Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

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

Review Article

Synaptic Elimination in Neurological Disorders

Author(s): Pablo L. Cardozo, Izabella B. Q. de Lima, Esther M.A. Maciel, Nathália C. Silva, Tomas Dobransky and Fabíola M. Ribeiro*

Volume 17, Issue 11, 2019

Page: [1071 - 1095] Pages: 25

DOI: 10.2174/1570159X17666190603170511

conference banner
Abstract

Synapses are well known as the main structures responsible for transmitting information through the release and recognition of neurotransmitters by pre- and post-synaptic neurons. These structures are widely formed and eliminated throughout the whole lifespan via processes termed synaptogenesis and synaptic pruning, respectively. Whilst the first process is needed for ensuring proper connectivity between brain regions and also with the periphery, the second phenomenon is important for their refinement by eliminating weaker and unnecessary synapses and, at the same time, maintaining and favoring the stronger ones, thus ensuring proper synaptic transmission. It is well-known that synaptic elimination is modulated by neuronal activity. However, only recently the role of the classical complement cascade in promoting this phenomenon has been demonstrated. Specifically, microglial cells recognize activated complement component 3 (C3) bound to synapses targeted for elimination, triggering their engulfment. As this is a highly relevant process for adequate neuronal functioning, disruptions or exacerbations in synaptic pruning could lead to severe circuitry alterations that could underlie neuropathological alterations typical of neurological and neuropsychiatric disorders. In this review, we focus on discussing the possible involvement of excessive synaptic elimination in Alzheimer’s disease, as it has already been reported dendritic spine loss in post-synaptic neurons, increased association of complement proteins with its synapses and, hence, augmented microglia-mediated pruning in animal models of this disorder. In addition, we briefly discuss how this phenomenon could be related to other neurological disorders, including multiple sclerosis and schizophrenia.

Keywords: Synaptic elimination, synaptic plasticity, microglia, complement cascade, alzheimer’s disease, multiple sclerosis, schizophrenia.

« Previous
Graphical Abstract
[1]
Riccomagno, M.M.; Kolodkin, A.L. Sculpting neural circuits by axon and dendrite pruning. Annu. Rev. Cell Dev. Biol., 2015, 31, 779-805.
[http://dx.doi.org/10.1146/annurev-cellbio-100913-013038]
[2]
Lichtman, J.W.; Colman, H. Synapse elimination and indelible memory. Neuron, 2000, 25(2), 269-278.
[http://dx.doi.org/10.1016/S0896-6273(00)80893-4] [PMID: 10719884]
[3]
Kano, M.; Hashimoto, K. Synapse elimination in the central nervous system. Curr. Opin. Neurobiol., 2009, 19(2), 154-161.
[http://dx.doi.org/10.1016/j.conb.2009.05.002] [PMID: 19481442]
[4]
Yang, G.; Pan, F.; Gan, W.B. Stably maintained dendritic spines are associated with lifelong memories. Nature, 2009, 462(7275), 920-924.
[http://dx.doi.org/10.1038/nature08577] [PMID: 19946265]
[5]
Fukui, Y.; Bedi, K.S. Quantitative study of the development of neurons and synapses in rats reared in the dark during early postnatal life. 1. Superior colliculus. J. Anat., 1991, 174, 49-60.
[PMID: 2032942]
[6]
Chen, C.; Regehr, W.G. Developmental remodeling of the retinogeniculate synapse. Neuron, 2000, 28(3), 955-966.
[http://dx.doi.org/10.1016/S0896-6273(00)00166-5] [PMID: 11163279]
[7]
Cragg, B.G. The development of synapses in kitten visual cortex during visual deprivation. Exp. Neurol., 1975, 46(3), 445-451.
[http://dx.doi.org/10.1016/0014-4886(75)90118-1] [PMID: 1112285]
[8]
Shatz, C.J.; Stryker, M.P. Ocular dominance in layer IV of the cat’s visual cortex and the effects of monocular deprivation. J. Physiol., 1978, 281, 267-283.
[http://dx.doi.org/10.1113/jphysiol.1978.sp012421] [PMID: 702379]
[9]
Shatz, C.J.; Stryker, M.P. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science, 1988, 242(4875), 87-89.
[http://dx.doi.org/10.1126/science.3175636] [PMID: 3175636]
[10]
Huttenlocher, P.R.; Dabholkar, A.S. Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol., 1997, 387(2), 167-178.
[http://dx.doi.org/10.1002/(SICI)1096-9861(19971020)387:2<167:AID-CNE1>3.0.CO;2-Z] [PMID: 9336221]
[11]
Petanjek, Z.; Judaš, M.; Šimic, G.; Rasin, M.R.; Uylings, H.B.; Rakic, P.; Kostovic, I. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc. Natl. Acad. Sci. USA, 2011, 108(32), 13281-13286.
[http://dx.doi.org/10.1073/pnas.1105108108] [PMID: 21788513]
[12]
Hoshiko, M.; Arnoux, I.; Avignone, E.; Yamamoto, N.; Audinat, E. Deficiency of the microglial receptor CX3CR1 impairs postnatal functional development of thalamocortical synapses in the barrel cortex. J. Neurosci., 2012, 32(43), 15106-15111.
[http://dx.doi.org/10.1523/JNEUROSCI.1167-12.2012] [PMID: 23100431]
[13]
Nägerl, U.V.; Eberhorn, N.; Cambridge, S.B.; Bonhoeffer, T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron, 2004, 44(5), 759-767.
[http://dx.doi.org/10.1016/j.neuron.2004.11.016] [PMID: 15572108]
[14]
Yildirim, M.; Mapp, O.M.; Janssen, W.G.; Yin, W.; Morrison, J.H.; Gore, A.C. Postpubertal decrease in hippocampal dendritic spines of female rats. Exp. Neurol., 2008, 210(2), 339-348.
[http://dx.doi.org/10.1016/j.expneurol.2007.11.003] [PMID: 18096161]
[15]
Koss, W.A.; Belden, C.E.; Hristov, A.D.; Juraska, J.M. Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse, 2014, 68(2), 61-72.
[http://dx.doi.org/10.1002/syn.21716] [PMID: 24105875]
[16]
Huttenlocher, P.R. Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res., 1979, 163(2), 195-205.
[http://dx.doi.org/10.1016/0006-8993(79)90349-4] [PMID: 427544]
[17]
Hashimoto, K.; Kano, M. Synapse elimination in the devel-oping cerebellum. Cellular and molecular life sciences. Cell. Mol. Life Sci., 2013, 70(24), 4667-4680.
[http://dx.doi.org/10.1007/s00018-013-1405-2] [PMID: 23811844]
[18]
Elston, G.N.; Oga, T.; Fujita, I. Spinogenesis and pruning scales across functional hierarchies. J. Neurosci., 2009, 29(10), 3271-3275.
[http://dx.doi.org/10.1523/JNEUROSCI.5216-08.2009] [PMID: 19279264]
[19]
Stevens, B.; Allen, N.J.; Vazquez, L.E.; Howell, G.R.; Christopherson, K.S.; Nouri, N.; Micheva, K.D.; Mehalow, A.K.; Huberman, A.D.; Stafford, B.; Sher, A.; Litke, A.M.; Lambris, J.D.; Smith, S.J.; John, S.W.; Barres, B.A. The classical complement cascade mediates CNS synapse elimination. Cell, 2007, 131(6), 1164-1178.
[http://dx.doi.org/10.1016/j.cell.2007.10.036] [PMID: 18083105]
[20]
Bialas, A.R.; Stevens, B. TGF-β signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat. Neurosci., 2013, 16(12), 1773-1782.
[http://dx.doi.org/10.1038/nn.3560] [PMID: 24162655]
[21]
Tremblay, M.E.; Lowery, R.L.; Majewska, A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biol., 2010, 8(11)e1000527
[http://dx.doi.org/10.1371/journal.pbio.1000527] [PMID: 21072242]
[22]
Nimmerjahn, A.; Kirchhoff, F.; Helmchen, F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science, 2005, 308(5726), 1314-1318.
[http://dx.doi.org/10.1126/science.1110647] [PMID: 15831717]
[23]
Coleman, J.E.; Nahmani, M.; Gavornik, J.P.; Haslinger, R.; Heynen, A.J.; Erisir, A.; Bear, M.F. Rapid structural remodeling of thalamocortical synapses parallels experience-dependent functional plasticity in mouse primary visual cortex. J. Neurosci., 2010, 30(29), 9670-9682.
[http://dx.doi.org/10.1523/JNEUROSCI.1248-10.2010] [PMID: 20660250]
[24]
Zhou, Q.; Homma, K.J.; Poo, M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron, 2004, 44(5), 749-757.
[http://dx.doi.org/10.1016/j.neuron.2004.11.011] [PMID: 15572107]
[25]
De Roo, M.; Klauser, P.; Muller, D. LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol., 2008, 6(9)e219
[http://dx.doi.org/10.1371/journal.pbio.0060219] [PMID: 18788894]
[26]
Bastrikova, N.; Gardner, G.A.; Reece, J.M.; Jeromin, A.; Dudek, S.M. Synapse elimination accompanies functional plasticity in hippocampal neurons. Proc. Natl. Acad. Sci. USA, 2008, 105(8), 3123-3127.
[http://dx.doi.org/10.1073/pnas.0800027105] [PMID: 18287055]
[27]
Becker, N.; Wierenga, C.J.; Fonseca, R.; Bonhoeffer, T.; Nägerl, U.V. LTD induction causes morphological changes of presynaptic boutons and reduces their contacts with spines. Neuron, 2008, 60(4), 590-597.
[http://dx.doi.org/10.1016/j.neuron.2008.09.018] [PMID: 19038217]
[28]
Gladding, C.M.; Fitzjohn, S.M.; Molnár, E. Metabotropic glutamate receptor-mediated long-term depression: molecular mechanisms. Pharmacol. Rev., 2009, 61(4), 395-412.
[http://dx.doi.org/10.1124/pr.109.001735] [PMID: 19926678]
[29]
He, K.; Lee, A.; Song, L.; Kanold, P.O.; Lee, H.K. AMPA receptor subunit GluR1 (GluA1) serine-845 site is involved in synaptic depression but not in spine shrinkage associated with chemical long-term depression. J. Neurophysiol., 2011, 105(4), 1897-1907.
[http://dx.doi.org/10.1152/jn.00913.2010] [PMID: 21307330]
[30]
Brigman, J.L.; Wright, T.; Talani, G.; Prasad-Mulcare, S.; Jinde, S.; Seabold, G.K.; Mathur, P.; Davis, M.I.; Bock, R.; Gustin, R.M.; Colbran, R.J.; Alvarez, V.A.; Nakazawa, K.; Delpire, E.; Lovinger, D.M.; Holmes, A. Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J. Neurosci., 2010, 30(13), 4590-4600.
[31]
Wang, X.B.; Yang, Y.; Zhou, Q. Independent expression of synaptic and morphological plasticity associated with long-term depression. J. Neurosci., 2007, 27(45), 12419-12429.
[http://dx.doi.org/10.1523/JNEUROSCI.2015-07.2007] [PMID: 17989307]
[32]
Henson, M.A.; Tucker, C.J.; Zhao, M.; Dudek, S.M. Long-term depression-associated signaling is required for an in vitro model of NMDA receptor-dependent synapse pruning. Neurobiol. Learn. Mem., 2017, 138, 39-53.
[http://dx.doi.org/10.1016/j.nlm.2016.10.013] [PMID: 27794462]
[33]
Kano, M.; Hashimoto, K.; Kurihara, H.; Watanabe, M.; Inoue, Y.; Aiba, A.; Tonegawa, S. Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron, 1997, 18(1), 71-79.
[http://dx.doi.org/10.1016/S0896-6273(01)80047-7] [PMID: 9010206]
[34]
Ichise, T.; Kano, M.; Hashimoto, K.; Yanagihara, D.; Nakao, K.; Shigemoto, R.; Katsuki, M.; Aiba, A. mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science, 2000, 288(5472), 1832-1835.
[http://dx.doi.org/10.1126/science.288.5472.1832] [PMID: 10846166]
[35]
Huber, K.M.; Kayser, M.S.; Bear, M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science, 2000, 288(5469), 1254-1257.
[http://dx.doi.org/10.1126/science.288.5469.1254] [PMID: 10818003]
[36]
Narushima, M.; Uchigashima, M.; Yagasaki, Y.; Harada, T.; Nagumo, Y.; Uesaka, N.; Hashimoto, K.; Aiba, A.; Watanabe, M.; Miyata, M.; Kano, M. The Metabotropic glutamate receptor subtype 1 Mediates experience-dependent maintenance of mature synaptic connectivity in the visual thalamus. Neuron, 2016, 91(5), 1097-1109.
[http://dx.doi.org/10.1016/j.neuron.2016.07.035] [PMID: 27545713]
[37]
Chen, C.C.; Lu, H.C.; Brumberg, J.C. mGluR5 knockout mice display increased dendritic spine densities. Neurosci. Lett., 2012, 524(1), 65-68.
[http://dx.doi.org/10.1016/j.neulet.2012.07.014] [PMID: 22819970]
[38]
Shinoda, Y.; Tanaka, T.; Tominaga-Yoshino, K.; Ogura, A. Persistent synapse loss induced by repetitive LTD in developing rat hippocampal neurons. PLoS One, 2010, 5(4)e10390
[http://dx.doi.org/10.1371/journal.pone.0010390] [PMID: 20436928]
[39]
Shinoda, Y.; Kamikubo, Y.; Egashira, Y.; Tominaga-Yoshino, K.; Ogura, A. Repetition of mGluR-dependent LTD causes slowly developing persistent reduction in synaptic strength accompanied by synapse elimination. Brain Res., 2005, 1042(1), 99-107.
[http://dx.doi.org/10.1016/j.brainres.2005.02.028] [PMID: 15823258]
[40]
Wiegert, J.S.; Oertner, T.G. Long-term depression triggers the selective elimination of weakly integrated synapses. Proc. Natl. Acad. Sci. USA, 2013, 110(47), E4510-E4519.
[http://dx.doi.org/10.1073/pnas.1315926110] [PMID: 24191047]
[41]
Oh, W.C.; Hill, T.C.; Zito, K. Synapse-specific and size-dependent mechanisms of spine structural plasticity accompanying synaptic weakening. Proc. Natl. Acad. Sci. USA, 2013, 110(4), E305-E312.
[http://dx.doi.org/10.1073/pnas.1214705110] [PMID: 23269840]
[42]
Uesaka, N.; Uchigashima, M.; Mikuni, T.; Nakazawa, T.; Nakao, H.; Hirai, H.; Aiba, A.; Watanabe, M.; Kano, M. Retrograde semaphorin signaling regulates synapse elimination in the developing mouse brain. Science, 2014, 344(6187), 1020-1023.
[http://dx.doi.org/10.1126/science.1252514] [PMID: 24831527]
[43]
O’Connor, T.P.; Cockburn, K.; Wang, W.; Tapia, L.; Currie, E.; Bamji, S.X. Semaphorin 5B mediates synapse elimination in hippocampal neurons. Neural Dev., 2009, 4, 18.
[http://dx.doi.org/10.1186/1749-8104-4-18] [PMID: 19463192]
[44]
Nakayama, H.; Abe, M.; Morimoto, C.; Iida, T.; Okabe, S.; Sakimura, K.; Hashimoto, K. Microglia permit climbing fiber elimination by promoting GABAergic inhibition in the developing cerebellum. Nat. Commun., 2018, 9(1), 2830.
