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CNS & Neurological Disorders - Drug Targets

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ISSN (Online): 1996-3181

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The Role of Ca2+ Permeable AMPA Receptors in Neurodegeneration, Neurotoxicity, and Neuroinflammation

Author(s): José Afonso Corrêa da Silva and Nadja Schröder*

Volume 22, Issue 5, 2023

Published on: 18 July, 2022

Page: [624 - 633] Pages: 10

DOI: 10.2174/1871527321666220510141735

open access plus

Abstract

It is believed that degenerative conditions that give rise to neurological diseases may share an abnormal influx of Ca2+, mainly through glutamate receptors. Current research on the glutamatergic system indicates that the N-methyl-D-aspartate receptor (NMDAR) is not the only receptor permeable to Ca2+. Under certain conditions, α -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPARs) are able to rapidly and potently mediate a neurotoxic Ca2+ influx. AMPARs are encoded by four genes designated GluR 1-4. The presence of the edited GluA2 subunit makes the heteromeric AMPAR impermeable to Ca2+ (CI-AMPAR's). On the other hand, the lack of GluA2 or disruptions in its post-translational editing result in Ca2+-permeable AMPA receptors (CP-AMPARs). In addition to triggering behavioral changes, the increase in CP-AMPARs is documented in several neurodegenerative, neuroinflammatory and neurotoxic conditions, demonstrating that AMPAR changes may play a role in the emergence and evolution of pathological conditions of the central nervous system (CNS). Seeking to better understand how CP-AMPARs influence CNS neuropathology, and how it may serve as a pharmacological target for future molecules, in this article, we summarize and discuss studies investigating changes in the composition of AMPARs and their cellular and molecular effects, to improve the understanding of the therapeutic potential of the CP-AMPAR in neurodegenerative, neurotoxic and neuroinflammatory diseases.

Keywords: AMPA receptors, calcium-permeable AMPA receptors (CP-AMPAR), neurodegenerative diseases, calcium, pharmacological target, neurotoxicity.

