Neuronal Gene Targets of NF-κB and Their Dysregulation in Alzheimer's Disease

Wanda M. Snow1,2, Benedict C. Albensi1,2
1Department of Pharmacology and Therapeutics, University of Manitoba, Winnipeg, MB, Canada
2Division of Neurodegenerative Disorders, St. Boniface Hospital Research, Winnipeg, MB, Canada

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Acquaah-Mensah, 2016, Brain in situ hybridization maps as a source for reverse-engineering transcriptional regulatory networks: Alzheimer's disease insights, Gene, 586, 77, 10.1016/j.gene.2016.03.045

Aguirre-Rueda, 2015, Astrocytes protect neurons from Aβ1-42 peptide-induced neurotoxicity increasing TFAM and PGC-1 and decreasing PPAR-gamma and SIRT-1, Int. J. Med. Sci., 12, 48, 10.7150/ijms.10035

Ahn, 2008, c-Rel, an NF-κB family transcription factor, is required for hippocampal long-term synaptic plasticity and memory formation, Learn. Mem., 15, 539, 10.1101/lm.866408

Aisen, 1994, Inflammatory mechanisms in Alzheimer's disease: implications for therapy, Am. J. Psychiatry, 151, 1105, 10.1176/ajp.151.8.1105

Albensi, 2000, Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity, Synapse, 35, 151, 10.1002/(SICI)1098-2396(200002)35:2151::AID-SYN83.0.CO;2-P

Alberini, 2014, The regulation of transcription in memory consolidation, Cold Spring Harb. Perspect. Biol., 7, a021741, 10.1101/cshperspect.a021741

Amada, 2005, Reduction of NR1 and phosphorylated Ca2+/calmodulin-dependent protein kinase II levels in Alzheimer's disease, Neuroreport, 16, 1809, 10.1097/01.wnr.0000185015.44563.5d

Anantharaman, 2006, β-amyloid mediated nitration of manganese superoxide dismutase: implication for oxidative stress in a APPNLH/NLH X PS-1P264L/P264L double knock-in mouse model of Alzheimer's disease, Am. J. Pathol., 168, 1608, 10.2353/ajpath.2006.051223

Angelucci, 2014, The effect of neuropeptide Y on cell survival and neurotrophin expression in in-vitro models of Alzheimer's disease, Can. J. Physiol. Pharmacol., 92, 621, 10.1139/cjpp-2014-0099

Arunsundar, 2015, 3,4-dihydroxyphenylethanol attenuates spatio-cognitive deficits in an Alzheimer's disease mouse model: modulation of the molecular signals in neuronal survival-apoptotic programs, Neurotox. Res., 27, 143, 10.1007/s12640-014-9492-x

Bales, 1998, The NF-κB/Rel family of proteins mediates Aβ-induced neurotoxicity and glial activation, Brain Res. Mol. Brain Res., 57, 63, 10.1016/S0169-328X(98)00066-7

Beal, 1986, Neuropeptides in neurological disease, Ann. Neurol., 20, 547, 10.1002/ana.410200502

Beckmann, 1997, Egr transcription factors in the nervous system, Neurochem. Int., 31, 477, 10.1016/s0197-0186(96)00136-2

Beg, 1994, Activation of multiple NF-κB/Rel, DNA-binding complexes by tumor necrosis factor, Oncogene, 9, 1487

Behl, 1994, Hydrogen peroxide mediates amyloid β protein toxicity, Cell, 77, 817, 10.1016/0092-8674(94)90131-7

Bekinschtein, 2007, Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus, Neuron, 53, 261, 10.1016/j.neuron.2006.11.025

Bevilaqua, 1999, Experience-dependent increase in cAMP-responsive element binding protein in synaptic and nonsynaptic mitochondria of the rat hippocampus, Eur. J. Neurosci., 11, 3753, 10.1046/j.1460-9568.1999.00830.x

Bliss, 1993, A synaptic model of memory: long-term potentiation in the hippocampus, Nature, 361, 31, 10.1038/361031a0

Bliss, 1973, Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path, J. Physiol., 232, 331, 10.1113/jphysiol.1973.sp010273

Bo, 2014, Exercise-induced neuroprotection of hippocampus in APP/PS1 transgenic mice via upregulation of mitochondrial 8-oxoguanine DNA glycosylase, Oxid. Med. Cell. Longev., 2014, 834502, 10.1155/2014/834502

Boersma, 2011, A requirement for nuclear factor-κB in developmental and plasticity-associated synaptogenesis, J. Neurosci., 31, 5414, 10.1523/JNEUROSCI.2456-10.2011

Borbély, 2013, Neuropeptides in learning and memory, Neuropeptides, 47, 439, 10.1016/j.npep.2013.10.012

Bourne, 2007, Differential regulation of BACE1 promoter activity by nuclear factor-κB in neurons and glia upon exposure to β-amyloid peptides, J. Neurosci. Res., 85, 1194, 10.1002/jnr.21252

Bui, 2001, Activation of nuclear factor κB and Bcl-x survival gene expression by nerve growth factor requires tyrosine phosphorylation of IκBα, J. Cell Biol., 152, 753, 10.1083/jcb.152.4.753

Cabezas-Opazo, 2015, Mitochondrial dysfunction contributes to the pathogenesis of Alzheimer's disease, Oxid. Med. Cell. Longev., 2015, 509654, 10.1155/2015/509654