[http://dx.doi.org/10.1038/s41467-018-05100-z] [PMID: 30026565]
[45]
Afroz, S.; Parato, J.; Shen, H.; Smith, S.S. Synaptic pruning in the female hippocampus is triggered at puberty by extrasynaptic GABAA receptors on dendritic spines. eLife, 2016, 5e15106
[http://dx.doi.org/10.7554/eLife.15106] [PMID: 27136678]
[46]
Tao, W.; Díaz-Alonso, J.; Sheng, N.; Nicoll, R.A. Postsynaptic δ1 glutamate receptor assembles and maintains hippocampal synapses via Cbln2 and neurexin. Proc. Natl. Acad. Sci. USA, 2018, 115(23), E5373-E5381.
[http://dx.doi.org/10.1073/pnas.1802737115] [PMID: 29784783]
[47]
Uemura, T.; Lee, S.J.; Yasumura, M.; Takeuchi, T.; Yoshida, T.; Ra, M.; Taguchi, R.; Sakimura, K.; Mishina, M. Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell, 2010, 141(6), 1068-1079.
[http://dx.doi.org/10.1016/j.cell.2010.04.035] [PMID: 20537373]
[48]
Bian, W.J.; Miao, W.Y.; He, S.J.; Qiu, Z.; Yu, X. Coordinated spine pruning and maturation mediated by inter-spine competition for cadherin/catenin complexes. Cell, 2015, 162(4), 808-822.
[49]
Li, M. Y.; Miao, W. Y.; Wu, Q. Z.; He, S. J.; Yan, G.; Yang, Y.; Liu, J. J.; Taketo, M. M.; Yu, X. A critical role of presynaptic cadherin/ catenin/p140Cap complexes in stabilizing spines and functional synapses in the neocortex. Neuron, 2017, 94 (6), 1155-1172 e8..
[50]
Huh, G.S.; Boulanger, L.M.; Du, H.; Riquelme, P.A.; Brotz, T.M.; Shatz, C.J. Functional requirement for class I MHC in CNS development and plasticity. Science, 2000, 290(5499), 2155-2159.
[http://dx.doi.org/10.1126/science.290.5499.2155] [PMID: 11118151]
[51]
Goddard, C.A.; Butts, D.A.; Shatz, C.J. Regulation of CNS synapses by neuronal MHC class I. Proc. Natl. Acad. Sci. USA, 2007, 104(16), 6828-6833.
[http://dx.doi.org/10.1073/pnas.0702023104] [PMID: 17420446]
[52]
Lee, H.; Brott, B.K.; Kirkby, L.A.; Adelson, J.D.; Cheng, S.; Feller, M.B.; Datwani, A.; Shatz, C.J. Synapse elimination and learning rules co-regulated by MHC class I H2-Db. Nature, 2014, 509(7499), 195-200.
[http://dx.doi.org/10.1038/nature13154] [PMID: 24695230]
[53]
Adelson, J.D.; Sapp, R.W.; Brott, B.K.; Lee, H.; Miyamichi, K.; Luo, L.; Cheng, S.; Djurisic, M.; Shatz, C.J. Developmental sculpting of intracortical circuits by MHC class I H2-Db and H2-Kb. Cereb. Cortex, 2016, 26(4), 1453-1463.
[http://dx.doi.org/10.1093/cercor/bhu243] [PMID: 25316337]
[54]
Datwani, A.; McConnell, M.J.; Kanold, P.O.; Micheva, K.D.; Busse, B.; Shamloo, M.; Smith, S.J.; Shatz, C.J. Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity. Neuron, 2009, 64(4), 463-470.
[http://dx.doi.org/10.1016/j.neuron.2009.10.015] [PMID: 19945389]
[55]
Vidal, G. S.; Djurisic, M.; Brown, K.; Sapp, R. W.; Shatz, C. J. Cell-autonomous regulation of dendritic spine density by PirB eNeuro 3(5), 0089-16.
[56]
Syken, J.; Grandpre, T.; Kanold, P.O.; Shatz, C.J. PirB restricts ocular-dominance plasticity in visual cortex. Science, 2006, 313(5794), 1795-1800.
[http://dx.doi.org/10.1126/science.1128232] [PMID: 16917027]
[57]
Bochner, D.N.; Sapp, R.W.; Adelson, J.D.; Zhang, S.; Lee, H.; Djurisic, M.; Syken, J.; Dan, Y.; Shatz, C.J. Blocking PirB up-regulates spines and functional synapses to unlock visual cortical plasticity and facilitate recovery from amblyopia. Sci. Transl. Med., 2014, 6(258)258ra140
[http://dx.doi.org/10.1126/scitranslmed.3010157] [PMID: 25320232]
[58]
Djurisic, M.; Brott, B.K.; Saw, N.L.; Shamloo, M.; Shatz, C.J. Activity-dependent modulation of hippocampal synaptic plasticity via PirB and endocannabinoids. Mol. Psychiatry, 2018, 24(8), 1206-1219.
[PMID: 29670176]
[59]
VanGuilder Starkey, H.D.; Van Kirk, C.A.; Bixler, G.V.; Imperio, C.G.; Kale, V.P.; Serfass, J.M.; Farley, J.A.; Yan, H.; Warrington, J.P.; Han, S.; Mitschelen, M.; Sonntag, W.E.; Freeman, W.M. Neuroglial expression of the MHCI pathway and PirB receptor is upregulated in the hippocampus with advanced aging. J. Mol. Neurosci., 2012, 48(1), 111-126.
[60]
Stephan, A.H.; Madison, D.V.; Mateos, J.M.; Fraser, D.A.; Lovelett, E.A.; Coutellier, L.; Kim, L.; Tsai, H.H.; Huang, E.J.; Rowitch, D.H.; Berns, D.S.; Tenner, A.J.; Shamloo, M.; Barres, B.A. A dramatic increase of C1q protein in the CNS during normal aging. J. Neurosci., 2013, 33(33), 13460-13474.
[http://dx.doi.org/10.1523/JNEUROSCI.1333-13.2013] [PMID: 23946404]
[61]
Schafer, D.P.; Lehrman, E.K.; Kautzman, A.G.; Koyama, R.; Mardinly, A.R.; Yamasaki, R.; Ransohoff, R.M.; Greenberg, M.E.; Barres, B.A.; Stevens, B. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron, 2012, 74(4), 691-705.
[http://dx.doi.org/10.1016/j.neuron.2012.03.026] [PMID: 22632727]
[62]
Zhang, J.; Malik, A.; Choi, H.B.; Ko, R.W.; Dissing-Olesen, L.; MacVicar, B.A. Microglial CR3 activation triggers long-term synaptic depression in the hippocampus via NADPH oxidase. Neuron, 2014, 82(1), 195-207.
[http://dx.doi.org/10.1016/j.neuron.2014.01.043] [PMID: 24631344]
[63]
Ertürk, A.; Wang, Y.; Sheng, M. Local pruning of dendrites and spines by caspase-3-dependent and proteasome-limited mechanisms. J. Neurosci., 2014, 34(5), 1672-1688.
[http://dx.doi.org/10.1523/JNEUROSCI.3121-13.2014] [PMID: 24478350]
[64]
Györffy, B.A.; Kun, J.; Török, G.; Bulyáki, É.; Borhegyi, Z.; Gulyássy, P.; Kis, V.; Szocsics, P.; Micsonai, A.; Matkó, J.; Drahos, L.; Juhász, G.; Kékesi, K.A.; Kardos, J. Local apoptotic-like mechanisms underlie complement-mediated synaptic pruning. Proc. Natl. Acad. Sci. USA, 2018, 115(24), 6303-6308.
[http://dx.doi.org/10.1073/pnas.1722613115] [PMID: 29844190]
[65]
Fraser, D.A.; Pisalyaput, K.; Tenner, A.J. C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J. Neurochem., 2010, 112(3), 733-743.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06494.x] [PMID: 19919576]
[66]
Meng, L.; Mulcahy, B.; Cook, S.J.; Neubauer, M.; Wan, A.; Jin, Y.; Yan, D. The cell death pathway regulates synapse elimination through cleavage of gelsolin in caenorhabditis elegans neurons. Cell Rep., 2015, 11(11), 1737-1748.
[http://dx.doi.org/10.1016/j.celrep.2015.05.031] [PMID: 26074078]
[67]
Paolicelli, R.C.; Bolasco, G.; Pagani, F.; Maggi, L.; Scianni, M.; Panzanelli, P.; Giustetto, M.; Ferreira, T.A.; Guiducci, E.; Dumas, L.; Ragozzino, D.; Gross, C.T. Synaptic pruning by microglia is necessary for normal brain development. Science, 2011, 333(6048), 1456-1458.
[http://dx.doi.org/10.1126/science.1202529] [PMID: 21778362]
[68]
Zhan, Y.; Paolicelli, R.C.; Sforazzini, F.; Weinhard, L.; Bolasco, G.; Pagani, F.; Vyssotski, A.L.; Bifone, A.; Gozzi, A.; Ragozzino, D.; Gross, C.T. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci., 2014, 17(3), 400-406.
[http://dx.doi.org/10.1038/nn.3641] [PMID: 24487234]
[69]
Sokolowski, J.D.; Chabanon-Hicks, C.N.; Han, C.Z.; Heffron, D.S.; Mandell, J.W. Fractalkine is a “find-me” signal released by neurons undergoing ethanol-induced apoptosis. Front. Cell. Neurosci., 2014, 8, 360.
[http://dx.doi.org/10.3389/fncel.2014.00360] [PMID: 25426022]
[70]
Lui, H.; Zhang, J.; Makinson, S.R.; Cahill, M.K.; Kelley, K.W.; Huang, H.Y.; Shang, Y.; Oldham, M.C.; Martens, L.H.; Gao, F.; Coppola, G.; Sloan, S.A.; Hsieh, C.L.; Kim, C.C.; Bigio, E.H.; Weintraub, S.; Mesulam, M.M.; Rademakers, R.; Mackenzie, I.R.; Seeley, W.W.; Karydas, A.; Miller, B.L.; Borroni, B.; Ghidoni, R.; Farese, R.V., Jr; Paz, J.T.; Barres, B.A.; Huang, E.J. Progranulin deficiency promotes circuit-Specific synaptic pruning by microglia via complement activation. Cell, 2016, 165(4), 921-935.
[http://dx.doi.org/10.1016/j.cell.2016.04.001] [PMID: 27114033]
[71]
Chang, M.C.; Srinivasan, K.; Friedman, B.A.; Suto, E.; Modrusan, Z.; Lee, W.P.; Kaminker, J.S.; Hansen, D.V.; Sheng, M. Progranulin deficiency causes impairment of autophagy and TDP-43 accumulation. J. Exp. Med., 2017, 214(9), 2611-2628.
[http://dx.doi.org/10.1084/jem.20160999] [PMID: 28778989]
[72]
Zhang, K.; Li, Y.J.; Guo, Y.; Zheng, K.Y.; Yang, Q.; Yang, L.; Wang, X.S.; Song, Q.; Chen, T.; Zhuo, M.; Zhao, M.G. Elevated progranulin contributes to synaptic and learning deficit due to loss of fragile X mental retardation protein. Brain, 2017, 140(12), 3215-3232.
[http://dx.doi.org/10.1093/brain/awx265] [PMID: 29096020]
[73]
Kim, H.J.; Cho, M.H.; Shim, W.H.; Kim, J.K.; Jeon, E.Y.; Kim, D.H.; Yoon, S.Y. Deficient autophagy in microglia impairs synaptic pruning and causes social behavioral defects. Mol. Psychiatry, 2017, 22(11), 1576-1584.
[http://dx.doi.org/10.1038/mp.2016.103] [PMID: 27400854]
[74]
Vainchtein, I.D.; Chin, G.; Cho, F.S.; Kelley, K.W.; Miller, J.G.; Chien, E.C.; Liddelow, S.A.; Nguyen, P.T.; Nakao-Inoue, H.; Dorman, L.C.; Akil, O.; Joshita, S.; Barres, B.A.; Paz, J.T.; Molofsky, A.B.; Molofsky, A.V. Astrocyte-derived interleukin-33 promotes microglial synapse engulfment and neural circuit development. Science, 2018, 359(6381), 1269-1273.
[http://dx.doi.org/10.1126/science.aal3589] [PMID: 29420261]
[75]
Parkhurst, C.N.; Yang, G.; Ninan, I.; Savas, J.N.; Yates, J.R., III; Lafaille, J.J.; Hempstead, B.L.; Littman, D.R.; Gan, W.B. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell, 2013, 155(7), 1596-1609.
[http://dx.doi.org/10.1016/j.cell.2013.11.030] [PMID: 24360280]
[76]
Lehrman, E. K.; Wilton, D. K.; Litvina, E. Y.; Welsh, C. A.; Chang, S. T.; Frouin, A.; Walker, A. J.; Heller, M. D.; Umemori, H.; Chen, C.; Stevens, B. CD47 Protects Synapses from Excess Microglia-Mediated Pruning during Develop-ment. Neuron, 100(1), 120-134 e6.2018,.
[77]
Bjartmar, L.; Huberman, A.D.; Ullian, E.M.; Rentería, R.C.; Liu, X.; Xu, W.; Prezioso, J.; Susman, M.W.; Stellwagen, D.; Stokes, C.C.; Cho, R.; Worley, P.; Malenka, R.C.; Ball, S.; Peachey, N.S.; Copenhagen, D.; Chapman, B.; Nakamoto, M.; Barres, B.A.; Perin, M.S. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J. Neurosci., 2006, 26(23), 6269-6281.
[http://dx.doi.org/10.1523/JNEUROSCI.4212-05.2006] [PMID: 16763034]
[78]
Koch, S.M.; Ullian, E.M. Neuronal pentraxins mediate silent synapse conversion in the developing visual system. J. Neurosci., 2010, 30(15), 5404-5414.
[http://dx.doi.org/10.1523/JNEUROSCI.4893-09.2010] [PMID: 20392962]
[79]
Martinelli, D.C.; Chew, K.S.; Rohlmann, A.; Lum, M.Y.; Ressl, S.; Hattar, S.; Brunger, A.T.; Missler, M.; Südhof, T.C. Expression of C1ql3 in discrete neuronal populations controls efferent synapse numbers and diverse behaviors. Neuron, 2016, 91(5), 1034-1051.
[http://dx.doi.org/10.1016/j.neuron.2016.07.002] [PMID: 27478018]
[80]
Bolliger, M.F.; Martinelli, D.C.; Südhof, T.C. The cell-adhesion G protein-coupled receptor BAI3 is a high-affinity receptor for C1q-like proteins. Proc. Natl. Acad. Sci. USA, 2011, 108(6), 2534-2539.
[http://dx.doi.org/10.1073/pnas.1019577108] [PMID: 21262840]
[81]
Chen, P.B.; Kawaguchi, R.; Blum, C.; Achiro, J.M.; Coppola, G.; O’Dell, T.J.; Martin, K.C. Mapping Gene Expression in Excitatory Neurons during Hippocampal Late-Phase Long-Term Potentiation. Front. Mol. Neurosci., 2017, 10, 39.
[http://dx.doi.org/10.3389/fnmol.2017.00039] [PMID: 28275336]
[82]
Weinhard, L.; di Bartolomei, G.; Bolasco, G.; Machado, P.; Schieber, N.L.; Neniskyte, U.; Exiga, M.; Vadisiute, A.; Raggioli, A.; Schertel, A.; Schwab, Y.; Gross, C.T. Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction. Nat. Commun., 2018, 9(1), 1228.