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[1]
Werner CT, Murray CH, Reimers JM, et al. Trafficking of calcium-permeable and calcium-impermeable AMPA receptors in nucleus accumbens medium spiny neurons co-cultured with prefrontal cortex neurons. Neuropharmacology 2017; 116: 224-32.
[http://dx.doi.org/10.1016/j.neuropharm.2016.12.014] [PMID: 27993521]
[2]
Collingridge GL, Olsen RW, Peters J, Spedding M. A nomenclature for ligand-gated ion channels. Neuropharmacology 2009; 56(1): 2-5.
[http://dx.doi.org/10.1016/j.neuropharm.2008.06.063] [PMID: 18655795]
[3]
Twomey EC, Yelshanskaya MV, Grassucci RA, Frank J, Sobolevsky AI. Channel opening and gating mechanism in AMPA-subtype glutamate receptors. Nature 2017; 549(7670): 60-5.
[http://dx.doi.org/10.1038/nature23479] [PMID: 28737760]
[4]
Wright A, Vissel B. The essential role of AMPA receptor GluR2 subunit RNA editing in the normal and diseased brain. Front Mol Neurosci 2012; 5: 34.
[http://dx.doi.org/10.3389/fnmol.2012.00034] [PMID: 22514516]
[5]
Liu SJ, Zukin RS. Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 2007; 30(3): 126-34.
[http://dx.doi.org/10.1016/j.tins.2007.01.006] [PMID: 17275103]
[6]
Donevan SD, Rogawski MA. Intracellular polyamines mediate inward rectification of Ca(2+)-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Proc Natl Acad Sci USA 1995; 92(20): 9298-302.
[http://dx.doi.org/10.1073/pnas.92.20.9298] [PMID: 7568121]
[7]
Liu SQ, Cull-Candy SG. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 2000; 405(6785): 454-8.
[http://dx.doi.org/10.1038/35013064] [PMID: 10839540]
[8]
Traynelis SF, Wollmuth LP, McBain CJ, et al. Glutamate receptor ion channels: Structure, regulation, and function. Pharmacol Rev 2010; 62(3): 405-96.
[http://dx.doi.org/10.1124/pr.109.002451] [PMID: 20716669]
[9]
Rogawski MA, Löscher W. The neurobiology of antiepileptic drugs. Nat Rev Neurosci 2004; 5(7): 553-64.
[http://dx.doi.org/10.1038/nrn1430] [PMID: 15208697]
[10]
Takeda A, Tamano H, Tempaku M, et al. Extracellular Zn2+ is essential for Amyloid β1-42-induced cognitive decline in the normal brain and its rescue. J Neurosci 2017; 37(30): 7253-62.
[http://dx.doi.org/10.1523/JNEUROSCI.0954-17.2017] [PMID: 28652412]
[11]
Tamano H, Nishio R, Morioka H, Takeda A. Extracellular Zn2+ influx into nigral dopaminergic neurons plays a key role for pathogenesis of 6-hydroxydopamine-induced Parkinson’s disease in rats. Mol Neurobiol 2019; 56(1): 435-43.
[http://dx.doi.org/10.1007/s12035-018-1075-z] [PMID: 29705946]
[12]
Selvaraj BT, Livesey MR, Zhao C, et al. C9ORF72 repeat expansion causes vulnerability of motor neurons to Ca2+-permeable AMPA receptor-mediated excitotoxicity. Nat Commun 2018; 9(1): 347.
[http://dx.doi.org/10.1038/s41467-017-02729-0] [PMID: 29367641]
[13]
Lewitus GM, Pribiag H, Duseja R, St-Hilaire M, Stellwagen D. An adaptive role of TNFα in the regulation of striatal synapses. J Neurosci 2014; 34(18): 6146-55.
[http://dx.doi.org/10.1523/JNEUROSCI.3481-13.2014] [PMID: 24790185]
[14]
Sobolevsky AI. Structure and gating of tetrameric glutamate receptors. J Physiol 2015; 593(1): 29-38.
[http://dx.doi.org/10.1113/jphysiol.2013.264911] [PMID: 25556785]
[15]
Renner MC, Albers EH, Gutierrez-Castellanos N, et al. Synaptic plasticity through activation of GluA3-containing AMPA-receptors. eLife 2017; 6: e25462.
[http://dx.doi.org/10.7554/eLife.25462] [PMID: 28762944]
[16]
Kita K, Albergaria C, Machado AS, Carey MR, Müller M, Delvendahl I. GluA4 facilitates cerebellar expansion coding and enables associative memory formation. eLife 2021; 10: e65152.
[http://dx.doi.org/10.7554/eLife.65152] [PMID: 34219651]
[17]
Wenthold RJ, Petralia RS, Blahos J II, Niedzielski AS. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 1996; 16(6): 1982-9.
[http://dx.doi.org/10.1523/JNEUROSCI.16-06-01982.1996] [PMID: 8604042]
[18]