Cammarota, 1999, Cyclic AMP-responsive element binding protein in brain mitochondria, J. Neurochem., 72, 2272, 10.1046/j.1471-4159.1999.0722272.x

Carayol, 2006, A dominant function of IKK/NF-κB signaling in global lipopolysaccharide-induced gene expression, J. Biol. Chem., 281, 31142, 10.1074/jbc.M603417200

Carter, 1996, Selective activation of NF-κB by nerve growth factor through the neurotrophin receptor p75, Science, 272, 542, 10.1126/science.272.5261.542

Chami, 2012, Nuclear factor-κB regulates βAPP and β- and gamma-secretases differently at physiological and supraphysiological Aβ concentrations, J. Biol. Chem., 287, 24573, 10.1074/jbc.M111.333054

Chen, 2012, Increased NF-κB signaling up-regulates BACE1 expression and its therapeutic potential in Alzheimer's disease, Int. J. Neuropsychopharmacol., 15, 77, 10.1017/S1461145711000149

Chen, 2002, Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity, J. Neurophysiol., 87, 2851, 10.1152/jn.00820.2001

Chen, 2002, Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-κB, EMBO J., 21, 6539, 10.1093/emboj/cdf660

Chen, 2005, NF-κB RelA phosphorylation regulates RelA acetylation, Mol. Cell. Biol., 25, 7966, 10.1128/MCB.25.18.7966-7975.2005

Chishti, 2001, Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695, J. Biol. Chem., 276, 21562, 10.1074/jbc.M100710200

Choi, 2014, A three-dimensional human neural cell culture model of Alzheimer's disease, Nature, 515, 274, 10.1038/nature13800

Chowdhury, 2015, Simultaneous evaluation of substrate-dependent oxygen consumption rates and mitochondrial membrane potential by TMRM and safranin in cortical mitochondria, Biosci. Rep., 36, e00286, 10.1042/BSR20150244

Collart, 1990, Regulation of tumor necrosis factor α transcription in macrophages: involvement of four κB-like motifs and of constitutive and inducible forms of NF-κB, Mol. Cell. Biol., 10, 1498, 10.1128/MCB.10.4.1498

Corrada, 2010, Dementia incidence continues to increase with age in the oldest old: the 90+ study, Ann. Neurol., 67, 114, 10.1002/ana.21915

Cowley, 2008, COX-2, but not COX-1, activity is necessary for the induction of perforant path long-term potentiation and spatial learning in vivo, Eur. J. Neurosci., 27, 2999, 10.1111/j.1460-9568.2008.06251.x

Croce, 2012, Neuropeptide Y protects rat cortical neurons against β-amyloid toxicity and re-establishes synthesis and release of nerve growth factor, ACS Chem. Neurosci., 3, 312, 10.1021/cn200127e

Croce, 2013, NPY modulates miR-30a-5p and BDNF in opposite direction in an in vitro model of Alzheimer disease: a possible role in neuroprotection?, Mol. Cell. Biochem., 376, 189, 10.1007/s11010-013-1567-0

De Felice, 2007, Cyclic AMP enhancers and Aβ oligomerization blockers as potential therapeutic agents in Alzheimer's disease, Curr. Alzheimer Res., 4, 263, 10.2174/156720507781077287

De Leo, 1998, Oxidative stress and overexpression of manganese superoxide dismutase in patients with Alzheimer's disease, Neurosci. Lett., 250, 173, 10.1016/S0304-3940(98)00469-8

de Mendonça, 2016, Role of genes GSTM1, GSTT1, and MnSOD in the development of late-onset Alzheimer disease and their relationship with APOE*4, Neurologia, 31, 535, 10.1016/j.nrl.2014.10.012

Diniz, 2011, Brain-derived neurotrophic factor and Alzheimer's disease: physiopathology and beyond, Neuromol. Med., 13, 217, 10.1007/s12017-011-8154-x

Dumont, 2009, Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer's disease, FASEB J., 23, 2459, 10.1096/fj.09-132928

Engelmann, 2016, Transcriptional control of synaptic plasticity by transcription factor NF-κB, Neural Plast., 2016, 7027949, 10.1155/2016/7027949

Eriksson, 1998, Neurogenesis in the adult human hippocampus, Nat. Med., 4, 1313, 10.1038/3305

Federman, 2013, Nuclear factor κB-dependent histone acetylation is specifically involved in persistent forms of memory, J. Neurosci., 33, 7603, 10.1523/JNEUROSCI.4181-12.2013

Ferrer, 1998, NF-kB immunoreactivity is observed in association with β A4 diffuse plaques in patients with Alzheimer's disease, Neuropathol. Appl. Neurobiol., 24, 271, 10.1046/j.1365-2990.1998.00116.x

Fink, 2003, Selective regulation of neurite extension and synapse formation by the β but not the α isoform of CaMKII, Neuron, 39, 283, 10.1016/S0896-6273(03)00428-8

Fitzjohn, 2006, Promiscuous interactions between AMPA-Rs and MAGUKs, Neuron, 52, 222, 10.1016/j.neuron.2006.10.002

Frankland, 2001, α-CaMKII-dependent plasticity in the cortex is required for permanent memory, Nature, 411, 309, 10.1038/35077089

Furukawa, 1998, The transcription factor NF-κB mediates increases in calcium currents and decreases in NMDA- and AMPA/kainate-induced currents induced by tumor necrosis factor-α in hippocampal neurons, J. Neurochem., 70, 1876, 10.1046/j.1471-4159.1998.70051876.x