[http://dx.doi.org/10.1038/s41467-018-03566-5] [PMID: 29581545]
[83]
Miyamoto, A.; Wake, H.; Ishikawa, A.W.; Eto, K.; Shibata, K.; Murakoshi, H.; Koizumi, S.; Moorhouse, A.J.; Yoshimura, Y.; Nabekura, J. Microglia contact induces synapse formation in developing somatosensory cortex. Nat. Commun., 2016, 7, 12540.
[http://dx.doi.org/10.1038/ncomms12540] [PMID: 27558646]
[84]
Shi, Q.; Colodner, K.J.; Matousek, S.B.; Merry, K.; Hong, S.; Kenison, J.E.; Frost, J.L.; Le, K.X.; Li, S.; Dodart, J.C.; Caldarone, B.J.; Stevens, B.; Lemere, C.A. Complement C3-Deficient mice fail to display age-related hippocampal decline. J. Neurosci., 2015, 35(38), 13029-13042.
[http://dx.doi.org/10.1523/JNEUROSCI.1698-15.2015] [PMID: 26400934]
[85]
Chung, W.S.; Clarke, L.E.; Wang, G.X.; Stafford, B.K.; Sher, A.; Chakraborty, C.; Joung, J.; Foo, L.C.; Thompson, A.; Chen, C.; Smith, S.J.; Barres, B.A. Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature, 2013, 504(7480), 394-400.
[http://dx.doi.org/10.1038/nature12776] [PMID: 24270812]
[86]
Patterson, C. World Alzheimer Report 2018; Alzheimer's Disease International (ADI): London, September. 2018. 2018, 1-48.
[87]
WHO), W. H. O., Towards a dementia plan: a WHO guide. Freel, S.; Seeher, K.; Chowdhary, N.; Sivananthan, S.; Pot, A. M., Eds. World Health Organization (WHO): Geneva, http://apps.who.int/iris/handle/10665/272642(accessed January 6th, 2019), 78.
[88]
Alzheimer, A.; Stelzmann, R.A.; Schnitzlein, H.N.; Murtagh, F.R. An English translation of Alzheimer’s 1907 paper, “Uber eine eigenartige Erkankung der Hirnrinde. Clin. Anat., 1995, 8(6), 429-431.
[89]
Colon, E.J. The cerebral cortex in presenile dementia. A quantitative analysis. Acta Neuropathol., 1973, 23(4), 281-290.
[http://dx.doi.org/10.1007/BF00687457] [PMID: 4718195]
[90]
Shefer, V.F. Absolute number of neurons and thickness of the cerebral cortex during aging, senile and vascular dementia, and Pick’s and Alzheimer’s diseases. Neurosci. Behav. Physiol., 1973, 6(4), 319-324.
[http://dx.doi.org/10.1007/BF01182672] [PMID: 4781784]
[91]
Najlerahim, A.; Bowen, D.M. Regional weight loss of the cerebral cortex and some subcortical nuclei in senile dementia of the Alzheimer type. Acta Neuropathol., 1988, 75(5), 509-512.
[http://dx.doi.org/10.1007/BF00687139] [PMID: 3376753]
[92]
Mann, D.M. Alzheimer’s disease and Down’s syndrome. Histopathology, 1988, 13(2), 125-137.
[http://dx.doi.org/10.1111/j.1365-2559.1988.tb02018.x] [PMID: 2971602]
[93]
Hubbard, B.M.; Anderson, J.M. A quantitative study of cerebral atrophy in old age and senile dementia. J. Neurol. Sci., 1981, 50(1), 135-145.
[http://dx.doi.org/10.1016/0022-510X(81)90048-4] [PMID: 7229656]
[94]
Davies, C.A.; Mann, D.M.; Sumpter, P.Q.; Yates, P.O. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer’s disease. J. Neurol. Sci., 1987, 78(2), 151-164.
[http://dx.doi.org/10.1016/0022-510X(87)90057-8] [PMID: 3572454]
[95]
Whitwell, J.L.; Przybelski, S.A.; Weigand, S.D.; Knopman, D.S.; Boeve, B.F.; Petersen, R.C.; Jack, C.R. Jr 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer’s disease. Brain, 2007, 130(Pt 7), 1777-1786.
[http://dx.doi.org/10.1093/brain/awm112] [PMID: 17533169]
[96]
Spires, T.L.; Meyer-Luehmann, M.; Stern, E.A.; McLean, P.J.; Skoch, J.; Nguyen, P.T.; Bacskai, B.J.; Hyman, B.T. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J. Neurosci., 2005, 25(31), 7278-7287.
[http://dx.doi.org/10.1523/JNEUROSCI.1879-05.2005]
[97]
Glenner, G.G.; Wong, C.W. Alzheimer’s disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun., 1984, 120(3), 885-890.
[http://dx.doi.org/10.1016/S0006-291X(84)80190-4] [PMID: 6375662]
[98]
Masters, C.L.; Multhaup, G.; Simms, G.; Pottgiesser, J.; Martins, R.N.; Beyreuther, K. Neuronal origin of a cerebral amyloid: neurofibrillary tangles of Alzheimer’s disease contain the same protein as the amyloid of plaque cores and blood vessels. EMBO J., 1985, 4(11), 2757-2763.
[http://dx.doi.org/10.1002/j.1460-2075.1985.tb04000.x] [PMID: 4065091]
[99]
Masters, C.L.; Simms, G.; Weinman, N.A.; Multhaup, G.; McDonald, B.L.; Beyreuther, K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. USA, 1985, 82(12), 4245-4249.
[http://dx.doi.org/10.1073/pnas.82.12.4245] [PMID: 3159021]
[100]
Knafo, S.; Alonso-Nanclares, L.; Gonzalez-Soriano, J.; Merino-Serrais, P.; Fernaud-Espinosa, I.; Ferrer, I.; DeFelipe, J. Widespread changes in dendritic spines in a model of Alzheimer’s disease. Cereb. Cortex, 2009, 19(3), 586-592.
[http://dx.doi.org/10.1093/cercor/bhn111] [PMID: 18632740]
[101]
Yoshiyama, Y.; Higuchi, M.; Zhang, B.; Huang, S.M.; Iwata, N.; Saido, T.C.; Maeda, J.; Suhara, T.; Trojanowski, J.Q.; Lee, V.M. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron, 2007, 53(3), 337-351.
[http://dx.doi.org/10.1016/j.neuron.2007.01.010] [PMID: 17270732]
[102]
Kandimalla, R.; Manczak, M.; Yin, X.; Wang, R.; Reddy, P.H. Hippocampal phosphorylated tau induced cognitive decline, dendritic spine loss and mitochondrial abnormalities in a mouse model of Alzheimer’s disease. Hum. Mol. Genet., 2018, 27(1), 30-40.
[http://dx.doi.org/10.1093/hmg/ddx381] [PMID: 29040533]
[103]
Hamelin, L.; Lagarde, J.; Dorothée, G.; Potier, M.C.; Corlier, F.; Kuhnast, B.; Caillé, F.; Dubois, B.; Fillon, L.; Chupin, M.; Bottlaender, M.; Sarazin, M. Distinct dynamic profiles of microglial activation are associated with progression of Alzheimer’s disease. Brain, 2018, 141(6), 1855-1870.
[http://dx.doi.org/10.1093/brain/awy079] [PMID: 29608645]
[104]
Dani, M.; Wood, M.; Mizoguchi, R.; Fan, Z.; Walker, Z.; Morgan, R.; Hinz, R.; Biju, M.; Kuruvilla, T.; Brooks, D.J.; Edison, P. Microglial activation correlates in vivo with both tau and amyloid in Alzheimer’s disease. Brain, 2018, 141(9), 2740-2754.
[http://dx.doi.org/10.1093/brain/awy188] [PMID: 30052812]
[105]
Xiang, Z.; Haroutunian, V.; Ho, L.; Purohit, D.; Pasinetti, G.M. Microglia activation in the brain as inflammatory biomarker of Alzheimer’s disease neuropathology and clinical dementia. Dis. Markers, 2006, 22(1-2), 95-102.
[http://dx.doi.org/10.1155/2006/276239] [PMID: 16410654]
[106]
Kang, J.; Lemaire, H.G.; Unterbeck, A.; Salbaum, J.M.; Masters, C.L.; Grzeschik, K.H.; Multhaup, G.; Beyreuther, K.; Müller-Hill, B. The precursor of Alzheimer’s disease amyloid A4 protein resembles a cell-surface receptor. Nature, 1987, 325(6106), 733-736.
[http://dx.doi.org/10.1038/325733a0] [PMID: 2881207]
[107]
Shoji, M.; Golde, T.E.; Ghiso, J.; Cheung, T.T.; Estus, S.; Shaffer, L.M.; Cai, X.D.; McKay, D.M.; Tintner, R.; Frangione, B. Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science, 1992, 258(5079), 126-129.
[http://dx.doi.org/10.1126/science.1439760] [PMID: 1439760]
[108]
Kimberly, W.T.; Esler, W.P.; Ye, W.; Ostaszewski, B.L.; Gao, J.; Diehl, T.; Selkoe, D.J.; Wolfe, M.S. Notch and the amyloid precursor protein are cleaved by similar gamma-secretase(s). Biochemistry, 2003, 42(1), 137-144.
[http://dx.doi.org/10.1021/bi026888g] [PMID: 12515548]
[109]
Kimberly, W.T.; Wolfe, M.S. Identity and function of gamma-secretase. J. Neurosci. Res., 2003, 74(3), 353-360.
[http://dx.doi.org/10.1002/jnr.10736] [PMID: 14598311]
[110]
Vassar, R.; Bennett, B.D.; Babu-Khan, S.; Kahn, S.; Mendiaz, E.A.; Denis, P.; Teplow, D.B.; Ross, S.; Amarante, P.; Loeloff, R.; Luo, Y.; Fisher, S.; Fuller, J.; Edenson, S.; Lile, J.; Jarosinski, M.A.; Biere, A.L.; Curran, E.; Burgess, T.; Louis, J.C.; Collins, F.; Treanor, J.; Rogers, G.; Citron, M. Beta-secretase cleavage of Alzheimer’s amyloid precursor protein by the transmembrane aspartic protease BACE. Science, 1999, 286(5440), 735-741.
[http://dx.doi.org/10.1126/science.286.5440.735] [PMID: 10531052]
[111]
Szaruga, M.; Veugelen, S.; Benurwar, M.; Lismont, S.; Sepulveda-Falla, D.; Lleo, A.; Ryan, N.S.; Lashley, T.; Fox, N.C.; Murayama, S.; Gijsen, H.; De Strooper, B.; Chávez-Gutiérrez, L. Qualitative changes in human γ-secretase underlie familial Alzheimer’s disease. J. Exp. Med., 2015, 212(12), 2003-2013.
[http://dx.doi.org/10.1084/jem.20150892] [PMID: 26481686]
[112]
Fu, L.; Sun, Y.; Guo, Y.; Chen, Y.; Yu, B.; Zhang, H.; Wu, J.
Yu, X.; Kong, W.; Wu, H. Comparison of neurotoxicity of different aggregated forms of Abeta40, Abeta42 and Abeta43 in cell cultures. Journal of peptide science. Eur. Peptide Soc., 2017, 23(3), 245-251.
[113]
Lue, L.F.; Kuo, Y.M.; Roher, A.E.; Brachova, L.; Shen, Y.; Sue, L.; Beach, T.; Kurth, J.H.; Rydel, R.E.; Rogers, J. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer’s disease. Am. J. Pathol., 1999, 155(3), 853-862.
[http://dx.doi.org/10.1016/S0002-9440(10)65184-X] [PMID: 10487842]
[114]
Tomiyama, T.; Matsuyama, S.; Iso, H.; Umeda, T.; Takuma, H.; Ohnishi, K.; Ishibashi, K.; Teraoka, R.; Sakama, N.; Yamashita, T.; Nishitsuji, K.; Ito, K.; Shimada, H.; Lambert, M.P.; Klein, W.L.; Mori, H. A mouse model of amyloid beta oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo. J. Neurosci., 2010, 30(14), 4845-4856.
[http://dx.doi.org/10.1523/JNEUROSCI.5825-09.2010] [PMID: 20371804]
[115]
Lambert, M.P.; Barlow, A.K.; Chromy, B.A.; Edwards, C.; Freed, R.; Liosatos, M.; Morgan, T.E.; Rozovsky, I.; Trommer, B.; Viola, K.L.; Wals, P.; Zhang, C.; Finch, C.E.; Krafft, G.A.; Klein, W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA, 1998, 95(11), 6448-6453.
[http://dx.doi.org/10.1073/pnas.95.11.6448] [PMID: 9600986]
[116]
Shankar, G.M.; Bloodgood, B.L.; Townsend, M.; Walsh, D.M.; Selkoe, D.J.; Sabatini, B.L. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci., 2007, 27(11), 2866-2875.
[http://dx.doi.org/10.1523/JNEUROSCI.4970-06.2007] [PMID: 17360908]
[117]
Wei, W.; Nguyen, L.N.; Kessels, H.W.; Hagiwara, H.; Sisodia, S.; Malinow, R. Amyloid beta from axons and dendrites reduces local spine number and plasticity. Nat. Neurosci., 2010, 13(2), 190-196.
[http://dx.doi.org/10.1038/nn.2476] [PMID: 20037574]
[118]
Stéphan, A.; Laroche, S.; Davis, S. Generation of aggregated beta-amyloid in the rat hippocampus impairs synaptic transmission and plasticity and causes memory deficits. J. Neurosci., 2001, 21(15), 5703-5714.
[http://dx.doi.org/10.1523/JNEUROSCI.21-15-05703.2001] [PMID: 11466442]
[119]
Wang, H.W.; Pasternak, J.F.; Kuo, H.; Ristic, H.; Lambert, M.P.; Chromy, B.; Viola, K.L.; Klein, W.L.; Stine, W.B.; Krafft, G.A.; Trommer, B.L. Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res., 2002, 924(2), 133-140.
[http://dx.doi.org/10.1016/S0006-8993(01)03058-X] [PMID: 11750898]
[120]
Shankar, G.M.; Li, S.; Mehta, T.H.; Garcia-Munoz, A.; Shepardson, N.E.; Smith, I.; Brett, F.M.; Farrell, M.A.; Rowan, M.J.; Lemere, C.A.; Regan, C.M.; Walsh, D.M.; Sabatini, B.L.; Selkoe, D.J. Amyloid-beta protein dimers isolated directly from Alzheimer’s brains impair synaptic plasticity and memory. Nat. Med., 2008, 14(8), 837-842.
[http://dx.doi.org/10.1038/nm1782] [PMID: 18568035]
[121]
Wang, Z.; Jackson, R.J.; Hong, W.; Taylor, W.M.; Corbett, G.T.; Moreno, A.; Liu, W.; Li, S.; Frosch, M.P.; Slutsky, I.; Young-Pearse, T.L.; Spires-Jones, T.L.; Walsh, D.M. Human Brain-Derived Aβ Oligomers Bind to Synapses and Disrupt Synaptic Activity in a Manner That Requires APP. J. Neurosci., 2017, 37(49), 11947-11966.
[http://dx.doi.org/10.1523/JNEUROSCI.2009-17.2017] [PMID: 29101243]
[122]
Chen, Q.S.; Kagan, B.L.; Hirakura, Y.; Xie, C.W. Impairment of hippocampal long-term potentiation by Alzheimer amyloid beta-peptides. J. Neurosci. Res., 2000, 60(1), 65-72.
