; Gerhardt, G.A.; Slevin, J.T. Linking kindling to increased glutamate release in the dentate gyrus of the hippocampus through the STXBP5/tomosyn-1 gene. Brain Behav., 2017, 7(9)e00795
[http://dx.doi.org/10.1002/brb3.795] [PMID: 28948088]
[61]
Toonen, R.F.; Wierda, K.; Sons, M.S. Munc18-1 expression levels control synapse recovery by regulating readily releasable pool size. Proc. Natl. Acad. Sci. USA, 2006, 103(48), 18332-18337.
[http://dx.doi.org/10.1073/pnas.0608507103] [PMID: 17110441]
[62]
Deprez, L.; Weckhuysen, S.; Holmgren, P. Clinical spectrum of early-onset epileptic encephalopathies associated with STXBP1 mutations. Neurology, 2010, 75(13), 1159-1165.
[http://dx.doi.org/10.1212/WNL.0b013e3181f4d7bf] [PMID: 20876469]
[63]
O’Brien, S.; Ng-Cordell, E.; Astle, D.E.; Scerif, G.; Baker, K. STXBP1-associated neurodevelopmental disorder: a comparative study of behavioural characteristics. J. Neurodev. Disord., 2019, 11(1), 17.
[http://dx.doi.org/10.1186/s11689-019-9278-9] [PMID: 31387522]
[64]
Shao, L.R.; Habela, C.W.; Stafstrom, C.E. Pediatric epilepsy mechanisms: expanding the paradigm of excitation/inhibition imbalance. Children (Basel), 2019, 6(2), 23.
[http://dx.doi.org/10.3390/children6020023] [PMID: 30764523]
[65]
Mohrmann, R.; Dhara, M.; Bruns, D. Complexins: small but capable. Cell. Mol. Life Sci., 2015, 72(22), 4221-4235.
[http://dx.doi.org/10.1007/s00018-015-1998-8] [PMID: 26245303]
[66]
Zhou, Q.; Zhou, P.; Wang, A.L. The primed SNARE-complexin-synaptotagmin complex for neuronal exocytosis. Nature, 2017, 548(7668), 420-425.
[http://dx.doi.org/10.1038/nature23484] [PMID: 28813412]
[67]
Itakura, M.; Misawa, H.; Sekiguchi, M.; Takahashi, S.; Takahashi, M. Transfection analysis of functional roles of complexin I and II in the exocytosis of two different types of secretory vesicles. Biochem. Biophys. Res. Commun., 1999, 265(3), 691-696.
[http://dx.doi.org/10.1006/bbrc.1999.1756] [PMID: 10600482]
[68]
van de Bospoort, R.; Farina, M.; Schmitz, S.K. Munc13 controls the location and efficiency of dense-core vesicle release in neurons. J. Cell Biol., 2012, 199(6), 883-891.
[http://dx.doi.org/10.1083/jcb.201208024] [PMID: 23229896]
[69]
Sakamoto, H.; Ariyoshi, T.; Kimpara, N. Synaptic weight set by Munc13-1 supramolecular assemblies. Nat. Neurosci., 2018, 21(1), 41-49.
[http://dx.doi.org/10.1038/s41593-017-0041-9] [PMID: 29230050]
[70]
Zhu, X.; Han, X.; Blendy, J.A.; Porter, B.E. Decreased CREB levels suppress epilepsy. Neurobiol. Dis., 2012, 45(1), 253-263.
[http://dx.doi.org/10.1016/j.nbd.2011.08.009] [PMID: 21867753]
[71]
Zhu, X.; Dubey, D.; Bermudez, C.; Porter, B.E. Suppressing cAMP response element-binding protein transcription shortens the duration of status epilepticus and decreases the number of spontaneous seizures in the pilocarpine model of epilepsy. Epilepsia, 2015, 56(12), 1870-8.
[http://dx.doi.org/10.1111/epi.13211] [PMID: 26419901]
[72]
Steiger, J.L.; Bandyopadhyay, S.; Farb, D.H.; Russek, S.J. cAMP response element-binding protein, activating transcription factor-4, and upstream stimulatory factor differentially control hippocampal GABABR1a and GABABR1b subunit gene expression through alternative promoters. J. Neurosci., 2004, 24(27), 6115-26.