Giese, 1998, Autophosphorylation at Thr286 of the α calcium-calmodulin kinase II in LTP and learning, Science, 279, 870, 10.1126/science.279.5352.870

Glabe, 2006, Common mechanisms of amyloid oligomer pathogenesis in degenerative disease, Neurobiol. Aging, 27, 570, 10.1016/j.neurobiolaging.2005.04.017

Gloire, 2006, NF-κB activation by reactive oxygen species: fifteen years later, Biochem. Pharmacol., 72, 1493, 10.1016/j.bcp.2006.04.011

Gómez Ravetti, 2010, Uncovering molecular biomarkers that correlate cognitive decline with the changes of hippocampus' gene expression profiles in Alzheimer's disease, PLoS ONE, 5, e10153, 10.1371/journal.pone.0010153

Goodman, 1996, Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid β-peptide toxicity, J. Neurochem., 66, 869, 10.1046/j.1471-4159.1996.66020869.x

Grilli, 1996a, Interleukin-1β and glutamate activate the NF-κB/Rel binding site from the regulatory region of the amyloid precursor protein gene in primary neuronal cultures, J. Biol. Chem., 271, 15002, 10.1074/jbc.271.25.15002

Grilli, 1996b, Neuroprotection by aspirin and sodium salicylate through blockade of NF-κB activation, Science, 274, 1383, 10.1126/science.274.5291.1383

Grilli, 1995, Identification and characterization of a κB/Rel binding site in the regulatory region of the amyloid precursor protein gene, J. Biol. Chem., 270, 26774, 10.1074/jbc.270.45.26774

Gu, 2009, B-amyloid impairs AMPA receptor trafficking and function by reducing Ca2+/calmodulin-dependent protein kinase II synaptic distribution, J. Biol. Chem., 284, 10639, 10.1074/jbc.M806508200

Guzmán, 2009, Sex-dependent effect of cyclooxygenase-2 inhibition on mouse spatial memory, Behav. Brain Res., 199, 355, 10.1016/j.bbr.2009.01.005

Guzowski, 2001, Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif, J. Neurosci., 21, 5089, 10.1523/JNEUROSCI.21-14-05089.2001

Haack, 2013, NF-κB and CREB are required for angiotensin II type 1 receptor upregulation in neurons, PLoS ONE, 8, e78695, 10.1371/journal.pone.0078695

Hanson, 1992, Neuronal Ca2+/calmodulin-dependent protein kinases, Annu. Rev. Biochem., 61, 559, 10.1146/annurev.bi.61.070192.003015

Hardy, 1992, Alzheimer's disease: the amyloid cascade hypothesis, Science, 256, 184, 10.1126/science.1566067

Hardy, 1991, Amyloid deposition as the central event in the aetiology of Alzheimer's disease, Trends Pharmacol. Sci., 12, 383, 10.1016/0165-6147(91)90609-V

Hayden, 2004, Signaling to NF-κB, Genes Dev., 18, 2195, 10.1101/gad.1228704

Heck, 1999, Insulin-like growth factor-1-mediated neuroprotection against oxidative stress is associated with activation of nuclear factor κB, J. Biol. Chem., 274, 9828, 10.1074/jbc.274.14.9828

Hendrickx, 2013, Epigenetic induction of EGR-1 expression by the amyloid precursor protein during exposure to novelty, PLoS ONE, 8, e74305, 10.1371/journal.pone.0074305

Hendrickx, 2014, Epigenetic regulations of immediate early genes expression involved in memory formation by the amyloid precursor protein of Alzheimer disease, PLoS ONE, 9, e99467, 10.1371/journal.pone.0099467

Huang, 2011, Long-term social isolation exacerbates the impairment of spatial working memory in APP/PS1 transgenic mice, Brain Res., 1371, 150, 10.1016/j.brainres.2010.11.043

Hudmon, 2005, CaMKII tethers to L-type Ca2+ channels, establishing a local and dedicated integrator of Ca2+ signals for facilitation, J. Cell Biol., 171, 537, 10.1083/jcb.200505155

Imbert, 1996, Tyrosine phosphorylation of IκB-α activates NF-κB without proteolytic degradation of IκB-α, Cell, 86, 787, 10.1016/S0092-8674(00)80153-1

Irie, 1997, Binding of neuroligins to PSD-95, Science, 277, 1511, 10.1126/science.277.5331.1511

Jacque, 2005, RelA repression of RelB activity induces selective gene activation downstream of TNF receptors, Proc. Natl. Acad. Sci. U.S.A., 102, 14635, 10.1073/pnas.0507342102

Jones, 2001, A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories, Nat. Neurosci., 4, 289, 10.1038/85138

Jourdain, 2003, Calcium/calmodulin-dependent protein kinase II contributes to activity-dependent filopodia growth and spine formation, J. Neurosci., 23, 10645, 10.1523/JNEUROSCI.23-33-10645.2003

Kairane, 2014, The effects of different antioxidants on the activity of cerebrocortical MnSOD and Na,K-ATPase from post mortem Alzheimer's disease and age-matched normal brains, Curr. Alzheimer Res., 11, 79, 10.2174/15672050113106660179

Kaltschmidt, 2002, Cyclooxygenase-2 is a neuronal target gene of NF-κB, BMC Mol. Biol., 3, 16, 10.1186/1471-2199-3-16

Kaltschmidt, 2006, NF-κB regulates spatial memory formation and synaptic plasticity through protein kinase A/CREB signaling, Mol. Cell. Biol., 26, 2936, 10.1128/MCB.26.8.2936-2946.2006