Zhu JJ, Esteban JA, Hayashi Y, Malinow R. Postnatal synaptic potentiation: Delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat Neurosci 2000; 3(11): 1098-106.
[http://dx.doi.org/10.1038/80614] [PMID: 11036266]
[19]
Incontro S, Ciruela F, Ziff E, Hofmann F, Sánchez-Prieto J, Torres M. The type II cGMP dependent protein kinase regulates GluA1 levels at the plasma membrane of developing cerebellar granule cells. Biochim Biophys Acta 2013; 1833(8): 1820-31.
[http://dx.doi.org/10.1016/j.bbamcr.2013.03.021] [PMID: 23545413]
[20]
Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, Choquet D. Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 2009; 63(1): 92-105.
[http://dx.doi.org/10.1016/j.neuron.2009.05.025] [PMID: 19607795]
[21]
Clem RL, Anggono V, Huganir RL. PICK1 regulates incorporation of calcium-permeable AMPA receptors during cortical synaptic strengthening. J Neurosci 2010; 30(18): 6360-6.
[http://dx.doi.org/10.1523/JNEUROSCI.6276-09.2010] [PMID: 20445062]
[22]
Santerre JL, Gigante ED, Landin JD, Werner DF. Molecular and behavioral characterization of adolescent protein kinase C following high dose ethanol exposure. Psychopharmacology (Berl) 2014; 231(8): 1809-20.
[http://dx.doi.org/10.1007/s00213-013-3267-6] [PMID: 24051603]
[23]
Taoro-Gonzalez L, Arenas YM, Cabrera-Pastor A, Felipo V. Extracellular cGMP reverses altered membrane expression of AMPA receptors in hippocampus of hyperammonemic rats: Underlying mechanisms. Mol Neurobiol 2019; 56(6): 4428-39.
[http://dx.doi.org/10.1007/s12035-018-1387-z] [PMID: 30328550]
[24]
Ishida K, Kotake Y, Sanoh S, Ohta S. Lead-Induced ERK activation is mediated by GluR2 non-containing AMPA receptor in cortical neurons. Biol Pharm Bull 2017; 40(3): 303-9.
[http://dx.doi.org/10.1248/bpb.b16-00784] [PMID: 28250271]
[25]
Oakes SA, Opferman JT, Pozzan T, Korsmeyer SJ, Scorrano L. Regulation of endoplasmic reticulum Ca2+ dynamics by proapoptotic BCL-2 family members. Biochem Pharmacol 2003; 66(8): 1335-40.
[http://dx.doi.org/10.1016/S0006-2952(03)00482-9] [PMID: 14555206]
[26]
Kwak S, Weiss JH. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr Opin Neurobiol 2006; 16(3): 281-7.
[http://dx.doi.org/10.1016/j.conb.2006.05.004] [PMID: 16698262]
[27]
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]
[28]
Litersky JM, Johnson GV, Jakes R, Goedert M, Lee M, Seubert P. Tau protein is phosphorylated by cyclic AMP-dependent protein kinase and calcium/calmodulin-dependent protein kinase II within its microtubule-binding domains at Ser-262 and Ser-356. Biochem J 1996; 316(Pt 2): 655-60.
[http://dx.doi.org/10.1042/bj3160655] [PMID: 8687413]
[29]
Baumann K, Mandelkow EM, Biernat J, Piwnica-Worms H, Mandelkow E. Abnormal Alzheimer-like phosphorylation of tauprotein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett 1993; 336(3): 417-24.
[http://dx.doi.org/10.1016/0014-5793(93)80849-P] [PMID: 8282104]
[30]
Hundehege P, Epping L, Meuth LE. Calcium homeostasis in multiple sclerosis. Neurology International Open 2017; 1: E127-35.
[http://dx.doi.org/10.1055/s-0043-109031]
[31]
Whitcomb DJ, Hogg EL, Regan P, et al. Intracellular oligomeric amyloid-beta rapidly regulates GluA1 subunit of AMPA receptor in the hippocampus. Sci Rep 2015; 5: 10934.
[http://dx.doi.org/10.1038/srep10934] [PMID: 26055072]
[32]
Kobylecki C, Crossman AR, Ravenscroft P. Alternative splicing of AMPA receptor subunits in the 6-OHDA-lesioned rat model of Parkinson’s disease and L-DOPA-induced dyskinesia. Exp Neurol 2013; 247: 476-84.
[http://dx.doi.org/10.1016/j.expneurol.2013.01.019] [PMID: 23360800]
[33]
Hoey SE, Buonocore F, Cox CJ, Hammond VJ, Perkinton MS, Williams RJ. AMPA receptor activation promotes non-amyloidogenic amyloid precursor protein processing and suppresses neuronal amyloid-β production. PLoS One 2013; 8(10): e78155.
[http://dx.doi.org/10.1371/journal.pone.0078155] [PMID: 24205136]
[34]