[http://dx.doi.org/10.1002/(SICI)10974547(20000401)60:1<65:AID-JNR7>3.0.CO;2-Q] [PMID: 10723069]
[123]
Walsh, D.M.; Klyubin, I.; Fadeeva, J.V.; Cullen, W.K.; Anwyl, R.; Wolfe, M.S.; Rowan, M.J.; Selkoe, D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature, 2002, 416(6880), 535-539.
[http://dx.doi.org/10.1038/416535a] [PMID: 11932745]
[124]
Li, S.; Hong, S.; Shepardson, N.E.; Walsh, D.M.; Shankar, G.M.; Selkoe, D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron, 2009, 62(6), 788-801.
[http://dx.doi.org/10.1016/j.neuron.2009.05.012] [PMID: 19555648]
[125]
Hsieh, H.; Boehm, J.; Sato, C.; Iwatsubo, T.; Tomita, T.; Sisodia, S.; Malinow, R. AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron, 2006, 52(5), 831-843.
[http://dx.doi.org/10.1016/j.neuron.2006.10.035] [PMID: 17145504]
[126]
Talantova, M.; Sanz-Blasco, S.; Zhang, X.; Xia, P.; Akhtar, M.W.; Okamoto, S.; Dziewczapolski, G.; Nakamura, T.; Cao, G.; Pratt, A.E.; Kang, Y.J.; Tu, S.; Molokanova, E.; McKercher, S.R.; Hires, S.A.; Sason, H.; Stouffer, D.G.; Buczynski, M.W.; Solomon, J.P.; Michael, S.; Powers, E.T.; Kelly, J.W.; Roberts, A.; Tong, G.; Fang-Newmeyer, T.; Parker, J.; Holland, E.A.; Zhang, D.; Nakanishi, N.; Chen, H.S.; Wolosker, H.; Wang, Y.; Parsons, L.H.; Ambasudhan, R.; Masliah, E.; Heinemann, S.F.; Piña-Crespo, J.C.; Lipton, S.A. Aβ induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc. Natl. Acad. Sci. USA, 2013, 110(27), E2518-E2527.
[http://dx.doi.org/10.1073/pnas.1306832110] [PMID: 23776240]
[127]
Lei, M.; Xu, H.; Li, Z.; Wang, Z.; O’Malley, T.T.; Zhang, D.; Walsh, D.M.; Xu, P.; Selkoe, D.J.; Li, S. Soluble Aβ oligomers impair hippocampal LTP by disrupting glutamatergic/GABAergic balance. Neurobiol. Dis., 2016, 85, 111-121.
[http://dx.doi.org/10.1016/j.nbd.2015.10.019] [PMID: 26525100]
[128]
Zhao, J.; Li, A.; Rajsombath, M.; Dang, Y.; Selkoe, D. J.; Li, S. Soluble Abeta Oligomers Impair Dipolar Heterodendritic Plasticity by Activation of mGluR in the Hippocampal CA1 Region iScience, 6, 138-150 2018.
[129]
Molokanova, E.; Akhtar, M.W.; Sanz-Blasco, S.; Tu, S.; Piña-Crespo, J.C.; McKercher, S.R.; Lipton, S.A. Differential effects of synaptic and extrasynaptic NMDA receptors on Aβ-induced nitric oxide production in cerebrocortical neurons. J. Neurosci., 2014, 34(14), 5023-5028.
[http://dx.doi.org/10.1523/JNEUROSCI.2907-13.2014] [PMID: 24695719]
[130]
Qu, J.; Nakamura, T.; Cao, G.; Holland, E.A.; McKercher, S.R.; Lipton, S.A. S-Nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by beta-amyloid peptide. Proc. Natl. Acad. Sci. USA, 2011, 108(34), 14330-14335.
[http://dx.doi.org/10.1073/pnas.1105172108] [PMID: 21844361]
[131]
Cleary, J.P.; Walsh, D.M.; Hofmeister, J.J.; Shankar, G.M.; Kuskowski, M.A.; Selkoe, D.J.; Ashe, K.H. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci., 2005, 8(1), 79-84.
[http://dx.doi.org/10.1038/nn1372] [PMID: 15608634]
[132]
Figueiredo, C.P.; Clarke, J.R.; Ledo, J.H.; Ribeiro, F.C.; Costa, C.V.; Melo, H.M.; Mota-Sales, A.P.; Saraiva, L.M.; Klein, W.L.; Sebollela, A.; De Felice, F.G.; Ferreira, S.T. Memantine rescues transient cognitive impairment caused by high-molecular-weight aβ oligomers but not the persistent impairment induced by low-molecular-weight oligomers. J. Neurosci., 2013, 33(23), 9626-9634.
[http://dx.doi.org/10.1523/JNEUROSCI.0482-13.2013] [PMID: 23739959]
[133]
Ledo, J.H.; Azevedo, E.P.; Clarke, J.R.; Ribeiro, F.C.; Figueiredo, C.P.; Foguel, D.; De Felice, F.G.; Ferreira, S.T. Amyloid-β oligomers link depressive-like behavior and cognitive deficits in mice. Mol. Psychiatry, 2013, 18(10), 1053-1054.
[http://dx.doi.org/10.1038/mp.2012.168] [PMID: 23183490]
[134]
Morroni, F.; Sita, G.; Tarozzi, A.; Rimondini, R.; Hrelia, P. Early effects of Aβ1-42 oligomers injection in mice: Involvement of PI3K/Akt/GSK3 and MAPK/ERK1/2 pathways. Behav. Brain Res., 2016, 314, 106-115.
[http://dx.doi.org/10.1016/j.bbr.2016.08.002] [PMID: 27498145]
[135]
King, R.D.; Brown, B.; Hwang, M.; Jeon, T.; George, A.T. Alzheimer’s Disease neuroimaging initiative. Fractal dimension analysis of the cortical ribbon in mild Alzheimer’s disease. Neuroimage, 2010, 53(2), 471-479.
[http://dx.doi.org/10.1016/j.neuroimage.2010.06.050] [PMID: 20600974]
[136]
Clare, R.; King, V.G.; Wirenfeldt, M.; Vinters, H.V. Synapse loss in dementias. J. Neurosci. Res., 2010, 88(10), 2083-2090.
[http://dx.doi.org/10.1002/jnr.22392] [PMID: 20533377]
[137]
Scheff, S.W.; Price, D.A.; Schmitt, F.A.; Mufson, E.J. Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol. Aging, 2006, 27(10), 1372-1384.
[http://dx.doi.org/10.1016/j.neurobiolaging.2005.09.012] [PMID: 16289476]
[138]
Scheff, S.W.; Price, D.A.; Schmitt, F.A.; DeKosky, S.T.; Mufson, E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology, 2007, 68(18), 1501-1508.
[http://dx.doi.org/10.1212/01.wnl.0000260698.46517.8f] [PMID: 17470753]
[139]
Scheff, S.W.; Price, D.A. Synapse loss in the temporal lobe in Alzheimer’s disease. Ann. Neurol., 1993, 33(2), 190-199.
[http://dx.doi.org/10.1002/ana.410330209] [PMID: 8434881]
[140]
Scheff, S.W.; DeKosky, S.T.; Price, D.A. Quantitative assessment of cortical synaptic density in Alzheimer’s disease. Neurobiol. Aging, 1990, 11(1), 29-37.
[http://dx.doi.org/10.1016/0197-4580(90)90059-9] [PMID: 2325814]
[141]
Reddy, P.H.; Mani, G.; Park, B.S.; Jacques, J.; Murdoch, G.; Whetsell, W., Jr; Kaye, J.; Manczak, M. Differential loss of synaptic proteins in Alzheimer’s disease: implications for synaptic dysfunction. J. Alzheimers Dis., 2005, 7(2), 103-117.
[http://dx.doi.org/10.3233/JAD-2005-7203] [PMID: 15851848]
[142]
Scheff, S.W.; Price, D.A.; Schmitt, F.A.; Roberts, K.N.; Ikonomovic, M.D.; Mufson, E.J. Synapse stability in the precuneus early in the progression of Alzheimer’s disease. J. Alzheimers Dis., 2013, 35(3), 599-609.
[http://dx.doi.org/10.3233/JAD-122353] [PMID: 23478309]
[143]
Honer, W.G. Pathology of presynaptic proteins in Alzheimer’s disease: more than simple loss of terminals. Neurobiol. Aging, 2003, 24(8), 1047-1062.
[http://dx.doi.org/10.1016/j.neurobiolaging.2003.04.005] [PMID: 14643376]
[144]
Masliah, E.; Mallory, M.; Alford, M.; DeTeresa, R.; Hansen, L.A.; McKeel, D.W., Jr; Morris, J.C. Altered expression of synaptic proteins occurs early during progression of Alzheimer’s disease. Neurology, 2001, 56(1), 127-129.
[http://dx.doi.org/10.1212/WNL.56.1.127] [PMID: 11148253]
[145]
Wakabayashi, K.; Honer, W.G.; Masliah, E. Synapse alterations in the hippocampal-entorhinal formation in Alzheimer’s disease with and without Lewy body disease. Brain Res., 1994, 667(1), 24-32.
[http://dx.doi.org/10.1016/0006-8993(94)91709-4] [PMID: 7895080]
[146]
Marksteiner, J.; Kaufmann, W.A.; Gurka, P.; Humpel, C. Synaptic proteins in Alzheimer’s disease. Journal of Molecular Neuroscience: MN, 2002, 18(1-2), 53-63.
[http://dx.doi.org/10.1385/JMN:18:1-2:53]
[147]
Almeida, C.G.; Tampellini, D.; Takahashi, R.H.; Greengard, P.; Lin, M.T.; Snyder, E.M.; Gouras, G.K. Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol. Dis., 2005, 20(2), 187-198.
[http://dx.doi.org/10.1016/j.nbd.2005.02.008] [PMID: 16242627]
[148]
Canas, P. M.; Simoes, A. P.; Rodrigues, R. J.; Cunha, R. A. Predominant loss of glutamatergic terminal markers in a beta-amyloid peptide model of Alzheimer's disease. Neuropharmacology, , 2014, 76(Pt A), 51-56.
[149]
Berchtold, N.C.; Coleman, P.D.; Cribbs, D.H.; Rogers, J.; Gillen, D.L.; Cotman, C.W. Synaptic genes are extensively downregulated across multiple brain regions in normal human aging and Alzheimer’s disease. Neurobiol. Aging, 2013, 34(6), 1653-1661.
[http://dx.doi.org/10.1016/j.neurobiolaging.2012.11.024] [PMID: 23273601]
[150]
Mitew, S.; Kirkcaldie, M.T.; Dickson, T.C.; Vickers, J.C. Altered synapses and gliotransmission in Alzheimer’s disease and AD model mice. Neurobiol. Aging, 2013, 34(10), 2341-2351.
[http://dx.doi.org/10.1016/j.neurobiolaging.2013.04.010] [PMID: 23643146]
[151]
Roselli, F.; Tirard, M.; Lu, J.; Hutzler, P.; Lamberti, P.; Livrea, P.; Morabito, M.; Almeida, O.F. Soluble beta-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses. J. Neurosci., 2005, 25(48), 11061-11070.
[http://dx.doi.org/10.1523/JNEUROSCI.3034-05.2005] [PMID: 16319306]
[152]
Sze, C.I.; Bi, H.; Kleinschmidt-DeMasters, B.K.; Filley, C.M.; Martin, L.J. Selective regional loss of exocytotic presynaptic vesicle proteins in Alzheimer’s disease brains. J. Neurol. Sci., 2000, 175(2), 81-90.
[http://dx.doi.org/10.1016/S0022-510X(00)00285-9] [PMID: 10831767]
[153]
DeKosky, S.T.; Scheff, S.W. Synapse loss in frontal cortex biopsies in Alzheimer’s disease: correlation with cognitive severity. Ann. Neurol., 1990, 27(5), 457-464.
[http://dx.doi.org/10.1002/ana.410270502] [PMID: 2360787]
[154]
Terry, R.D.; Masliah, E.; Salmon, D.P.; Butters, N.; DeTeresa, R.; Hill, R.; Hansen, L.A.; Katzman, R. Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol., 1991, 30(4), 572-580.
[http://dx.doi.org/10.1002/ana.410300410] [PMID: 1789684]
[155]
Chen, M.K.; Mecca, A.P.; Naganawa, M.; Finnema, S.J.; Toyonaga, T.; Lin, S.F.; Najafzadeh, S.; Ropchan, J.; Lu, Y.; McDonald, J.W.; Michalak, H.R.; Nabulsi, N.B.; Arnsten, A.F.T.; Huang, Y.; Carson, R.E.; van Dyck, C.H. Assessing Synaptic Density in Alzheimer Disease With Synaptic Vesicle Glycoprotein 2A Positron Emission Tomographic Imaging. JAMA Neurol., 2018, 75(10), 1215-1224.
[http://dx.doi.org/10.1001/jamaneurol.2018.1836] [PMID: 30014145]
[156]
Jackson, R.J.; Rudinskiy, N.; Herrmann, A.G.; Croft, S.; Kim, J.M.; Petrova, V.; Ramos-Rodriguez, J.J.; Pitstick, R.; Wegmann, S.; Garcia-Alloza, M.; Carlson, G.A.; Hyman, B.T.; Spires-Jones, T.L. Human tau increases amyloid β plaque size but not amyloid β-mediated synapse loss in a novel mouse model of Alzheimer’s disease. Eur. J. Neurosci., 2016, 44(12), 3056-3066.
[http://dx.doi.org/10.1111/ejn.13442] [PMID: 27748574]
[157]
Merino-Serrais, P.; Benavides-Piccione, R.; Blazquez-Llorca, L.; Kastanauskaite, A.; Rábano, A.; Avila, J.; DeFelipe, J. The influence of phospho-τ on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease. Brain, 2013, 136(Pt 6), 1913-1928.
[http://dx.doi.org/10.1093/brain/awt088] [PMID: 23715095]
[158]
Fein, J.A.; Sokolow, S.; Miller, C.A.; Vinters, H.V.; Yang, F.; Cole, G.M.; Gylys, K.H. Co-localization of amyloid beta and tau pathology in Alzheimer’s disease synaptosomes. Am. J. Pathol., 2008, 172(6), 1683-1692.
[http://dx.doi.org/10.2353/ajpath.2008.070829] [PMID: 18467692]
[159]
Hoover, B.R.; Reed, M.N.; Su, J.; Penrod, R.D.; Kotilinek, L.A.; Grant, M.K.; Pitstick, R.; Carlson, G.A.; Lanier, L.M.; Yuan, L.L.; Ashe, K.H.; Liao, D. Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron, 2010, 68(6), 1067-1081.
[http://dx.doi.org/10.1016/j.neuron.2010.11.030] [PMID: 21172610]
[160]
Takahashi, R.H.; Capetillo-Zarate, E.; Lin, M.T.; Milner, T.A.; Gouras, G.K. Co-occurrence of Alzheimer’s disease ß-amyloid and τ pathologies at synapses. Neurobiol. Aging, 2010, 31(7), 1145-1152.
[http://dx.doi.org/10.1016/j.neurobiolaging.2008.07.021] [PMID: 18771816]
[161]
Ittner, L.M.; Ke, Y.D.; Delerue, F.; Bi, M.; Gladbach, A.; van Eersel, J.; Wölfing, H.; Chieng, B.C.; Christie, M.J.; Napier, I.A.; Eckert, A.; Staufenbiel, M.; Hardeman, E.; Götz, J. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer’s disease mouse models. Cell, 2010, 142(3), 387-397.
[http://dx.doi.org/10.1016/j.cell.2010.06.036] [PMID: 20655099]
[162]
Lasagna-Reeves, C.A.; Castillo-Carranza, D.L.; Sengupta, U.; Clos, A.L.; Jackson, G.R.; Kayed, R. Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice. Mol. Neurodegener., 2011, 6, 39.