Kaltschmidt, 1997, Transcription factor NF-κB is activated in primary neurons by amyloid β peptides and in neurons surrounding early plaques from patients with Alzheimer disease, Proc. Natl. Acad. Sci. U.S.A., 94, 2642, 10.1073/pnas.94.6.2642

Kaltschmidt, 1999, Inhibition of NF-κB potentiates amyloid β-mediated neuronal apoptosis, Proc. Natl. Acad. Sci. U.S.A., 96, 9409, 10.1073/pnas.96.16.9409

Kandel, 2012, The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB, Mol. Brain, 5, 14, 10.1186/1756-6606-5-14

Kassed, 2004, Injury-induced NF-κB activation in the hippocampus: implications for neuronal survival, FASEB J., 18, 723, 10.1096/fj.03-0773fje

Khachaturian, 1994, Calcium hypothesis of Alzheimer's disease and brain aging, Ann. N.Y. Acad. Sci., 747, 1, 10.1111/j.1749-6632.1994.tb44398.x

Kiernan, 2003, Post-activation turn-off of NF-κB-dependent transcription is regulated by acetylation of p65, J. Biol. Chem., 278, 2758, 10.1074/jbc.M209572200

Kim, 2010, Ischemic preconditioning mediates cyclooxygenase-2 expression via nuclear factor-κB activation in mixed cortical neuronal cultures, Transl. Stroke Res., 1, 40, 10.1007/s12975-009-0006-8

Kitamura, 1997, Alteration of transcription factors NF-κB and STAT1 in Alzheimer's disease brains, Neurosci. Lett., 237, 17, 10.1016/S0304-3940(97)00797-0

Ko, 1998, Ca2+-mediated activation of c-Jun N-terminal kinase and nuclear factor κB by NMDA in cortical cell cultures, J. Neurochem., 71, 1390, 10.1046/j.1471-4159.1998.71041390.x

Kolesnick, 1994, The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signaling, Cell, 77, 325, 10.1016/0092-8674(94)90147-3

Kotilinek, 2008, Cyclooxygenase-2 inhibition improves amyloid-β-mediated suppression of memory and synaptic plasticity, Brain, 131, 651, 10.1093/brain/awn008

Kwok, 1994, Nuclear protein CBP is a coactivator for the transcription factor CREB, Nature, 370, 223, 10.1038/370223a0

Lanzillotta, 2010, The acetylation of RelA in Lys310 dictates the NF-κB-dependent response in post-ischemic injury, Cell Death Dis., 1, e96, 10.1038/cddis.2010.76

Laske, 2006, Stage-dependent BDNF serum concentrations in Alzheimer's disease, J. Neural Transm., 113, 1217, 10.1007/s00702-005-0397-y

Lee, 2005, Mitochondrial cyclic AMP response element-binding protein (CREB) mediates mitochondrial gene expression and neuronal survival, J. Biol. Chem., 280, 40398, 10.1074/jbc.C500140200

Lee, 2004, Independent cellular processes for hippocampal memory consolidation and reconsolidation, Science, 304, 839, 10.1126/science.1095760

Lemberger, 2008, CREB has a context-dependent role in activity-regulated transcription and maintains neuronal cholesterol homeostasis, FASEB J., 22, 2872, 10.1096/fj.08-107888

Li, 2004, Increased plaque burden in brains of APP mutant MnSOD heterozygous knockout mice, J. Neurochem., 89, 1308, 10.1111/j.1471-4159.2004.02455.x

Li, 2007, Egr3, a synaptic activity regulated transcription factor that is essential for learning and memory, Mol. Cell. Neurosci., 35, 76, 10.1016/j.mcn.2007.02.004

Liang, 2008, Altered neuronal gene expression in brain regions differentially affected by Alzheimer's disease: a reference data set, Physiol. Genomics, 33, 240, 10.1152/physiolgenomics.00242.2007

Lilienbaum, 2003, From calcium to NF-κB signaling pathways in neurons, Mol. Cell. Biol., 23, 2680, 10.1128/MCB.23.8.2680-2698.2003

Lim, 2011, Increased interactions between PKA and NF-κB signaling in the hippocampus following loss of cholinergic input, Neuroscience, 192, 485, 10.1016/j.neuroscience.2011.05.074

Lipsky, 2001, Nuclear factor κB is a critical determinant in N-methyl-D-aspartate receptor-mediated neuroprotection, J. Neurochem., 78, 254, 10.1046/j.1471-4159.2001.00386.x

Logan, 2011, Estrogen-induced signaling attenuates soluble Aβ peptide-mediated dysfunction of pathways in synaptic plasticity, Brain Res., 1383, 1, 10.1016/j.brainres.2011.01.038

Lu, 2014, BDNF and synaptic plasticity, cognitive function, and dysfunction, Handb. Exp. Pharmacol., 220, 223, 10.1007/978-3-642-45106-5_9

Lu, 2013, Spike-timing-dependent BDNF secretion and synaptic plasticity, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 369, 20130132, 10.1098/rstb.2013.0132

Lu, 2011, Early growth response 1 (Egr-1) regulates phosphorylation of microtubule-associated protein tau in mammalian brain, J. Biol. Chem., 286, 20569, 10.1074/jbc.M111.220962

Lukiw, 2012, NF-κB-regulated, proinflammatory miRNAs in Alzheimer's disease, Alzheimers. Res. Ther., 4, 47, 10.1186/alzrt150