Van Den Bosch L, Vandenberghe W, Klaassen H, Van Houtte E, Robberecht W. Ca(2+)-permeable AMPA receptors and selective vulnerability of motor neurons. J Neurol Sci 2000; 180(1-2): 29-34.
[http://dx.doi.org/10.1016/S0022-510X(00)00414-7] [PMID: 11090861]
[35]
Ankolekar SM, Sikdar SK. Early postnatal exposure to lithium in vitro induces changes in AMPAR mEPSCs and vesicular recycling at hippocampal glutamatergic synapses. J Biosci 2015; 40(2): 339-54.
[http://dx.doi.org/10.1007/s12038-015-9527-3] [PMID: 25963261]
[36]
Chieia MA, Oliveira AS, Silva HC, Gabbai AA. Amyotrophic lateral sclerosis: Considerations on diagnostic criteria. Arq Neuropsiquiatr 2010; 68(6): 837-42.
[http://dx.doi.org/10.1590/S0004-282X2010000600002] [PMID: 21243238]
[37]
Bogaert E, Goris A, Van Damme P, et al. Polymorphisms in the GluR2 gene are not associated with amyotrophic lateral sclerosis. Neurobiol Aging 2012; 33(2): 418-20.
[http://dx.doi.org/10.1016/j.neurobiolaging.2010.03.007] [PMID: 20409611]
[38]
Stellwagen D, Malenka RC. Synaptic scaling mediated by glial TNF-α. Nature 2006; 440: 1054-9.
[39]
Yin HZ, Sensi SL, Ogoshi F, Weiss JH. Blockade of Ca2+-permeable AMPA/kainate channels decreases oxygen-glucose deprivation-induced Zn2+ accumulation and neuronal loss in hippocampal pyramidal neurons. J Neurosci 2002; 22(4): 1273-9.
[http://dx.doi.org/10.1523/JNEUROSCI.22-04-01273.2002] [PMID: 11850455]
[40]
Appel SH, Smith RG, Alexianu M, et al. Neurodegenerative disease: Autoimmunity involving calcium channels. Ann N Y Acad Sci 1994; 747: 183-94.
[http://dx.doi.org/10.1111/j.1749-6632.1994.tb44409.x] [PMID: 7847670]
[41]
Carriedo SG, Sensi SL, Yin HZ, Weiss JH. AMPA exposures induce mitochondrial Ca(2+) overload and ROS generation in spinal motor neurons in vitro. J Neurosci 2000; 20(1): 240-50.
[http://dx.doi.org/10.1523/JNEUROSCI.20-01-00240.2000] [PMID: 10627601]
[42]
Van Damme P, Braeken D, Callewaert G, Robberecht W, Van Den Bosch L. GluR2 deficiency accelerates motor neuron degeneration in a mouse model of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 2005; 64(7): 605-12.
[http://dx.doi.org/10.1097/01.jnen.0000171647.09589.07] [PMID: 16042312]
[43]
Yamashita T, Kwak S. Cell death cascade and molecular therapy in ADAR2-deficient motor neurons of ALS. Neurosci Res 2019; 144: 4-13.
[http://dx.doi.org/10.1016/j.neures.2018.06.004] [PMID: 29944911]
[44]
Gregory JM, Livesey MR, McDade K, et al. Dysregulation of AMPA receptor subunit expression in sporadic ALS post-mortem brain. J Pathol 2020; 250(1): 67-78.
[http://dx.doi.org/10.1002/path.5351] [PMID: 31579943]
[45]
Akamatsu M, Yamashita T, Hirose N, Teramoto S, Kwak S. The AMPA receptor antagonist perampanel robustly rescues amyotrophic lateral sclerosis (ALS) pathology in sporadic ALS model mice. Sci Rep 2016; 6: 28649.
[http://dx.doi.org/10.1038/srep28649] [PMID: 27350567]
[46]
Van Damme P, Leyssen M, Callewaert G, Robberecht W, Van Den Bosch L. The AMPA receptor antagonist NBQX prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis. Neurosci Lett 2003; 343(2): 81-4.
[http://dx.doi.org/10.1016/S0304-3940(03)00314-8] [PMID: 12759169]
[47]
Yin HZ, Hsu CI, Yu S, Rao SD, Sorkin LS, Weiss JH. TNF-α triggers rapid membrane insertion of Ca(2+) permeable AMPA receptors into adult motor neurons and enhances their susceptibility to slow excitotoxic injury. Exp Neurol 2012; 238(2): 93-102.
[http://dx.doi.org/10.1016/j.expneurol.2012.08.004] [PMID: 22921461]
[48]
Nihei K, Kowall NW. Involvement of NPY-immunoreactive neurons in the cerebral cortex of amyotrophic lateral sclerosis patients. Neurosci Lett 1993; 159(1-2): 67-70.
[http://dx.doi.org/10.1016/0304-3940(93)90800-Z] [PMID: 8264981]
[49]
Young KC, McGehee DS, Brorson JR. Glutamate receptor expression and chronic glutamate toxicity in rat motor cortex. Neurobiol Dis 2007; 26(1): 78-85.
[http://dx.doi.org/10.1016/j.nbd.2006.12.002] [PMID: 17240155]