[http://dx.doi.org/10.1186/1750-1326-6-39] [PMID: 21645391]
[163]
Shipton, O.A.; Leitz, J.R.; Dworzak, J.; Acton, C.E.; Tunbridge, E.M.; Denk, F.; Dawson, H.N.; Vitek, M.P.; Wade-Martins, R.; Paulsen, O.; Vargas-Caballero, M. Tau protein is required for amyloid beta-induced impairment of hippocampal long-term potentiation. J. Neurosci., 2011, 31(5), 1688-1692.
[http://dx.doi.org/10.1523/JNEUROSCI.2610-10.2011] [PMID: 21289177]
[164]
Roberson, E.D.; Scearce-Levie, K.; Palop, J.J.; Yan, F.; Cheng, I.H.; Wu, T.; Gerstein, H.; Yu, G.Q.; Mucke, L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer’s disease mouse model. Science, 2007, 316(5825), 750-754.
[http://dx.doi.org/10.1126/science.1141736] [PMID: 17478722]
[165]
Gatz, M.; Reynolds, C.A.; Fratiglioni, L.; Johansson, B.; Mortimer, J.A.; Berg, S.; Fiske, A.; Pedersen, N.L. Role of genes and environments for explaining Alzheimer disease. Arch. Gen. Psychiatry, 2006, 63(2), 168-174.
[http://dx.doi.org/10.1001/archpsyc.63.2.168] [PMID: 16461860]
[166]
Emahazion, T.; Feuk, L.; Jobs, M.; Sawyer, S.L.; Fredman, D.; St Clair, D.; Prince, J.A.; Brookes, A.J. SNP association studies in Alzheimer’s disease highlight problems for complex disease analysis. Trends Genet., 2001, 17(7), 407-413.
[http://dx.doi.org/10.1016/S0168-9525(01)02342-3] [PMID: 11418222]
[167]
Zhu, X.C.; Tan, L.; Wang, H.F.; Jiang, T.; Cao, L.; Wang, C.; Wang, J.; Tan, C.C.; Meng, X.F.; Yu, J.T. Rate of early onset Alzheimer’s disease: a systematic review and meta-analysis. Ann. Transl. Med., 2015, 3(3), 38.
[PMID: 25815299]
[168]
Goate, A.; Chartier-Harlin, M.C.; Mullan, M.; Brown, J.; Crawford, F.; Fidani, L.; Giuffra, L.; Haynes, A.; Irving, N.; James, L. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer’s disease. Nature, 1991, 349(6311), 704-706.
[http://dx.doi.org/10.1038/349704a0] [PMID: 1671712]
[169]
Jarrett, J.T.; Berger, E.P.; Lansbury, P.T., Jr The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer’s disease. Biochemistry, 1993, 32(18), 4693-4697.
[http://dx.doi.org/10.1021/bi00069a001] [PMID: 8490014]
[170]
Jarrett, J.T.; Berger, E.P.; Lansbury, P.T., Jr The C-terminus of the beta protein is critical in amyloidogenesis. Ann. N. Y. Acad. Sci., 1993, 695, 144-148.
[http://dx.doi.org/10.1111/j.1749-6632.1993.tb23043.x] [PMID: 8239273]
[171]
Suzuki, N.; Cheung, T.T.; Cai, X.D.; Odaka, A.; Otvos, L., Jr; Eckman, C.; Golde, T.E.; Younkin, S.G. An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. Science, 1994, 264(5163), 1336-1340.
[http://dx.doi.org/10.1126/science.8191290] [PMID: 8191290]
[172]
Roher, A.E.; Lowenson, J.D.; Clarke, S.; Woods, A.S.; Cotter, R.J.; Gowing, E.; Ball, M.J. beta-Amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease. Proc. Natl. Acad. Sci. USA, 1993, 90(22), 10836-10840.
[http://dx.doi.org/10.1073/pnas.90.22.10836] [PMID: 8248178]
[173]
van Duijn, C.M.; de Knijff, P.; Cruts, M.; Wehnert, A.; Havekes, L.M.; Hofman, A.; Van Broeckhoven, C. Apolipoprotein E4 allele in a population-based study of early-onset Alzheimer’s disease. Nat. Genet., 1994, 7(1), 74-78.
[http://dx.doi.org/10.1038/ng0594-74] [PMID: 8075646]
[174]
Strittmatter, W.J.; Weisgraber, K.H.; Huang, D.Y.; Dong, L.M.; Salvesen, G.S.; Pericak-Vance, M.; Schmechel, D.; Saunders, A.M.; Goldgaber, D.; Roses, A.D. Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc. Natl. Acad. Sci. USA, 1993, 90(17), 8098-8102.
[http://dx.doi.org/10.1073/pnas.90.17.8098] [PMID: 8367470]
[175]
Strittmatter, W.J.; Saunders, A.M.; Schmechel, D.; Pericak-Vance, M.; Enghild, J.; Salvesen, G.S.; Roses, A.D.; Apolipoprotein, E. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. USA, 1993, 90(5), 1977-1981.
[http://dx.doi.org/10.1073/pnas.90.5.1977] [PMID: 8446617]
[176]
Chartier-Harlin, M.C.; Parfitt, M.; Legrain, S.; Pérez-Tur, J.; Brousseau, T.; Evans, A.; Berr, C.; Vidal, O.; Roques, P.; Gourlet, V. Apolipoprotein E, epsilon 4 allele as a major risk factor for sporadic early and late-onset forms of Alzheimer’s disease: analysis of the 19q13.2 chromosomal region. Hum. Mol. Genet., 1994, 3(4), 569-574.
[http://dx.doi.org/10.1093/hmg/3.4.569] [PMID: 8069300]
[177]
Talbot, C.; Lendon, C.; Craddock, N.; Shears, S.; Morris, J.C.; Goate, A. Protection against Alzheimer’s disease with apoE epsilon 2. Lancet, 1994, 343(8910), 1432-1433.
[http://dx.doi.org/10.1016/S0140-6736(94)92557-7] [PMID: 7910910]
[178]
Corder, E.H.; Saunders, A.M.; Strittmatter, W.J.; Schmechel, D.E.; Gaskell, P.C.; Small, G.W.; Roses, A.D.; Haines, J.L.; Pericak-Vance, M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science, 1993, 261(5123), 921-923.
[http://dx.doi.org/10.1126/science.8346443] [PMID: 8346443]
[179]
Huang, Y.A.; Zhou, B.; Wernig, M.; Sudhof, T.C. ApoE2, ApoE3, and ApoE4 Differentially Stimulate APP Transcription and Abeta Secretion. Cell, 168(3), 427-441.
[180]
Hashimoto, T.; Serrano-Pozo, A.; Hori, Y.; Adams, K.W.; Takeda, S.; Banerji, A.O.; Mitani, A.; Joyner, D.; Thyssen, D.H.; Bacskai, B.J.; Frosch, M.P.; Spires-Jones, T.L.; Finn, M.B.; Holtzman, D.M.; Hyman, B.T.; Apolipoprotein, E. Apolipoprotein E, especially apolipoprotein E4, increases the oligomerization of amyloid β peptide. J. Neurosci., 2012, 32(43), 15181-15192.
[http://dx.doi.org/10.1523/JNEUROSCI.1542-12.2012] [PMID: 23100439]
[181]
Dumanis, S.B.; Tesoriero, J.A.; Babus, L.W.; Nguyen, M.T.; Trotter, J.H.; Ladu, M.J.; Weeber, E.J.; Turner, R.S.; Xu, B.; Rebeck, G.W.; Hoe, H.S. ApoE4 decreases spine density and dendritic complexity in cortical neurons in vivo. J. Neurosci., 2009, 29(48), 15317-15322.
[http://dx.doi.org/10.1523/JNEUROSCI.4026-09.2009] [PMID: 19955384]
[182]
Klein, R.C.; Mace, B.E.; Moore, S.D.; Sullivan, P.M. Progressive loss of synaptic integrity in human apolipoprotein E4 targeted replacement mice and attenuation by apolipoprotein E2. Neuroscience, 2010, 171(4), 1265-1272.
[http://dx.doi.org/10.1016/j.neuroscience.2010.10.027] [PMID: 20951774]
[183]
Nwabuisi-Heath, E.; Rebeck, G.W.; Ladu, M.J.; Yu, C. ApoE4 delays dendritic spine formation during neuron development and accelerates loss of mature spines in vitro. ASN Neuro, 2014, 6(1)e00134
[PMID: 24328732]
[184]
Zhu, Y.; Nwabuisi-Heath, E.; Dumanis, S.B.; Tai, L.M.; Yu, C.; Rebeck, G.W.; LaDu, M.J. APOE genotype alters glial activation and loss of synaptic markers in mice. Glia, 2012, 60(4), 559-569.
[http://dx.doi.org/10.1002/glia.22289] [PMID: 22228589]
[185]
Andrews-Zwilling, Y.; Bien-Ly, N.; Xu, Q.; Li, G.; Bernardo, A.; Yoon, S.Y.; Zwilling, D.; Yan, T.X.; Chen, L.; Huang, Y. Apolipoprotein E4 causes age- and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J. Neurosci., 2010, 30(41), 13707-13717.
[186]
Koffie, R.M.; Hashimoto, T.; Tai, H.C.; Kay, K.R.; Serrano-Pozo, A.; Joyner, D.; Hou, S.; Kopeikina, K.J.; Frosch, M.P.; Lee, V.M.; Holtzman, D.M.; Hyman, B.T.; Spires-Jones, T.L. Apolipoprotein E4 effects in Alzheimer’s disease are mediated by synaptotoxic oligomeric amyloid-β. Brain, 2012, 135(Pt 7), 2155-2168.
[http://dx.doi.org/10.1093/brain/aws127] [PMID: 22637583]
[187]
Lin, Y.T.; Seo, J.; Gao, F.; Feldman, H.M.; Wen, H.L.; Pen-ney, J.; Cam, H.P.; Gjoneska, E.; Raja, W.K.; Cheng, J.; Rueda, R.; Kritskiy, O.; Abdurrob, F.; Peng, Z.; Milo, B.; Yu, C.J.; Elmsaouri, S.; Dey, D.; Ko, T.; Yankner, B.A.; Tsai, L.H. APOE4 Causes Widespread Molecular and Cellular Altera-tions Associated with Alzheimer’s Disease Phenotypes in Human iPSC-Derived Brain Cell Types. Neuron, 2018, 98(6), 1141-1154.
[188]
Chung, W.S.; Verghese, P.B.; Chakraborty, C.; Joung, J.; Hyman, B.T.; Ulrich, J.D.; Holtzman, D.M.; Barres, B.A. Novel allele-dependent role for APOE in controlling the rate of synapse pruning by astrocytes. Proc. Natl. Acad. Sci. USA, 2016, 113(36), 10186-10191.
[http://dx.doi.org/10.1073/pnas.1609896113] [PMID: 27559087]
[189]
Egensperger, R.; Kösel, S.; von Eitzen, U.; Graeber, M.B. Microglial activation in Alzheimer disease: Association with APOE genotype. Brain Pathol., 1998, 8(3), 439-447.
[http://dx.doi.org/10.1111/j.1750-3639.1998.tb00166.x] [PMID: 9669695]
[190]
Currais, A.; Quehenberger, O.A. M. A.; Daugherty, D.; Ma-her, P.; Schubert, D. Amyloid proteotoxicity initiates an in-flammatory response blocked by cannabinoids. NPJ Aging Mech. Dis., 2016, 2, 16012.
[http://dx.doi.org/10.1038/npjamd.2016.12] [PMID: 28721267]
[191]
Bornemann, K.D.; Wiederhold, K.H.; Pauli, C.; Ermini, F.; Stalder, M.; Schnell, L.; Sommer, B.; Jucker, M.; Staufenbiel, M. Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am. J. Pathol., 2001, 158(1), 63-73.
[http://dx.doi.org/10.1016/S0002-9440(10)63945-4] [PMID: 11141480]
[192]
Lue, L.F.; Brachova, L.; Civin, W.H. Rogers, J. Inflammation, A beta deposition, and neurofibrillary tangle formation as correlates of Alzheimer’s disease neurodegeneration. J. Neuropathol. Exp. Neurol., 1996, 55(10), 1083-1088.
[http://dx.doi.org/10.1097/00005072-199655100-00008] [PMID: 8858005]
[193]
Yang, L.B.; Li, R.; Meri, S.; Rogers, J.; Shen, Y. Deficiency of complement defense protein CD59 may contribute to neurodegeneration in Alzheimer’s disease. J. Neurosci., 2000, 20(20), 7505-7509.
[http://dx.doi.org/10.1523/JNEUROSCI.20-20-07505.2000] [PMID: 11027207]
[194]
Reichwald, J.; Danner, S.; Wiederhold, K.H.; Staufenbiel, M. Expression of complement system components during aging and amyloid deposition in APP transgenic mice. J. Neuroinflammation, 2009, 6, 35.
[http://dx.doi.org/10.1186/1742-2094-6-35] [PMID: 19917141]
[195]
Fonseca, M.I.; Zhou, J.; Botto, M.; Tenner, A.J. Absence of C1q leads to less neuropathology in transgenic mouse models of Alzheimer’s disease. J. Neurosci., 2004, 24(29), 6457-6465.
[http://dx.doi.org/10.1523/JNEUROSCI.0901-04.2004] [PMID: 15269255]
[196]
Shi, Q.; Chowdhury, S.; Ma, R.; Le, K.X.; Hong, S.; Caldarone, B.J.; Stevens, B.; Lemere, C.A. Complement C3 deficiency protects against neurodegeneration in aged plaque-rich APP/PS1 mice. Sci. Transl. Med., 2017, 9(392)eaaf6295
[http://dx.doi.org/10.1126/scitranslmed.aaf6295] [PMID: 28566429]
[197]
Shen, Y.; Meri, S. Yin and Yang: complement activation and regulation in Alzheimer’s disease. Prog. Neurobiol., 2003, 70(6), 463-472.
[http://dx.doi.org/10.1016/j.pneurobio.2003.08.001] [PMID: 14568360]
[198]
Hong, S.; Beja-Glasser, V.F.; Nfonoyim, B.M.; Frouin, A.; Li, S.; Ramakrishnan, S.; Merry, K.M.; Shi, Q.; Rosenthal, A.; Barres, B.A.; Lemere, C.A.; Selkoe, D.J.; Stevens, B. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science, 2016, 352(6286), 712-716.
[http://dx.doi.org/10.1126/science.aad8373] [PMID: 27033548]
[199]
Dejanovic, B.; Huntley, M.A.; De Maziere, A.; Meilandt, W.J.; Wu, T.; Srinivasan, K.; Jiang, Z.; Gandham, V.; Friedman, B.A.; Ngu, H.; Foreman, O.; Carano, R.A.D.; Chih, B.; Klumperman, J.; Bakalarski, C.; Hanson, J.E.; Sheng, M. Changes in the Synaptic Proteome in Tauopathy and Rescue of Tau-Induced Synapse Loss by C1q Antibodies. Neuron, 2018, 100(6), 1322-1336.
[http://dx.doi.org/10.1016/j.neuron.2018.10.014]
[200]
Savas, J.N.; Wang, Y.Z.; DeNardo, L.A.; Martinez-Bartolome, S.; McClatchy, D.B.; Hark, T.J.; Shanks, N.F.; Cozzolino, K.A.; Lavallée-Adam, M.; Smukowski, S.N.; Park, S.K.; Kelly, J.W.; Koo, E.H.; Nakagawa, T.; Masliah, E.; Ghosh, A.; Yates, J.R. III Amyloid Accumulation Drives Proteome-wide Alterations in Mouse Models of Alzheimer’s Disease-like Pathology. Cell Rep., 2017, 21(9), 2614-2627.