Lukiw, 1998, Strong nuclear factor-κB-DNA binding parallels cyclooxygenase-2 gene transcription in aging and in sporadic Alzheimer's disease superior temporal lobe neocortex, J. Neurosci. Res., 53, 583, 10.1002/(SICI)1097-4547(19980901)53:5<583::AID-JNR8>3.0.CO;2-5

Ma, 2014, gammaCaMKII shuttles Ca(2)(+)/CaM to the nucleus to trigger CREB phosphorylation and gene expression, Cell, 159, 281, 10.1016/j.cell.2014.09.019

MacGibbon, 1997, Expression of Fos, Jun, and Krox family proteins in Alzheimer's disease, Exp. Neurol., 147, 316, 10.1006/exnr.1997.6600

Marcus, 2006, Differential neuronal expression of manganese superoxide dismutase in Alzheimer's disease, Med. Sci. Monit., 12, BR8-14

Marini, 2004, Role of brain-derived neurotrophic factor and NF-κB in neuronal plasticity and survival: From genes to phenotype, Restor. Neurol. Neurosci., 22, 121

Massaad, 2009, Overexpression of SOD-2 reduces hippocampal superoxide and prevents memory deficits in a mouse model of Alzheimer's disease, Proc. Natl. Acad. Sci. U.S.A., 106, 13576, 10.1073/pnas.0902714106

Mattson, 1997, Cellular actions of β-amyloid precursor protein and its soluble and fibrillogenic derivatives, Physiol. Rev., 77, 1081, 10.1152/physrev.1997.77.4.1081

Mattson, 1992, β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity, J. Neurosci., 12, 376, 10.1523/JNEUROSCI.12-02-00376.1992

Meffert, 2003, NF-κB functions in synaptic signaling and behavior, Nat. Neurosci., 6, 1072, 10.1038/nn1110

Melnikova, 2006, Cycloxygenase-2 activity promotes cognitive deficits but not increased amyloid burden in a model of Alzheimer's disease in a sex-dimorphic pattern, Neuroscience, 141, 1149, 10.1016/j.neuroscience.2006.05.001

Migaud, 1998, Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein, Nature, 396, 433, 10.1038/24790

Mihalas, 2013, Opposing action of nuclear factor κB and Polo-like kinases determines a homeostatic end point for excitatory synaptic adaptation, J. Neurosci., 33, 16490, 10.1523/JNEUROSCI.2131-13.2013

Millan, 2014, The epigenetic dimension of Alzheimer's disease: causal, consequence, or curiosity?, Dialog. Clin. Neurosci., 16, 373, 10.31887/DCNS.2014.16.3/mmillan

Millar, 1987, The toxic effects of ethylcholine mustard aziridinium ion on cholinergic cells in the chicken retina, J. Neurosci., 7, 343, 10.1523/JNEUROSCI.07-02-00343.1987

Min, 2013, The alterations of Ca2+/calmodulin/CaMKII/CaV1.2 signaling in experimental models of Alzheimer's disease and vascular dementia, Neurosci. Lett., 538, 60, 10.1016/j.neulet.2013.02.001

Mincheva-Tasheva, 2013, NF-κB signaling pathways: role in nervous system physiology and pathology, Neuroscientist, 19, 175, 10.1177/1073858412444007

Mota, 2015, Oxidative stress involving changes in Nrf2 and ER stress in early stages of Alzheimer's disease, Biochim. Biophys. Acta, 1852, 1428, 10.1016/j.bbadis.2015.03.015

Musso, 1997, Regulation of mouse neuropeptide Y Y1 receptor gene transcription: a potential role for nuclear factor-κB/Rel proteins, Mol. Pharmacol., 51, 27, 10.1124/mol.51.1.27

Nafez, 2015, Early growth response 2 (Egr-2) expression is triggered by NF-κB activation, Mol. Cell. Neurosci., 64, 95, 10.1016/j.mcn.2014.12.008

Niethammer, 1996, Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases, J. Neurosci., 16, 2157, 10.1523/JNEUROSCI.16-07-02157.1996

Noble, 2011, The lighter side of BDNF, Am. J. Physiol. Regul. Integr. Comp. Physiol., 300, R1053, 10.1152/ajpregu.00776.2010

Nogawa, 1997, Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage, J. Neurosci., 17, 2746, 10.1523/JNEUROSCI.17-08-02746.1997

Oddo, 2003a, Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease, Neurobiol. Aging, 24, 1063, 10.1016/j.neurobiolaging.2003.08.012

Oddo, 2003b, Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Aβ and synaptic dysfunction, Neuron, 39, 409, 10.1016/S0896-6273(03)00434-3

Okamoto, 2007, The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure, Proc. Natl. Acad. Sci. U.S.A., 104, 6418, 10.1073/pnas.0701656104

Ollivier, 1996, Elevated cyclic AMP inhibits NF-κB-mediated transcription in human monocytic cells and endothelial cells, J. Biol. Chem., 271, 20828, 10.1074/jbc.271.34.20828

O'Neal-Moffitt, 2015, Prophylactic melatonin significantly reduces Alzheimer's neuropathology and associated cognitive deficits independent of antioxidant pathways in AβPP(swe)/PS1 mice, Mol. Neurodegener., 10, 27, 10.1186/s13024-015-0027-6

Park, 2008, α-Isoform of calcium-calmodulin-dependent protein kinase II and postsynaptic density protein 95 differentially regulate synaptic expression of NR2A- and NR2B-containing N-methyl-d-aspartate receptors in hippocampus, Neuroscience, 151, 43, 10.1016/j.neuroscience.2007.09.075