[50]
Denes L, Szilágyi G, Gál A, Nagy Z. Talampanel a non-competitive AMPA-antagonist attenuates caspase-3 dependent apoptosis in mouse brain after transient focal cerebral ischemia. Brain Res Bull 2006; 70(3): 260-2.
[http://dx.doi.org/10.1016/j.brainresbull.2006.02.024] [PMID: 16861112]
[51]
Patai R, Paizs M, Tortarolo M, et al. Presymptomatically applied AMPA receptor antagonist prevents calcium increase in vulnerable type of motor axon terminals of mice modeling amyotrophic lateral sclerosis. Biochim Biophys Acta Mol Basis Dis 2017; 1863(7): 1739-48.
[http://dx.doi.org/10.1016/j.bbadis.2017.05.016] [PMID: 28528135]
[52]
Jonsson PA, Graffmo KS, Brännström T, Nilsson P, Andersen PM, Marklund SL. Motor neuron disease in mice expressing the wild type-like D90A mutant superoxide dismutase-1. J Neuropathol Exp Neurol 2006; 65(12): 1126-36.
[http://dx.doi.org/10.1097/01.jnen.0000248545.36046.3c] [PMID: 17146286]
[53]
Goyal NA, Mozaffar T. Experimental trials in amyotrophic lateral sclerosis: A review of recently completed, ongoing and planned trials using existing and novel drugs. Expert Opin Investig Drugs 2014; 23(11): 1541-51.
[http://dx.doi.org/10.1517/13543784.2014.933807] [PMID: 24965719]
[54]
Mhyre TR, Boyd JT, Hamill RW, Maguire-Zeiss KA. Parkinson’s disease. Subcell Biochem 2012; 65: 389-455.
[http://dx.doi.org/10.1007/978-94-007-5416-4_16] [PMID: 23225012]
[55]
Marras C, Beck JC, Bower JH, et al. Prevalence of Parkinson’s disease across North America. NPJ Parkinsons Dis 2018; 4: 21.
[http://dx.doi.org/10.1038/s41531-018-0058-0] [PMID: 30003140]
[56]
Van der Perren A, Gelders G, Fenyi A, et al. The structural differences between patient-derived α -synuclein strains dictate characteristics of Parkinson’s disease, multiple system atrophy and dementia with Lewy bodies. Acta Neuropathol 2020; 139(6): 977-1000.
[http://dx.doi.org/10.1007/s00401-020-02157-3] [PMID: 32356200]
[57]
Morin N, Di Paolo T. Pharmacological treatments inhibiting levodopa-induced dyskinesias in MPTP-lesioned monkeys: Brain glutamate biochemical correlates. Front Neurol 2014; 5: 144.
[http://dx.doi.org/10.3389/fneur.2014.00144] [PMID: 25140165]
[58]
Gass JT, Trantham-Davidson H, Kassab AS, Glen WB Jr, Olive MF, Chandler LJ. Enhancement of extinction learning attenuates ethanol-seeking behavior and alters plasticity in the prefrontal cortex. J Neurosci 2014; 34(22): 7562-74.
[http://dx.doi.org/10.1523/JNEUROSCI.5616-12.2014] [PMID: 24872560]
[59]
Kobylecki C, Cenci MA, Crossman AR, Ravenscroft P. Calcium-permeable AMPA receptors are involved in the induction and expression of l-DOPA-induced dyskinesia in Parkinson’s disease. J Neurochem 2010; 114(2): 499-511.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06776.x] [PMID: 20456008]
[60]
Lindenbach D, Conti MM, Ostock CY, et al. The Role of Primary Motor Cortex (M1) Glutamate and GABA signaling in l-DOPA-induced dyskinesia in parkinsonian rats. J Neurosci 2016; 36(38): 9873-87.
[http://dx.doi.org/10.1523/JNEUROSCI.1318-16.2016] [PMID: 27656025]
[61]
Nakajima S, Saeki N, Tamano H, et al. Age-related vulnerability to nigral dopaminergic degeneration in rats via Zn2+-permeable GluR2-lacking AMPA receptor activation. Neurotoxicology 2021; 83: 69-76.
[http://dx.doi.org/10.1016/j.neuro.2020.12.014] [PMID: 33400970]
[62]
Diógenes MJ, Dias RB, Rombo DM, et al. Extracellular alpha-synuclein oligomers modulate synaptic transmission and impair LTP via NMDA-receptor activation. J Neurosci 2012; 32(34): 11750-62.
[http://dx.doi.org/10.1523/JNEUROSCI.0234-12.2012] [PMID: 22915117]
[63]
Musiek ES, Holtzman DM. Three dimensions of the amyloid hypothesis: Time, space and ‘wingmen’. Nat Neurosci 2015; 18(6): 800-6.
[http://dx.doi.org/10.1038/nn.4018] [PMID: 26007213]
[64]