[http://dx.doi.org/10.1016/j.celrep.2017.11.009] [PMID: 29186695]
[201]
Seyfried, N.T.; Dammer, E.B.; Swarup, V.; Nandakumar, D.; Duong, D.M.; Yin, L.; Deng, Q.; Nguyen, T.; Hales, C.M.; Wingo, T.; Glass, J.; Gearing, M.; Thambisetty, M.; Troncoso, J.C.; Geschwind, D.H.; Lah, J.J.; Levey, A.I. A Multi-network Approach Identifies Protein-Specific Co-expression in Asymptomatic and Symptomatic Alzheimer’s Disease. Cell Syst., 2017, 4(1), 60-72.
[http://dx.doi.org/10.1016/j.cels.2016.11.006]
[202]
Litvinchuk, A.; Wan, Y.W.; Swartzlander, D.B.; Chen, F.; Cole, A.; Propson, N.E.; Wang, Q.; Zhang, B.; Liu, Z.; Zheng, H. Complement C3aR Inactivation Attenuates Tau Pathology and Reverses an Immune Network Deregulated in Tauopathy Models and Alzheimer’s Disease. Neuron, 2018, 100(6), 1337-1353.
[http://dx.doi.org/10.1016/j.neuron.2018.10.031]
[203]
Shen, Y.; Yang, L.; Li, R. What does complement do in Alzheimer’s disease? Old molecules with new insights. Transl. Neurodegener., 2013, 2(1), 21.
[http://dx.doi.org/10.1186/2047-9158-2-21] [PMID: 24119446]
[204]
Keren-Shaul, H.; Spinrad, A.; Weiner, A.; Matcovitch-Natan, O.; Dvir-Szternfeld, R.; Ulland, T.K.; David, E.; Baruch, K.; Lara-Astaiso, D.; Toth, B.; Itzkovitz, S.; Colonna, M.; Schwartz, M.; Amit, I. A Unique Microglia Type Associated with Restricting Development of Alzheimer’s Disease. Cell, 2017, 169(7), 1276-1290.
[http://dx.doi.org/10.1016/j.cell.2017.05.018]
[205]
Liddelow, S.A.; Guttenplan, K.A.; Clarke, L.E.; Bennett, F.C.; Bohlen, C.J.; Schirmer, L.; Bennett, M.L.; Münch, A.E.; Chung, W.S.; Peterson, T.C.; Wilton, D.K.; Frouin, A.; Napier, B.A.; Panicker, N.; Kumar, M.; Buckwalter, M.S.; Rowitch, D.H.; Dawson, V.L.; Dawson, T.M.; Stevens, B.; Barres, B.A. Neurotoxic reactive astrocytes are induced by activated microglia. Nature, 2017, 541(7638), 481-487.
[http://dx.doi.org/10.1038/nature21029] [PMID: 28099414]
[206]
Fonseca, M.I.; Chu, S.H.; Hernandez, M.X.; Fang, M.J.; Modarresi, L.; Selvan, P.; MacGregor, G.R.; Tenner, A.J. Cell-specific deletion of C1qa identifies microglia as the dominant source of C1q in mouse brain. J. Neuroinflammation, 2017, 14(1), 48.
[http://dx.doi.org/10.1186/s12974-017-0814-9] [PMID: 28264694]
[207]
Bie, B.; Wu, J.; Foss, J.F.; Naguib, M. Activation of mGluR1 mediates C1q-dependent microglial phagocytosis of glutamatergic synapses in Alzheimer’s Rodent models. Mol. Neurobiol., 2019, 56(8), 5568-5585.
[http://dx.doi.org/10.1007/s12035-019-1467-8] [PMID: 30652266]
[208]
Louneva, N.; Cohen, J.W.; Han, L.Y.; Talbot, K.; Wilson, R.S.; Bennett, D.A.; Trojanowski, J.Q.; Arnold, S.E. Caspase-3 is enriched in postsynaptic densities and increased in Alzheimer’s disease. Am. J. Pathol., 2008, 173(5), 1488-1495.
[http://dx.doi.org/10.2353/ajpath.2008.080434] [PMID: 18818379]
[209]
D’Amelio, M.; Cavallucci, V.; Middei, S.; Marchetti, C.; Pacioni, S.; Ferri, A.; Diamantini, A.; De Zio, D.; Carrara, P.; Battistini, L.; Moreno, S.; Bacci, A.; Ammassari-Teule, M.; Marie, H.; Cecconi, F. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer’s disease. Nat. Neurosci., 2011, 14(1), 69-76.
[http://dx.doi.org/10.1038/nn.2709] [PMID: 21151119]
[210]
Kim, T.; Vidal, G.S.; Djurisic, M.; William, C.M.; Birnbaum, M.E.; Garcia, K.C.; Hyman, B.T.; Shatz, C.J. Human LilrB2 is a β-amyloid receptor and its murine homolog PirB regulates synaptic plasticity in an Alzheimer’s model. Science, 2013, 341(6152), 1399-1404.
[http://dx.doi.org/10.1126/science.1242077] [PMID: 24052308]
[211]
Chapuis, J.; Hot, D.; Hansmannel, F.; Kerdraon, O.; Ferreira, S.; Hubans, C.; Maurage, C.A.; Huot, L.; Bensemain, F.; Laumet, G.; Ayral, A.M.; Fievet, N.; Hauw, J.J.; DeKosky, S.T.; Lemoine, Y.; Iwatsubo, T.; Wavrant-Devrièze, F.; Dartigues, J.F.; Tzourio, C.; Buée, L.; Pasquier, F.; Berr, C.; Mann, D.; Lendon, C.; Alpérovitch, A.; Kamboh, M.I.; Amouyel, P.; Lambert, J.C. Transcriptomic and genetic studies identify IL-33 as a candidate gene for Alzheimer’s disease. Mol. Psychiatry, 2009, 14(11), 1004-1016.
[http://dx.doi.org/10.1038/mp.2009.10] [PMID: 19204726]
[212]
Fu, A.K.; Hung, K.W.; Yuen, M.Y.; Zhou, X.; Mak, D.S.; Chan, I.C.; Cheung, T.H.; Zhang, B.; Fu, W.Y.; Liew, F.Y.; Ip, N.Y. IL-33 ameliorates Alzheimer’s disease-like pathology and cognitive decline. Proc. Natl. Acad. Sci. USA, 2016, 113(19), E2705-E2713.
[http://dx.doi.org/10.1073/pnas.1604032113] [PMID: 27091974]
[213]
Ma, Q.L.; Teng, E.; Zuo, X.; Jones, M.; Teter, B.; Zhao, E.Y.; Zhu, C.; Bilousova, T.; Gylys, K.H.; Apostolova, L.G.; LaDu, M.J.; Hossain, M.A.; Frautschy, S.A.; Cole, G.M. Neuronal pentraxin 1: A synaptic-derived plasma biomarker in Alzheimer’s disease. Neurobiol. Dis., 2018, 114, 120-128.
[http://dx.doi.org/10.1016/j.nbd.2018.02.014] [PMID: 29501530]
[214]
Abad, M.A.; Enguita, M.; DeGregorio-Rocasolano, N.; Ferrer, I.; Trullas, R. Neuronal pentraxin 1 contributes to the neuronal damage evoked by amyloid-beta and is overexpressed in dystrophic neurites in Alzheimer’s brain. J. Neurosci., 2006, 26(49), 12735-12747.
[http://dx.doi.org/10.1523/JNEUROSCI.0575-06.2006] [PMID: 17151277]
[215]
Suarez-Calvet, M.; Capell, A.; Araque Caballero, M.A.; Morenas-Rodriguez, E.; Fellerer, K.; Franzmeier, N.; Klein-berger, G.; Eren, E.; Deming, Y.; Piccio, L.; Karch, C.M.; Cruchaga, C.; Paumier, K.; Bateman, R.J.; Fagan, A.M.; Mor-ris, J.C.; Levin, J.; Danek, A.; Jucker, M.; Masters, C.L.; Rossor, M.N.; Ringman, J.M.; Shaw, L.M.; Trojanowski, J.Q.; Weiner, M.; Ewers, M.; Haass, C.; Dominantly Inherited Alzheimer, N. Alzheimer’s Disease Neuroimaging, I., CSF progranulin increases in the course of Alzheimer’s disease and is associated with sTREM2, neurodegeneration and cog-nitive decline. EMBO Mol. Med., 2018, 10(12)
[http://dx.doi.org/10.15252/emmm.201809712] [PMID: 30482868]
[216]
Cooper, Y.A.; Nachun, D.; Dokuru, D.; Yang, Z.; Karydas, A.M.; Serrero, G.; Yue, B. Alzheimer’s Disease Neuroimag-ing, I.; Boxer, A. L.; Miller, B. L.; Coppola, G., Progranulin levels in blood in Alzheimer’s disease and mild cognitive im-pairment. Ann. Clin. Transl. Neurol., 2018, 5(5), 616-629.
[http://dx.doi.org/10.1002/acn3.560] [PMID: 29761124]
[217]
Minami, S.S.; Min, S.W.; Krabbe, G.; Wang, C.; Zhou, Y.; Asgarov, R.; Li, Y.; Martens, L.H.; Elia, L.P.; Ward, M.E.; Mucke, L.; Farese, R.V., Jr; Gan, L. Progranulin protects against amyloid β deposition and toxicity in Alzheimer’s disease mouse models. Nat. Med., 2014, 20(10), 1157-1164.
[http://dx.doi.org/10.1038/nm.3672] [PMID: 25261995]
[218]
Takahashi, H.; Klein, Z.A.; Bhagat, S.M.; Kaufman, A.C.; Kostylev, M.A.; Ikezu, T.; Strittmatter, S.M. Alzheimer’s Disease Neuroimaging, I. Opposing effects of progranulin de-ficiency on amyloid and tau pathologies via microglial TYROBP network. Acta Neuropathol., 2017, 133(5), 785-807.
[http://dx.doi.org/10.1007/s00401-017-1668-z] [PMID: 28070672]
[219]
Perea, J.R.; Lleó, A.; Alcolea, D.; Fortea, J.; Ávila, J.; Bolós, M. Decreased CX3CL1 levels in the Cerebrospinal fluid of patients With Alzheimer’s Disease. Front. Neurosci., 2018, 12, 609.
[http://dx.doi.org/10.3389/fnins.2018.00609] [PMID: 30245615]
[220]
Cho, S.H.; Sun, B.; Zhou, Y.; Kauppinen, T.M.; Halabisky, B.; Wes, P.; Ransohoff, R.M.; Gan, L. CX3CR1 protein signaling modulates microglial activation and protects against plaque-independent cognitive deficits in a mouse model of Alzheimer disease. J. Biol. Chem., 2011, 286(37), 32713-32722.
[http://dx.doi.org/10.1074/jbc.M111.254268] [PMID: 21771791]
[221]
Lee, S.; Xu, G.; Jay, T.R.; Bhatta, S.; Kim, K.W.; Jung, S.; Landreth, G.E.; Ransohoff, R.M.; Lamb, B.T. Opposing effects of membrane-anchored CX3CL1 on amyloid and tau pathologies via the p38 MAPK pathway. J. Neurosci., 2014, 34(37), 12538-12546.
[http://dx.doi.org/10.1523/JNEUROSCI.0853-14.2014] [PMID: 25209291]
[222]
Lee, S.; Varvel, N.H.; Konerth, M.E.; Xu, G.; Cardona, A.E.; Ransohoff, R.M.; Lamb, B.T. CX3CR1 deficiency alters microglial activation and reduces beta-amyloid deposition in two Alzheimer’s disease mouse models. Am. J. Pathol., 2010, 177(5), 2549-2562.
[http://dx.doi.org/10.2353/ajpath.2010.100265] [PMID: 20864679]
[223]
Park, D.; Na, M.; Kim, J.A.; Lee, U.; Cho, E.; Jang, M.; Chang, S. Activation of CaMKIV by soluble amyloid-β1-42 impedes trafficking of axonal vesicles and impairs activity-dependent synaptogenesis. Sci. Signal., 2017, 10(487)eaam8661
[PMID: 28698220]
[224]
Levi, O.; Jongen-Relo, A.L.; Feldon, J.; Roses, A.D.; Michaelson, D.M. ApoE4 impairs hippocampal plasticity isoform-specifically and blocks the environmental stimulation of synaptogenesis and memory. Neurobiol. Dis., 2003, 13(3), 273-282.
[http://dx.doi.org/10.1016/S0969-9961(03)00045-7] [PMID: 12901842]
[225]
Van Kampen, J.M.; Kay, D.G. Progranulin gene delivery reduces plaque burden and synaptic atrophy in a mouse model of Alzheimer’s disease. PLoS One, 2017, 12(8)e0182896
[http://dx.doi.org/10.1371/journal.pone.0182896] [PMID: 28837568]
[226]
Chen, Y.; Wang, B.; Liu, D.; Li, J.J.; Xue, Y.; Sakata, K.; Zhu, L.Q.; Heldt, S.A.; Xu, H.; Liao, F.F. Hsp90 chaperone inhibitor 17-AAG attenuates Abeta-induced synaptic toxicity and memory impairment. J. Neurosci., 2014, 34(7), 2464-2470.
[227]
Wang, R.; Zhang, Y.; Li, J.; Zhang, C. Resveratrol ameliorates spatial learning memory impairment induced by Aβ1-42 in rats. Neuroscience, 2017, 344, 39-47.
[http://dx.doi.org/10.1016/j.neuroscience.2016.08.051] [PMID: 27600946]
[228]
Kodali, M.; Parihar, V.K.; Hattiangady, B.; Mishra, V.; Shuai, B.; Shetty, A.K. Resveratrol prevents age-related memory and mood dysfunction with increased hippocampal neurogenesis and microvasculature, and reduced glial activation. Sci. Rep., 2015, 5, 8075.
[http://dx.doi.org/10.1038/srep08075] [PMID: 25627672]
[229]
Zhao, H.; Wang, Q.; Cheng, X.; Li, X.; Li, N.; Liu, T.; Li, J.; Yang, Q.; Dong, R.; Zhang, Y.; Zhang, L. Inhibitive Effect of Resveratrol on the Inflammation in Cultured Astrocytes and Microglia Induced by Aβ1-42. Neuroscience, 2018, 379, 390-404.
[http://dx.doi.org/10.1016/j.neuroscience.2018.03.047] [PMID: 29627302]
[230]
Craft, S.; Baker, L.D.; Montine, T.J.; Minoshima, S.; Watson, G.S.; Claxton, A.; Arbuckle, M.; Callaghan, M.; Tsai, E.; Plymate, S.R.; Green, P.S.; Leverenz, J.; Cross, D.; Gerton, B. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch. Neurol., 2012, 69(1), 29-38.
[http://dx.doi.org/10.1001/archneurol.2011.233] [PMID: 21911655]
[231]
De Felice, F.G.; Vieira, M.N.; Bomfim, T.R.; Decker, H.; Velasco, P.T.; Lambert, M.P.; Viola, K.L.; Zhao, W.Q.; Ferreira, S.T.; Klein, W.L. Protection of synapses against Alzheimer’s-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc. Natl. Acad. Sci. USA, 2009, 106(6), 1971-1976.