Pasinetti, 1998, Cyclooxygenase and inflammation in Alzheimer's disease: experimental approaches and clinical interventions, J. Neurosci. Res., 54, 1, 10.1002/(SICI)1097-4547(19981001)54:1<1::AID-JNR1>3.0.CO;2-M

Pasinetti, 1998, Cyclooxygenase-2 expression is increased in frontal cortex of Alzheimer's disease brain, Neuroscience, 87, 319, 10.1016/S0306-4522(98)00218-8

Patel, 2008, Age-related differences in NFκB translocation and Bcl-2/Bax ratio caused by TNFα and Aβ42 promote survival in middle-age neurons and death in old neurons, Exp. Neurol., 213, 93, 10.1016/j.expneurol.2008.05.007

Paz-Y-Miño, 2015, Positive Association of the Cathepsin D Ala224Val Gene Polymorphism With the Risk of Alzheimer's Disease, Am. J. Med. Sci., 350, 296, 10.1097/MAJ.0000000000000555

Penke, 2013, Zif268/Egr1 gain of function facilitates hippocampal synaptic plasticity and long-term spatial recognition memory, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 369, 20130159, 10.1098/rstb.2013.0159

Pizzi, 2002, Opposing roles for NF-κB/Rel factors p65 and c-Rel in the modulation of neuron survival elicited by glutamate and interleukin-1β, J. Biol. Chem., 277, 20717, 10.1074/jbc.M201014200

Pizzi, 2005, NF-κB factor c-Rel mediates neuroprotection elicited by mGlu5 receptor agonists against amyloid β-peptide toxicity, Cell Death Differ., 12, 761, 10.1038/sj.cdd.4401598

Poirier, 2007, Paradoxical role of an Egr transcription factor family member, Egr2/Krox20, in learning and memory, Front. Behav. Neurosci., 1, 6, 10.3389/neuro.08.006.2007

Poirier, 2008, Distinct functions of egr gene family members in cognitive processes, Front. Neurosci., 2, 47, 10.3389/neuro.01.002.2008

Porte, 2008, Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus, Learn. Mem., 15, 885, 10.1101/lm.1094208

Post, 1998, Induction of NF-κB activity during haloperidol-induced oxidative toxicity in clonal hippocampal cells: suppression of NF-κB and neuroprotection by antioxidants, J. Neurosci., 18, 8236, 10.1523/JNEUROSCI.18-20-08236.1998

Rall, 2003, Intrahippocampal infusion of a cyclooxygenase-2 inhibitor attenuates memory acquisition in rats, Brain Res., 968, 273, 10.1016/S0006-8993(03)02248-0

Randall, 1992, Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons, J. Neurosci., 12, 1882, 10.1523/JNEUROSCI.12-05-01882.1992

Rao, 2012, Epigenetic modifications in frontal cortex from Alzheimer's disease and bipolar disorder patients, Transl. Psychiatry, 2, e132, 10.1038/tp.2012.55

Reese, 2011, Dysregulated phosphorylation of Ca(2+) /calmodulin-dependent protein kinase II-α in the hippocampus of subjects with mild cognitive impairment and Alzheimer's disease, J. Neurochem., 119, 791, 10.1111/j.1471-4159.2011.07447.x

Riquelme, 2011, High-frequency field stimulation of primary neurons enhances ryanodine receptor-mediated Ca2+ release and generates hydrogen peroxide, which jointly stimulate NF-κB activity, Antioxid. Redox Signal., 14, 1245, 10.1089/ars.2010.3238

Rohe, 2009, Brain-derived neurotrophic factor reduces amyloidogenic processing through control of SORLA gene expression, J. Neurosci., 29, 15472, 10.1523/JNEUROSCI.3960-09.2009

Rojo, 2004, Regulation of Cu/Zn-superoxide dismutase expression via the phosphatidylinositol 3 kinase/Akt pathway and nuclear factor-κB, J. Neurosci., 24, 7324, 10.1523/JNEUROSCI.2111-04.2004

Roselli, 2005, Soluble β-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses, J. Neurosci., 25, 11061, 10.1523/JNEUROSCI.3034-05.2005

Saha, 2009, TNF-α preconditioning protects neurons via neuron-specific up-regulation of CREB-binding protein, J. Immunol., 183, 2068, 10.4049/jimmunol.0801892

Salles, 2014, Synaptic NF-κB pathway in neuronal plasticity and memory, J. Physiol. Paris, 108, 256, 10.1016/j.jphysparis.2014.05.002

Santee, 1996, Human tumor necrosis factor receptor p75/80 (CD120b) gene structure and promoter characterization, J. Biol. Chem., 271, 21151, 10.1074/jbc.271.35.21151

Saura, 2011, The role of CREB signaling in Alzheimer's disease and other cognitive disorders, Rev. Neurosci., 22, 153, 10.1515/rns.2011.018

Savioz, 2014, A framework to understand the variations of PSD-95 expression in brain aging and in Alzheimer's disease, Ageing Res. Rev., 18, 86, 10.1016/j.arr.2014.09.004

Schoonbroodt, 2000, Oxidative stress interference with the nuclear factor-κB activation pathways, Biochem. Pharmacol., 60, 1075, 10.1016/S0006-2952(00)00371-3

Shankar, 2007, Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway, J. Neurosci., 27, 2866, 10.1523/JNEUROSCI.4970-06.2007