[http://dx.doi.org/10.1523/JNEUROSCI.1200-04.2004] [PMID: 15240803]
[73]
Gasnier, B. The loading of neurotransmitters into synaptic vesicles. Biochimie, 2000, 82(4), 327-337.
[http://dx.doi.org/10.1016/S0300-9084(00)00221-2] [PMID: 10865121]
[74]
Wang, Y.; Kakizaki, T.; Sakagami, H. Fluorescent labeling of both GABAergic and glycinergic neurons in vesicular GABA transporter (VGAT)-venus transgenic mouse. Neuroscience, 2009, 164(3), 1031-43.
[http://dx.doi.org/10.1016/j.neuroscience.2009.09.010] [PMID: 19766173]
[75]
DeRosa, B.A.; Belle, K.C.; Thomas, B.J. hVGAT-mCherry: A novel molecular tool for analysis of GABAergic neurons derived from human pluripotent stem cells. Mol. Cell. Neurosci., 2015, 68, 244-57.
[http://dx.doi.org/10.1016/j.mcn.2015.08.007] [PMID: 26284979]
[76]
Sagné, C.; El Mestikawy, S.; Isambert, M.F. Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett., 1997, 417(2), 177-83.
[http://dx.doi.org/10.1016/S0014-5793(97)01279-9] [PMID: 9395291]
[77]
Dias-Gunasekara, S.; Gubbens, J.; van Lith, M. Tissue-specific expression and dimerization of the endoplasmic reticulum oxidoreductase Ero1β. J. Biol. Chem., 2005, 280(38), 33066-75.
[http://dx.doi.org/10.1074/jbc.M505023200] [PMID: 16012172]
[78]
Kaeser, P.S.; Südhof, T.C. RIM function in short- and long-term synaptic plasticity. Biochem. Soc. Trans., 2005, 33(Pt 6), 1345-9.
[http://dx.doi.org/10.1042/BST0331345] [PMID: 16246115]
[79]
Schoch, S.; Mittelstaedt, T.; Kaeser, P.S. Redundant functions of RIM1α and RIM2α in Ca(2+)-triggered neurotransmitter release. EMBO J., 2006, 25(24), 5852-63.
[http://dx.doi.org/10.1038/sj.emboj.7601425] [PMID: 17124501]
[80]
Jiang, X.; Litkowski, P.E.; Taylor, A.A.; Lin, Y.; Snider, B.J.; Moulder, K.L. A role for the ubiquitin-proteasome system in activity-dependent presynaptic silencing. J. Neurosci., 2010, 30(5), 1798-809.
[http://dx.doi.org/10.1523/JNEUROSCI.4965-09.2010] [PMID: 20130189]
[81]
Pitsch, J.; Opitz, T.; Borm, V. The presynaptic active zone protein RIM1α controls epileptogenesis following status epilepticus. J. Neurosci., 2012, 32(36), 12384-95.
[http://dx.doi.org/10.1523/JNEUROSCI.0223-12.2012] [PMID: 22956829]
[82]
Walker, A.; Russmann, V.; Deeg, C.A. Proteomic profiling of epileptogenesis in a rat model: Focus on inflammation. Brain Behav. Immun., 2016, 53, 138-58.
[http://dx.doi.org/10.1016/j.bbi.2015.12.007] [PMID: 26685804]
[83]
Giffard, R.G.; Xu, L.; Zhao, H. Chaperones, protein aggregation, and brain protection from hypoxic/ischemic injury. J. Exp. Biol., 2004, 207(Pt 18), 3213-20.
[http://dx.doi.org/10.1242/jeb.01034] [PMID: 15299042]
[84]
Wishart, T.M.; Rooney, T.M.; Lamont, D.J. Combining comparative proteomics and molecular genetics uncovers regulators of synaptic and axonal stability and degeneration in vivo. PLoS Genet., 2012, 8(8)e1002936
[http://dx.doi.org/10.1371/journal.pgen.1002936] [PMID: 22952455]
[85]
Varoqueaux, F.; Sigler, A.; Rhee, J.S. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. Sci. USA, 2002, 99(13), 9037-42.