[http://dx.doi.org/10.1073/pnas.0809158106] [PMID: 19188609]
[232]
Thompson, A.J.; Baranzini, S.E.; Geurts, J.; Hemmer, B.; Ciccarelli, O. Multiple sclerosis. Lancet, 2018, 391(10130), 1622-1636.
[http://dx.doi.org/10.1016/S0140-6736(18)30481-1] [PMID: 29576504]
[233]
Reich, D.S.; Lucchinetti, C.F.; Calabresi, P.A. Multiple Sclerosis. N. Engl. J. Med., 2018, 378(2), 169-180.
[http://dx.doi.org/10.1056/NEJMra1401483] [PMID: 29320652]
[234]
Di Filippo, M.; de Iure, A.; Durante, V.; Gaetani, L.; Mancini, A.; Sarchielli, P.; Calabresi, P. Synaptic plasticity and experimental autoimmune encephalomyelitis: implications for multiple sclerosis. Brain Res., 2015, 1621, 205-213.
[http://dx.doi.org/10.1016/j.brainres.2014.12.004] [PMID: 25498984]
[235]
Mandolesi, G.; Gentile, A.; Musella, A.; Fresegna, D.; De Vito, F.; Bullitta, S.; Sepman, H.; Marfia, G.A.; Centonze, D. Synaptopathy connects inflammation and neurodegeneration in multiple sclerosis. Nat. Rev. Neurol., 2015, 11(12), 711-724.
[http://dx.doi.org/10.1038/nrneurol.2015.222] [PMID: 26585978]
[236]
Ruano, L.; Portaccio, E.; Goretti, B.; Niccolai, C.; Severo, M.; Patti, F.; Cilia, S.; Gallo, P.; Grossi, P.; Ghezzi, A.; Roscio, M.; Mattioli, F.; Stampatori, C.; Trojano, M.; Viterbo, R.G.; Amato, M.P. Age and disability drive cognitive impairment in multiple sclerosis across disease subtypes. Mult. Scler., 2017, 23(9), 1258-1267.
[http://dx.doi.org/10.1177/1352458516674367] [PMID: 27738090]
[237]
Achiron, A.; Polliack, M.; Rao, S.M.; Barak, Y.; Lavie, M.; Appelboim, N.; Harel, Y. Cognitive patterns and progression in multiple sclerosis: construction and validation of percentile curves. J. Neurol. Neurosurg. Psychiatry, 2005, 76(5), 744-749.
[http://dx.doi.org/10.1136/jnnp.2004.045518] [PMID: 15834042]
[238]
Centonze, D.; Muzio, L.; Rossi, S.; Cavasinni, F.; De Chiara, V.; Bergami, A.; Musella, A.; D’Amelio, M.; Cavallucci, V.; Martorana, A.; Bergamaschi, A.; Cencioni, M.T.; Diamantini, A.; Butti, E.; Comi, G.; Bernardi, G.; Cecconi, F.; Battistini, L.; Furlan, R.; Martino, G. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J. Neurosci., 2009, 29(11), 3442-3452.
[http://dx.doi.org/10.1523/JNEUROSCI.5804-08.2009] [PMID: 19295150]
[239]
Rossi, S.; Motta, C.; Studer, V.; Barbieri, F.; Buttari, F.; Bergami, A.; Sancesario, G.; Bernardini, S.; De Angelis, G.; Martino, G.; Furlan, R.; Centonze, D. Tumor necrosis factor is elevated in progressive multiple sclerosis and causes excitotoxic neurodegeneration. Mult. Scler., 2014, 20(3), 304-312.
[http://dx.doi.org/10.1177/1352458513498128] [PMID: 23886826]
[240]
Kim, D.Y.; Hao, J.; Liu, R.; Turner, G.; Shi, F.D.; Rho, J.M. Inflammation-mediated memory dysfunction and effects of a ketogenic diet in a murine model of multiple sclerosis. PLoS One, 2012, 7(5)e35476
[http://dx.doi.org/10.1371/journal.pone.0035476] [PMID: 22567104]
[241]
DeLuca, G.C.; Yates, R.L.; Beale, H.; Morrow, S.A. Cognitive impairment in multiple sclerosis: clinical, radiologic and pathologic insights. Brain Pathol., 2015, 25(1), 79-98.
[http://dx.doi.org/10.1111/bpa.12220] [PMID: 25521179]
[242]
Pitt, D.; Werner, P.; Raine, C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med., 2000, 6(1), 67-70.
[http://dx.doi.org/10.1038/71555] [PMID: 10613826]
[243]
Calabrese, M.; Agosta, F.; Rinaldi, F.; Mattisi, I.; Grossi, P.; Favaretto, A.; Atzori, M.; Bernardi, V.; Barachino, L.; Rinaldi, L.; Perini, P.; Gallo, P.; Filippi, M. Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. Arch. Neurol., 2009, 66(9), 1144-1150.
[http://dx.doi.org/10.1001/archneurol.2009.174] [PMID: 19752305]
[244]
Batista, S.; Zivadinov, R.; Hoogs, M.; Bergsland, N.; Heininen-Brown, M.; Dwyer, M.G.; Weinstock-Guttman, B.; Benedict, R.H. Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J. Neurol., 2012, 259(1), 139-146.
[http://dx.doi.org/10.1007/s00415-011-6147-1] [PMID: 21720932]
[245]
Bergsland, N.; Zivadinov, R.; Dwyer, M.G.; Weinstock-Guttman, B.; Benedict, R.H. Localized atrophy of the thalamus and slowed cognitive processing speed in MS patients. Mult. Scler., 2016, 22(10), 1327-1336.
[http://dx.doi.org/10.1177/1352458515616204] [PMID: 26541795]
[246]
Steenwijk, M.D.; Geurts, J.J.; Daams, M.; Tijms, B.M.; Wink, A.M.; Balk, L.J.; Tewarie, P.K.; Uitdehaag, B.M.; Barkhof, F.; Vrenken, H.; Pouwels, P.J. Cortical atrophy patterns in multiple sclerosis are non-random and clinically relevant. Brain, 2016, 139(Pt 1), 115-126.
[http://dx.doi.org/10.1093/brain/awv337] [PMID: 26637488]
[247]
Cocozza, S.; Petracca, M.; Mormina, E.; Buyukturkoglu, K.; Podranski, K.; Heinig, M.M.; Pontillo, G.; Russo, C.; Tedeschi, E.; Russo, C.V.; Costabile, T.; Lanzillo, R.; Harel, A.; Klineova, S.; Miller, A.; Brunetti, A.; Morra, V.B.; Lublin, F.; Inglese, M. Cerebellar lobule atrophy and disability in progressive MS. J. Neurol. Neurosurg. Psychiatry, 2017, 88(12), 1065-1072.
[http://dx.doi.org/10.1136/jnnp-2017-316448] [PMID: 28844067]
[248]
Batista, S.; d’Almeida, O.C.; Afonso, A.; Freitas, S.; Macário, C.; Sousa, L.; Castelo-Branco, M.; Santana, I.; Cunha, L. Impairment of social cognition in multiple sclerosis: Amygdala atrophy is the main predictor. Mult. Scler., 2017, 23(10), 1358-1366.
[http://dx.doi.org/10.1177/1352458516680750] [PMID: 28273767]
[249]
Sicotte, N.L.; Kern, K.C.; Giesser, B.S.; Arshanapalli, A.; Schultz, A.; Montag, M.; Wang, H.; Bookheimer, S.Y. Regional hippocampal atrophy in multiple sclerosis. Brain, 2008, 131(Pt 4), 1134-1141.
[http://dx.doi.org/10.1093/brain/awn030] [PMID: 18375977]
[250]
Ziehn, M.O.; Avedisian, A.A.; Tiwari-Woodruff, S.; Voskuhl, R.R. Hippocampal CA1 atrophy and synaptic loss during experimental autoimmune encephalomyelitis, EAE. Lab. Invest., 2010, 90(5), 774-786.
[http://dx.doi.org/10.1038/labinvest.2010.6] [PMID: 20157291]
[251]
Wegner, C.; Esiri, M.M.; Chance, S.A.; Palace, J.; Matthews, P.M. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology, 2006, 67(6), 960-967.
[http://dx.doi.org/10.1212/01.wnl.0000237551.26858.39] [PMID: 17000961]
[252]
Magliozzi, R.; Howell, O.W.; Reeves, C.; Roncaroli, F.; Nicholas, R.; Serafini, B.; Aloisi, F.; Reynolds, R. A Gradient of neuronal loss and meningeal inflammation in multiple sclerosis. Ann. Neurol., 2010, 68(4), 477-493.
[http://dx.doi.org/10.1002/ana.22230] [PMID: 20976767]
[253]
Peterson, J.W.; Bö, L.; Mörk, S.; Chang, A.; Trapp, B.D. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann. Neurol., 2001, 50(3), 389-400.
[http://dx.doi.org/10.1002/ana.1123] [PMID: 11558796]
[254]
Jurewicz, A.; Matysiak, M.; Tybor, K.; Kilianek, L.; Raine, C.S.; Selmaj, K. Tumour necrosis factor-induced death of adult human oligodendrocytes is mediated by apoptosis inducing factor. Brain, 2005, 128(Pt 11), 2675-2688.
[http://dx.doi.org/10.1093/brain/awh627] [PMID: 16219674]
[255]
Vartanian, T.; Li, Y.; Zhao, M.; Stefansson, K. Interferon-gamma-induced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis. Mol. Med., 1995, 1(7), 732-743.
[http://dx.doi.org/10.1007/BF03401888] [PMID: 8612196]
[256]
Takeuchi, H.; Wang, J.; Kawanokuchi, J.; Mitsuma, N.; Mizuno, T.; Suzumura, A. Interferon-gamma induces microglial-activation-induced cell death: a hypothetical mechanism of relapse and remission in multiple sclerosis. Neurobiol. Dis., 2006, 22(1), 33-39.
[http://dx.doi.org/10.1016/j.nbd.2005.09.014] [PMID: 16386911]
[257]
Rossi, S.; Motta, C.; Studer, V.; Macchiarulo, G.; Volpe, E.; Barbieri, F.; Ruocco, G.; Buttari, F.; Finardi, A.; Mancino, R.; Weiss, S.; Battistini, L.; Martino, G.; Furlan, R.; Drulovic, J.; Centonze, D. Interleukin-1β causes excitotoxic neurodegeneration and multiple sclerosis disease progression by activating the apoptotic protein p53. Mol. Neurodegener., 2014, 9, 56.
[http://dx.doi.org/10.1186/1750-1326-9-56] [PMID: 25495224]
[258]
Gilgun-Sherki, Y.; Melamed, E.; Offen, D. The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J. Neurol., 2004, 251(3), 261-268.
[http://dx.doi.org/10.1007/s00415-004-0348-9] [PMID: 15015004]
[259]
Nataf, S.; Carroll, S.L.; Wetsel, R.A.; Szalai, A.J.; Barnum, S.R. Attenuation of experimental autoimmune demyelination in complement-deficient mice. J. Immunol., 2000, 165(10), 5867-5873.
[http://dx.doi.org/10.4049/jimmunol.165.10.5867] [PMID: 11067947]
[260]
Szalai, A.J.; Hu, X.; Adams, J.E.; Barnum, S.R. Complement in experimental autoimmune encephalomyelitis revisited: C3 is required for development of maximal disease. Mol. Immunol., 2007, 44(12), 3132-3136.
[http://dx.doi.org/10.1016/j.molimm.2007.02.002] [PMID: 17353050]
[261]
Roostaei, T.; Sadaghiani, S.; Mashhadi, R.; Falahatian, M.; Mohamadi, E.; Javadian, N.; Nazeri, A.; Doosti, R.; Naser Moghadasi, A.; Owji, M.; Hashemi Taheri, A.P.; Shakouri Rad, A.; Azimi, A.; Voineskos, A.N.; Nazeri, A.; Sahraian, M.A. Convergent effects of a functional C3 variant on brain atrophy, demyelination, and cognitive impairment in multiple sclerosis. Mult. Scler., 2018.1352458518760715
[PMID: 29485352]
[262]
Niculescu, T.; Weerth, S.; Niculescu, F.; Cudrici, C.; Rus, V.; Raine, C.S.; Shin, M.L.; Rus, H. Effects of complement C5 on apoptosis in experimental autoimmune encephalomyelitis. J. Immunol., 2004, 172(9), 5702-5706.
[http://dx.doi.org/10.4049/jimmunol.172.9.5702] [PMID: 15100315]
[263]
Watkins, L.M.; Neal, J.W.; Loveless, S.; Michailidou, I.; Ramaglia, V.; Rees, M.I.; Reynolds, R.; Robertson, N.P.; Morgan, B.P.; Howell, O.W. Complement is activated in progressive multiple sclerosis cortical grey matter lesions. J. Neuroinflammation, 2016, 13(1), 161.
[http://dx.doi.org/10.1186/s12974-016-0611-x] [PMID: 27333900]
[264]
Papadopoulos, D.; Dukes, S.; Patel, R.; Nicholas, R.; Vora, A.; Reynolds, R. Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis. Brain Pathol., 2009, 19(2), 238-253.
[http://dx.doi.org/10.1111/j.1750-3639.2008.00177.x] [PMID: 18492094]
[265]
Jürgens, T.; Jafari, M.; Kreutzfeldt, M.; Bahn, E.; Brück, W.; Kerschensteiner, M.; Merkler, D. Reconstruction of single cortical projection neurons reveals primary spine loss in multiple sclerosis. Brain, 2016, 139(Pt 1), 39-46.
[http://dx.doi.org/10.1093/brain/awv353] [PMID: 26667278]
[266]
Dutta, R.; Chang, A.; Doud, M.K.; Kidd, G.J.; Ribaudo, M.V.; Young, E.A.; Fox, R.J.; Staugaitis, S.M.; Trapp, B.D. Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients. Ann. Neurol., 2011, 69(3), 445-454.
[http://dx.doi.org/10.1002/ana.22337] [PMID: 21446020]
[267]
Zhu, B.; Luo, L.; Moore, G.R.; Paty, D.W.; Cynader, M.S. Dendritic and synaptic pathology in experimental autoimmune encephalomyelitis. Am. J. Pathol., 2003, 162(5), 1639-1650.
[http://dx.doi.org/10.1016/S0002-9440(10)64298-8] [PMID: 12707048]
[268]
Michailidou, I.; Willems, J.G.; Kooi, E.J.; van Eden, C.; Gold, S.M.; Geurts, J.J.; Baas, F.; Huitinga, I.; Ramaglia, V. Complement C1q-C3-associated synaptic changes in multiple sclerosis hippocampus. Ann. Neurol., 2015, 77(6), 1007-1026.
[http://dx.doi.org/10.1002/ana.24398] [PMID: 25727254]
[269]
Koning, N.; Bö, L.; Hoek, R.M.; Huitinga, I. Downregulation of macrophage inhibitory molecules in multiple sclerosis lesions. Ann. Neurol., 2007, 62(5), 504-514.
[http://dx.doi.org/10.1002/ana.21220] [PMID: 17879969]
[270]
Han, M.H.; Lundgren, D.H.; Jaiswal, S.; Chao, M.; Graham, K.L.; Garris, C.S.; Axtell, R.C.; Ho, P.P.; Lock, C.B.; Woodard, J.I.; Brownell, S.E.; Zoudilova, M.; Hunt, J.F.; Baranzini, S.E.; Butcher, E.C.; Raine, C.S.; Sobel, R.A.; Han, D.K.; Weissman, I.; Steinman, L. Janus-like opposing roles of CD47 in autoimmune brain inflammation in humans and mice. J. Exp. Med., 2012, 209(7), 1325-1334.