Shankar, 2008, Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory, Nat. Med., 14, 837, 10.1038/nm1782

Shao, 2011, Postsynaptic degeneration as revealed by PSD-95 reduction occurs after advanced Aβ and tau pathology in transgenic mouse models of Alzheimer's disease, Acta Neuropathol., 122, 285, 10.1007/s00401-011-0843-x

Shaywitz, 1999, CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals, Annu. Rev. Biochem., 68, 821, 10.1146/annurev.biochem.68.1.821

Sheng, 2012, Impaired mitochondrial biogenesis contributes to mitochondrial dysfunction in Alzheimer's disease, J. Neurochem., 120, 419, 10.1111/j.1471-4159.2011.07581.x

Shenkar, 1999, Mechanisms of lung neutrophil activation after hemorrhage or endotoxemia: roles of reactive oxygen intermediates, NF-κB, and cyclic AMP response element binding protein, J. Immunol., 163, 954, 10.4049/jimmunol.163.2.954

Shenkar, 2001, Interactions between CBP, NF-κB, and CREB in the lungs after hemorrhage and endotoxemia, Am. J. Physiol. Lung Cell. Mol. Physiol., 281, L418, 10.1152/ajplung.2001.281.2.L418

Sheppard, 1999, Transcriptional activation by NF-κB requires multiple coactivators, Mol. Cell. Biol., 19, 6367, 10.1128/MCB.19.9.6367

Shim, 2003, Aberrant protein expression of transcription factors BACH1 and ERG, both encoded on chromosome 21, in brains of patients with Down syndrome and Alzheimer's disease, J. Neural Transm. Suppl., 67, 39, 10.1007/978-3-7091-6721-2_3

Shrestha, 2006, Amyloid β peptide adversely affects spine number and motility in hippocampal neurons, Mol. Cell. Neurosci., 33, 274, 10.1016/j.mcn.2006.07.011

Silva, 1992a, Impaired spatial learning in α-calcium-calmodulin kinase II mutant mice, Science, 257, 206, 10.1126/science.1321493

Silva, 1992b, Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice, Science, 257, 201, 10.1126/science.1378648

Šimic, 2016, Tau protein hyperphosphorylation and aggregation in Alzheimer's Disease and other tauopathies, and possible neuroprotective strategies, Biomolecules, 6, 6, 10.3390/biom6010006

Snow, 2014, Roles for NF-κB and gene targets of NF-κB in synaptic plasticity, memory, and navigation, Mol. Neurobiol., 49, 757, 10.1007/s12035-013-8555-y

Sompol, 2008, A neuronal model of Alzheimer's disease: an insight into the mechanisms of oxidative stress-mediated mitochondrial injury, Neuroscience, 153, 120, 10.1016/j.neuroscience.2008.01.044

Song, 1999, Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses, Proc. Natl. Acad. Sci. U.S.A., 96, 1100, 10.1073/pnas.96.3.1100

Spisak, 2014, rs2070424 of the SOD1 gene is associated with risk of Alzheimer's disease, Neurol. Neurochir. Pol., 48, 342, 10.1016/j.pjnns.2014.09.002

Stratton, 2013, Activation-triggered subunit exchange between CaMKII holoenzymes facilitates the spread of kinase activity, Elife, 3, e01610, 10.7554/eLife.01610

Sun, 1994, Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity, Genes Dev., 8, 2527, 10.1101/gad.8.21.2527

Sun, 2011, Non-canonical NF-κB signaling pathway, Cell Res., 21, 71, 10.1038/cr.2010.177

Sun, 1993, NF-κB controls expression of inhibitor I κB α: evidence for an inducible autoregulatory pathway, Science, 259, 1912, 10.1126/science.8096091

Sweatt, 2016, Neural plasticity and behavior - sixty years of conceptual advances, J. Neurochem, 139, 179, 10.1111/jnc.13580

Tanaka, 2002, Generation of reactive oxygen species and activation of NF-κB by non-Aβ component of Alzheimer's disease amyloid, J. Neurochem., 82, 305, 10.1046/j.1471-4159.2002.00958.x

Tannenberg, 2006, Selective loss of synaptic proteins in Alzheimer's disease: evidence for an increased severity with APOE varepsilon4, Neurochem. Int., 49, 631, 10.1016/j.neuint.2006.05.004

Tao, 1998, Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism, Neuron, 20, 709, 10.1016/S0896-6273(00)81010-7

Teather, 2002, Post-training cyclooxygenase-2 (COX-2) inhibition impairs memory consolidation, Learn. Mem., 9, 41, 10.1101/lm.43602

Teich, 2015, Synaptic therapy in Alzheimer's disease: a CREB-centric approach, Neurotherapeutics, 12, 29, 10.1007/s13311-014-0327-5

Terai, 1996, Enhancement of immunoreactivity for NF-κB in the hippocampal formation and cerebral cortex of Alzheimer's disease, Brain Res., 735, 159, 10.1016/0006-8993(96)00310-1

Terry, 1991, Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment, Ann. Neurol., 30, 572, 10.1002/ana.410300410

Tong, 2001, β -amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival is not compromised, J. Biol. Chem., 276, 17301, 10.1074/jbc.M010450200

Valerio, 2006, NF-κB pathway: a target for preventing β-amyloid (Aβ)-induced neuronal damage and Aβ42 production, Eur. J. Neurosci., 23, 1711, 10.1111/j.1460-9568.2006.04722.x