Bukke VN, Archana M, Villani R, et al. The dual role of glutamatergic neurotransmission in Alzheimer’s disease: From pathophysiology to pharmacotherapy. Int J Mol Sci 2020; 21(20): 7452.
[http://dx.doi.org/10.3390/ijms21207452] [PMID: 33050345]
[65]
Cascella R, Evangelisti E, Bigi A, et al. Soluble oligomers require a ganglioside to trigger neuronal calcium overload. J Alzheimers Dis 2017; 60(3): 923-38.
[http://dx.doi.org/10.3233/JAD-170340] [PMID: 28922156]
[66]
Megill A, Tran T, Eldred K, et al. Defective Age-Dependent Metaplasticity in a Mouse Model of Alzheimer’s Disease. J Neurosci 2015; 35(32): 11346-57.
[http://dx.doi.org/10.1523/JNEUROSCI.5289-14.2015] [PMID: 26269641]
[67]
Whitehead G, Regan P, Whitcomb DJ, Cho K. Ca2+-permeable AMPA receptor: A new perspective on amyloid-beta mediated pathophysiology of Alzheimer’s disease. Neuropharmacology 2017; 112(Pt A): 221-7.
[http://dx.doi.org/10.1016/j.neuropharm.2016.08.022] [PMID: 27561971]
[68]
Gilbert J, Shu S, Yang X, Lu Y, Zhu LQ, Man HY. β-Amyloid triggers aberrant over-scaling of homeostatic synaptic plasticity. Acta Neuropathol Commun 2016; 4(1): 131.
[http://dx.doi.org/10.1186/s40478-016-0398-0] [PMID: 27955702]
[69]
Gascon E, Lynch K, Ruan H, et al. Alterations in microRNA-124 and AMPA receptors contribute to social behavioral deficits in frontotemporal dementia. Nat Med 2014; 20(12): 1444-51.
[http://dx.doi.org/10.1038/nm.3717] [PMID: 25401692]
[70]
Chang EH, Savage MJ, Flood DG, et al. AMPA receptor downscaling at the onset of Alzheimer’s disease pathology in double knockin mice. Proc Natl Acad Sci USA 2006; 103(9): 3410-5.
[http://dx.doi.org/10.1073/pnas.0507313103] [PMID: 16492745]
[71]
Ishida K, Kotake Y, Miyara M, et al. Involvement of decreased glutamate receptor subunit GluR2 expression in lead-induced neuronal cell death. J Toxicol Sci 2013; 38(3): 513-21.
[http://dx.doi.org/10.2131/jts.38.513] [PMID: 23719929]
[72]
Simons TJ, Pocock G. Lead enters bovine adrenal medullary cells through calcium channels. J Neurochem 1987; 48(2): 383-9.
[http://dx.doi.org/10.1111/j.1471-4159.1987.tb04105.x] [PMID: 2432178]
[73]
Albensi BC, Mattson MP. Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity. Synapse 2000; 35(2): 151-9.
[http://dx.doi.org/10.1002/(SICI)1098-2396(200002)35:2<151::AID-SYN8>3.0.CO;2-P] [PMID: 10611641]
[74]
Marin I, Kipnis J. Learning and memory ... and the immune system. Learn Mem 2013; 20(10): 601-6.
[http://dx.doi.org/10.1101/lm.028357.112] [PMID: 24051097]
[75]
Pribiag H, Stellwagen D. Neuroimmune regulation of homeostatic synaptic plasticity. Neuropharmacology 2014; 78: 13-22.
[http://dx.doi.org/10.1016/j.neuropharm.2013.06.008] [PMID: 23774138]
[76]
Koszegi Z, Fiuza M, Hanley JG. Endocytosis and lysosomal degradation of GluA2/3 AMPARs in response to oxygen/glucose deprivation in hippocampal but not cortical neurons. Sci Rep 2017; 7(1): 12318.
[http://dx.doi.org/10.1038/s41598-017-12534-w] [PMID: 28951554]
[77]
Arundine M, Tymianski M. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 2004; 61(6): 657-68.
[http://dx.doi.org/10.1007/s00018-003-3319-x] [PMID: 15052409]
[78]
Liu B, Liao M, Mielke JG, et al. Ischemic insults direct glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites. J Neurosci 2006; 26(20): 5309-19.
[http://dx.doi.org/10.1523/JNEUROSCI.0567-06.2006] [PMID: 16707783]
[79]
Achzet LM, Davison CJ, Shea M, Sturgeon I, Jackson DA. Oxidative stress underlies the ischemia/reperfusion-induced internalization and degradation of AMPA receptors. Int J Mol Sci 2021; 22(2): 717.
[http://dx.doi.org/10.3390/ijms22020717] [PMID: 33450848]
[80]
Chen S, Wang Y, Wang X, He M, Zhang L, Dong Z. PKA-dependent membrane surface recruitment of CI-AMPARs is crucial for BCP-mediated protection against post-acute ischemic stroke cognitive impairment. Front Neurol 2020; 11: 566067.
[http://dx.doi.org/10.3389/fneur.2020.566067] [PMID: 33391143]

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