[http://dx.doi.org/10.1073/pnas.122623799] [PMID: 12070347]
[86]
Meng, F.; You, Y.; Liu, Z.; Liu, J.; Ding, H.; Xu, R. Neuronal calcium signaling pathways are associated with the development of epilepsy. Mol. Med. Rep., 2015, 11(1), 196-202.
[http://dx.doi.org/10.3892/mmr.2014.2756] [PMID: 25339366]
[87]
Baghel, R.; Grover, S.; Kaur, H. Synergistic association of STX1A and VAMP2 with cryptogenic epilepsy in North Indian population. Brain Behav., 2016, 6(7)e00490
[http://dx.doi.org/10.1002/brb3.490] [PMID: 27458546]
[88]
Schoch, S.; Deák, F.; Königstorfer, A. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science, 2001, 294(5544), 1117-1122.
[http://dx.doi.org/10.1126/science.1064335] [PMID: 11691998]
[89]
Deák, F.; Schoch, S.; Liu, X.; Südhof, T.C.; Kavalali, E.T. Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat. Cell Biol., 2004, 6(11), 1102-08.
[http://dx.doi.org/10.1038/ncb1185] [PMID: 15475946]
[90]
Li, D.; Hérault, K.; Zylbersztejn, K. Astrocyte VAMP3 vesicles undergo Ca2+ -independent cycling and modulate glutamate transporter trafficking. J. Physiol., 2015, 593(13), 2807-32.
[http://dx.doi.org/10.1113/JP270362] [PMID: 25864578]
[91]
Aizenman, E.; Lipton, S.A.; Loring, R.H. Selective modulation of NMDA responses by reduction and oxidation. Neuron, 1989, 2(3), 1257-63.
[http://dx.doi.org/10.1016/0896-6273(89)90310-3] [PMID: 2696504]
[92]
Sucher, N.J.; Lipton, S.A. Redox modulatory site of the NMDA receptor-channel complex: regulation by oxidized glutathione. J. Neurosci. Res., 1991, 30(3), 582-591.
[http://dx.doi.org/10.1002/jnr.490300316] [PMID: 1666131]
[93]
Turano, C.; Coppari, S.; Altieri, F.; Ferraro, A. Proteins of the PDI family: unpredicted non-ER locations and functions. J. Cell. Physiol., 2002, 193(2), 154-163.
[http://dx.doi.org/10.1002/jcp.10172] [PMID: 12384992]
[94]
Kim, J.Y.; Ko, A.R.; Hyun, H.W.; Min, S.J.; Kim, J.E. PDI regulates seizure activity via NMDA receptor redox in rats. Sci. Rep., 2017, 7(1), 42491.
[http://dx.doi.org/10.1038/srep42491] [PMID: 28198441]
[95]
Lu, Z.; Xu, S. ERK1/2 MAP kinases in cell survival and apoptosis. IUBMB Life, 2006, 58(11), 621-631.
[http://dx.doi.org/10.1080/15216540600957438] [PMID: 17085381]
[96]
Ferrer-Orta, C.; Pérez-Sánchez, M.D.; Coronado-Parra, T. Structural characterization of the Rabphilin-3A-SNAP25 interaction. Proc. Natl. Acad. Sci. USA, 2017, 114(27), E5343-51.
[http://dx.doi.org/10.1073/pnas.1702542114] [PMID: 28634303]
[97]
Liu, G.; Guo, H.; Guo, C.; Zhao, S.; Gong, D.; Zhao, Y. Involvement of IRE1α signaling in the hippocampus in patients with mesial temporal lobe epilepsy. Brain Res. Bull., 2011, 84(1), 94-102.
[http://dx.doi.org/10.1016/j.brainresbull.2010.10.004] [PMID: 20965234]
[98]
Rangel, A.; Madroñal, N.; Gruart, A. Regulation of GABA(A) and glutamate receptor expression, synaptic facilitation and long-term potentiation in the hippocampus of prion mutant mice. PLoS One, 2009, 4(10)e7592
[http://dx.doi.org/10.1371/journal.pone.0007592] [PMID: 19855845]


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