Ventriglia, 2005, Lack of association between MnSOD gene polymorphism and sporadic Alzheimer's disease, Aging Clin. Exp. Res., 17, 445, 10.1007/BF03327410

Veyrac, 2014, The transcription factor Zif268/Egr1, brain plasticity, and memory, Prog. Mol. Biol. Transl. Sci., 122, 89, 10.1016/B978-0-12-420170-5.00004-0

Veyrac, 2013, Zif268/egr1 gene controls the selection, maturation and functional integration of adult hippocampal newborn neurons by learning, Proc. Natl. Acad. Sci. U.S.A., 110, 7062, 10.1073/pnas.1220558110

Vickers, 2006, Neurone specific regulation of dendritic spines in vivo by post synaptic density 95 protein (PSD-95), Brain Res., 1090, 89, 10.1016/j.brainres.2006.03.075

Wadgaonkar, 1999, CREB-binding protein is a nuclear integrator of nuclear factor-κB and p53 signaling, J. Biol. Chem., 274, 1879, 10.1074/jbc.274.4.1879

Wallace, 2016, Commentary: Age-related neurodegenerative disease research needs aging models, Front. Aging Neurosci., 8, 9, 10.3389/fnagi.2016.00009

Walton, 2000, Is CREB a key to neuronal survival?, Trends Neurosci., 23, 48, 10.1016/S0166-2236(99)01500-3

Wang, 2013, Naringin enhances CaMKII activity and improves long-term memory in a mouse model of Alzheimer's disease, Int. J. Mol. Sci., 14, 5576, 10.3390/ijms14035576

Wang, 2005, The expression of calcium/calmodulin-dependent protein kinase II-α in the hippocampus of patients with Alzheimer's disease and its links with AD-related pathology, Brain Res., 1031, 101, 10.1016/j.brainres.2004.10.061

Whitson, 1990, β-amyloid protein promotes neuritic branching in hippocampal cultures, Neurosci. Lett., 110, 319, 10.1016/0304-3940(90)90867-9

Whitson, 1989, Amyloid β protein enhances the survival of hippocampal neurons in vitro, Science, 243, 1488, 10.1126/science.2928783

Williams, 1995, Krox20 may play a key role in the stabilization of long-term potentiation, Brain Res. Mol. Brain Res., 28, 87, 10.1016/0169-328X(94)00187-J

Wood, 1995, Regulation of NF-κB activity in rat dorsal root ganglia and PC12 cells by tumour necrosis factor and nerve growth factor, Neurosci. Lett., 192, 41, 10.1016/0304-3940(95)11603-T

Yalcin, 2003, Apoptosis in cerebellar granule neurons is associated with reduced interaction between CREB-binding protein and NF-κB, J. Neurochem., 84, 397, 10.1046/j.1471-4159.2003.01540.x

Yamagata, 1993, Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids, Neuron, 11, 371, 10.1016/0896-6273(93)90192-T

Yan, 1995, Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid β-peptide, Nat. Med., 1, 693, 10.1038/nm0795-693

Yang, 1998, Upregulation of amyloid precursor protein gene promoter in rat primary hippocampal neurons by phorbol ester, IL-1 and retinoic acid, but not by reactive oxygen species, Brain Res. Mol. Brain Res., 60, 40, 10.1016/S0169-328X(98)00164-8

Yankner, 1990, Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides, Science, 250, 279, 10.1126/science.2218531

Yiu, 2011, Increasing CREB function in the CA1 region of dorsal hippocampus rescues the spatial memory deficits in a mouse model of Alzheimer's disease, Neuropsychopharmacology, 36, 2169, 10.1038/npp.2011.107

Yu, 1999, Lack of the p50 subunit of nuclear factor-κB increases the vulnerability of hippocampal neurons to excitotoxic injury, J. Neurosci., 19, 8856, 10.1523/JNEUROSCI.19-20-08856.1999

Zalcman, 2015, Nuclear factor κB-dependent Zif268 expression in hippocampus is required for recognition memory in mice, Neurobiol. Learn. Mem., 119, 10, 10.1016/j.nlm.2014.12.013

Zeng, 2010, Neurotrophins enhance CaMKII activity and rescue amyloid-β-induced deficits in hippocampal synaptic plasticity, J. Alzheimers. Dis., 21, 823, 10.3233/JAD-2010-100264

Zhang, 2012, Roles of brain-derived neurotrophic factor/tropomyosin-related kinase B (BDNF/TrkB) signaling in Alzheimer's disease, J. Clin. Neurosci., 19, 946, 10.1016/j.jocn.2011.12.022

Zhao, 2013, Regulation of TREM2 expression by an NF-small ka, CyrillicB-sensitive miRNA-34a, Neuroreport, 24, 318, 10.1097/WNR.0b013e32835fb6b0

Zheng, 2011, Structural studies of NF-κB signaling, Cell Res., 21, 183, 10.1038/cr.2010.171

Zhong, 2002, The phosphorylation status of nuclear NF-κB determines its association with CBP/p300 or HDAC-1, Mol. Cell, 9, 625, 10.1016/S1097-2765(02)00477-X

Zhong, 1997, The transcriptional activity of NF-κB is regulated by the IκB-associated PKAc subunit through a cyclic AMP-independent mechanism, Cell, 89, 413, 10.1016/S0092-8674(00)80222-6

Zhong, 1998, Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300, Mol. Cell, 1, 661, 10.1016/S1097-2765(00)80066-0