[http://dx.doi.org/10.1084/jem.20101974] [PMID: 22734047]
[271]
Freria, C.M.; Zanon, R.G.; Santos, L.M.; Oliveira, A.L. Major histocompatibility complex class I expression and glial reaction influence spinal motoneuron synaptic plasticity during the course of experimental autoimmune encephalomyelitis. J. Comp. Neurol., 2010, 518(7), 990-1007.
[http://dx.doi.org/10.1002/cne.22259] [PMID: 20127802]
[272]
Vercellino, M.; Fenoglio, C.; Galimberti, D.; Mattioda, A.; Chiavazza, C.; Binello, E.; Pinessi, L.; Giobbe, D.; Scarpini, E.; Cavalla, P. Progranulin genetic polymorphisms influence progression of disability and relapse recovery in multiple sclerosis. Mult. Scler., 2016, 22(8), 1007-1012.
[http://dx.doi.org/10.1177/1352458515610646] [PMID: 26447062]
[273]
Vercellino, M.; Grifoni, S.; Romagnolo, A.; Masera, S.; Mattioda, A.; Trebini, C.; Chiavazza, C.; Caligiana, L.; Capello, E.; Mancardi, G.L.; Giobbe, D.; Mutani, R.; Giordana, M.T.; Cavalla, P. Progranulin expression in brain tissue and cerebrospinal fluid levels in multiple sclerosis. Mult. Scler., 2011, 17(10), 1194-1201.
[http://dx.doi.org/10.1177/1352458511406164] [PMID: 21613335]
[274]
De Riz, M.; Galimberti, D.; Fenoglio, C.; Piccio, L.M.; Scalabrini, D.; Venturelli, E.; Pietroboni, A.; Piola, M.; Naismith, R.T.; Parks, B.J.; Fumagalli, G.; Bresolin, N.; Cross, A.H.; Scarpini, E. Cerebrospinal fluid progranulin levels in patients with different multiple sclerosis subtypes. Neurosci. Lett., 2010, 469(2), 234-236.
[http://dx.doi.org/10.1016/j.neulet.2009.12.002] [PMID: 19963041]
[275]
Kastenbauer, S.; Koedel, U.; Wick, M.; Kieseier, B.C.; Hartung, H.P.; Pfister, H.W. CSF and serum levels of soluble fractalkine (CX3CL1) in inflammatory diseases of the nervous system. J. Neuroimmunol., 2003, 137(1-2), 210-217.
[http://dx.doi.org/10.1016/S0165-5728(03)00085-7] [PMID: 12667665]
[276]
Mills, J.H.; Alabanza, L.M.; Mahamed, D.A.; Bynoe, M.S. Extracellular adenosine signaling induces CX3CL1 expression in the brain to promote experimental autoimmune encephalomyelitis. J. Neuroinflammation, 2012, 9, 193.
[http://dx.doi.org/10.1186/1742-2094-9-193] [PMID: 22883932]
[277]
Hulshof, S.; van Haastert, E.S.; Kuipers, H.F.; van den Elsen, P.J.; De Groot, C.J.; van der Valk, P.; Ravid, R.; Biber, K. CX3CL1 and CX3CR1 expression in human brain tissue: noninflammatory control versus multiple sclerosis. J. Neuropathol. Exp. Neurol., 2003, 62(9), 899-907.
[http://dx.doi.org/10.1093/jnen/62.9.899] [PMID: 14533779]
[278]
Huang, D.; Shi, F.D.; Jung, S.; Pien, G.C.; Wang, J.; Salazar-Mather, T.P.; He, T.T.; Weaver, J.T.; Ljunggren, H.G.; Biron, C.A.; Littman, D.R.; Ransohoff, R.M. The neuronal chemokine CX3CL1/fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. FASEB J., 2006, 20(7), 896-905.
[http://dx.doi.org/10.1096/fj.05-5465com] [PMID: 16675847]
[279]
Kroksveen, A.C.; Guldbrandsen, A.; Vedeler, C.; Myhr, K.M.; Opsahl, J.A.; Berven, F.S. Cerebrospinal fluid proteome comparison between multiple sclerosis patients and controls. Acta Neurol. Scand. Suppl., 2012, (195), 90-96.
[http://dx.doi.org/10.1111/ane.12029] [PMID: 23278663]
[280]
Blakely, P.K.; Hussain, S.; Carlin, L.E.; Irani, D.N. Astrocyte matricellular proteins that control excitatory synaptogenesis are regulated by inflammatory cytokines and correlate with paralysis severity during experimental autoimmune encephalomyelitis. Front. Neurosci., 2015, 9, 344.
[http://dx.doi.org/10.3389/fnins.2015.00344] [PMID: 26500475]
[281]
Vercellino, M.; Merola, A.; Piacentino, C.; Votta, B.; Capello, E.; Mancardi, G.L.; Mutani, R.; Giordana, M.T.; Cavalla, P. Altered glutamate reuptake in relapsing-remitting and secondary progressive multiple sclerosis cortex: Correlation with microglia infiltration, demyelination, and neuronal and synaptic damage. J. Neuropathol. Exp. Neurol., 2007, 66(8), 732-739.
[http://dx.doi.org/10.1097/nen.0b013e31812571b0] [PMID: 17882017]
[282]
Rossi, S.; Muzio, L.; De Chiara, V.; Grasselli, G.; Musella, A.; Musumeci, G.; Mandolesi, G.; De Ceglia, R.; Maida, S.; Biffi, E.; Pedrocchi, A.; Menegon, A.; Bernardi, G.; Furlan, R.; Martino, G.; Centonze, D. Impaired striatal GABA transmission in experimental autoimmune encephalomyelitis. Brain Behav. Immun., 2011, 25(5), 947-956.
[http://dx.doi.org/10.1016/j.bbi.2010.10.004] [PMID: 20940040]
[283]
Habbas, S.; Santello, M.; Becker, D.; Stubbe, H.; Zappia, G.; Liaudet, N.; Klaus, F.R.; Kollias, G.; Fontana, A.; Pryce, C.R.; Suter, T.; Volterra, A. Neuroinflammatory TNFα Impairs Memory via Astrocyte Signaling. Cell, 2015, 163(7), 1730-1741.
[http://dx.doi.org/10.1016/j.cell.2015.11.023] [PMID: 26686654]
[284]
Takeuchi, H.; Jin, S.; Wang, J.; Zhang, G.; Kawanokuchi, J.; Kuno, R.; Sonobe, Y.; Mizuno, T.; Suzumura, A. Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J. Biol. Chem., 2006, 281(30), 21362-21368.
[http://dx.doi.org/10.1074/jbc.M600504200] [PMID: 16720574]
[285]
Yang, G.; Parkhurst, C.N.; Hayes, S.; Gan, W.B. Peripheral elevation of TNF-α leads to early synaptic abnormalities in the mouse somatosensory cortex in experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA, 2013, 110(25), 10306-10311.
[http://dx.doi.org/10.1073/pnas.1222895110] [PMID: 23733958]
[286]
de Lago, E.; Moreno-Martet, M.; Cabranes, A.; Ramos, J.A.; Fernández-Ruiz, J. Cannabinoids ameliorate disease progression in a model of multiple sclerosis in mice, acting preferentially through CB1 receptor-mediated anti-inflammatory effects. Neuropharmacology, 2012, 62(7), 2299-2308.
[http://dx.doi.org/10.1016/j.neuropharm.2012.01.030] [PMID: 22342378]
[287]
Rossi, S.; Furlan, R.; De Chiara, V.; Muzio, L.; Musella, A.; Motta, C.; Studer, V.; Cavasinni, F.; Bernardi, G.; Martino, G.; Cravatt, B.F.; Lutz, B.; Maccarrone, M.; Centonze, D. Cannabinoid CB1 receptors regulate neuronal TNF-α effects in experimental autoimmune encephalomyelitis. Brain Behav. Immun., 2011, 25(6), 1242-1248.
[http://dx.doi.org/10.1016/j.bbi.2011.03.017] [PMID: 21473912]
[288]
Shijie, J.; Takeuchi, H.; Yawata, I.; Harada, Y.; Sonobe, Y.; Doi, Y.; Liang, J.; Hua, L.; Yasuoka, S.; Zhou, Y.; Noda, M.; Kawanokuchi, J.; Mizuno, T.; Suzumura, A. Blockade of glutamate release from microglia attenuates experimental autoimmune encephalomyelitis in mice. Tohoku J. Exp. Med., 2009, 217(2), 87-92.
[http://dx.doi.org/10.1620/tjem.217.87] [PMID: 19212100]
[289]
Stilo, S.A.; Murray, R.M. The epidemiology of schizophrenia: replacing dogma with knowledge. Dialogues Clin. Neurosci., 2010, 12(3), 305-315.
[PMID: 20954427]
[290]
Patel, K.R.; Cherian, J.; Gohil, K.; Atkinson, D. Schizophrenia: overview and treatment options. P&T, 2014, 39(9), 638-345.
[291]
Picchioni, M.M.; Murray, R.M. Schizophrenia. BMJ, 2007, 335(7610), 91-95.
[http://dx.doi.org/10.1136/bmj.39227.616447.BE] [PMID: 17626963]
[292]
Johnstone, E.C.; Crow, T.J.; Frith, C.D.; Husband, J.; Kreel, L. Cerebral ventricular size and cognitive impairment in chronic schizophrenia. Lancet, 1976, 2(7992), 924-926.
[http://dx.doi.org/10.1016/S0140-6736(76)90890-4] [PMID: 62160]
[293]
Keilp, J.G.; Sweeney, J.A.; Jacobsen, P.; Solomon, C.; St Louis, L.; Deck, M.; Frances, A.; Mann, J.J. Cognitive impairment in schizophrenia: specific relations to ventricular size and negative symptomatology. Biol. Psychiatry, 1988, 24(1), 47-55.
[http://dx.doi.org/10.1016/0006-3223(88)90120-5] [PMID: 3370277]
[294]
Vita, A.; De Peri, L.; Silenzi, C.; Dieci, M. Brain morphology in first-episode schizophrenia: a meta-analysis of quantitative magnetic resonance imaging studies. Schizophr. Res., 2006, 82(1), 75-88.
[http://dx.doi.org/10.1016/j.schres.2005.11.004] [PMID: 16377156]
[295]
Lawrie, S.M.; Abukmeil, S.S. Brain abnormality in schizophrenia. A systematic and quantitative review of volumetric magnetic resonance imaging studies. Br. J. Psychiatry, 1998, 172, 110-120.
[http://dx.doi.org/10.1192/bjp.172.2.110] [PMID: 9519062]
[296]
Goldman, A.L.; Pezawas, L.; Mattay, V.S.; Fischl, B.; Verchinski, B.A.; Chen, Q.; Weinberger, D.R.; Meyer-Lindenberg, A. Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Arch. Gen. Psychiatry, 2009, 66(5), 467-477.
[http://dx.doi.org/10.1001/archgenpsychiatry.2009.24] [PMID: 19414706]
[297]
Thune, J.J.; Uylings, H.B.; Pakkenberg, B. No deficit in total number of neurons in the prefrontal cortex in schizophrenics. J. Psychiatr. Res., 2001, 35(1), 15-21.
[http://dx.doi.org/10.1016/S0022-3956(00)00043-1] [PMID: 11287052]
[298]
Selemon, L.D.; Rajkowska, G.; Goldman-Rakic, P.S. Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch. Gen. Psychiatry, 1995, 52(10), 805-818.
[http://dx.doi.org/10.1001/archpsyc.1995.03950220015005] [PMID: 7575100]
[299]
Selemon, L.D.; Rajkowska, G.; Goldman-Rakic, P.S. Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J. Comp. Neurol., 1998, 392(3), 402-412.
[http://dx.doi.org/10.1002/(SICI)1096-9861(19980316)392:3<402:AID-CNE9>3.0.CO;2-5] [PMID: 9511926]
[300]
Roberts, R.C.; Conley, R.; Kung, L.; Peretti, F.J.; Chute, D.J. Reduced striatal spine size in schizophrenia: a postmortem ultrastructural study. Neuroreport, 1996, 7(6), 1214-1218.
[http://dx.doi.org/10.1097/00001756-199604260-00024] [PMID: 8817535]
[301]
Rosoklija, G.; Toomayan, G.; Ellis, S.P.; Keilp, J.; Mann, J.J.; Latov, N.; Hays, A.P.; Dwork, A.J. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch. Gen. Psychiatry, 2000, 57(4), 349-356.
[http://dx.doi.org/10.1001/archpsyc.57.4.349] [PMID: 10768696]
[302]
Garey, L.J.; Ong, W.Y.; Patel, T.S.; Kanani, M.; Davis, A.; Mortimer, A.M.; Barnes, T.R.; Hirsch, S.R. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J. Neurol. Neurosurg. Psychiatry, 1998, 65(4), 446-453.
[http://dx.doi.org/10.1136/jnnp.65.4.446] [PMID: 9771764]
[303]
Sweet, R. A.; Henteleff, R. A.; Zhang, W.; Sampson, A. R.; Lewis, D. A. Reduced dendritic spine density in auditory cor-tex of subjects with schizophrenia. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, 34(4), 374-389.2009.
[304]
Glantz, L.A.; Lewis, D.A. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch. Gen. Psychiatry, 2000, 57(1), 65-73.
[http://dx.doi.org/10.1001/archpsyc.57.1.65] [PMID: 10632234]
[305]
Konopaske, G.T.; Lange, N.; Coyle, J.T.; Benes, F.M. Prefrontal cortical dendritic spine pathology in schizophrenia and bipolar disorder. JAMA Psychiatry, 2014, 71(12), 1323-1331.
[http://dx.doi.org/10.1001/jamapsychiatry.2014.1582] [PMID: 25271938]
[306]
Feinberg, I. Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? J. Psychiatr. Res., 1982-1983, 17(4), 319-334.
[http://dx.doi.org/10.1016/0022-3956(82) 90038-3] [PMID: 7187776]
[307]
Davis, J.; Eyre, H.; Jacka, F.N.; Dodd, S.; Dean, O.; McEwen, S.; Debnath, M.; McGrath, J.; Maes, M.; Amminger, P.; McGorry, P.D.; Pantelis, C.; Berk, M. A review of vulnerability and risks for schizophrenia: Beyond the two hit hypothesis. Neurosci. Biobehav. Rev., 2016, 65, 185-194.
[http://dx.doi.org/10.1016/j.neubiorev. 2016.03.017] [PMID: 27073049]
[308]
Sekar, A.; Bialas, A.R.; de Rivera, H.; Davis, A.; Hammond, T.R.; Kamitaki, N.; Tooley, K.; Presumey, J.; Baum, M.; Van Doren, V.; Genovese, G.; Rose, S.A.; Handsaker, R.E.; Daly, M.J.; Carroll, M.C.; Stevens, B.; McCarroll, S.A. Schizophrenia Working Group of the Psychiatric Genomics Consortium. Schizophrenia risk from complex variation of complement component 4. Nature, 2016, 530(7589), 177-183.
[http://dx.doi.org/10.1038/nature16549] [PMID: 26814963]
[309]
Prasad, K.M.; Chowdari, K.V.; D’Aiuto, L.A.; Iyengar, S.; Stanley, J.A.; Nimgaonkar, V.L. Neuropil contraction in relation to Complement C4 gene copy numbers in independent cohorts of adolescent-onset and young adult-onset schizophrenia patients-a pilot study. Transl. Psychiatry, 2018, 8(1), 134.
[http://dx.doi.org/10.1038/s41398-018-0181-z] [PMID: 30026462]
[310]
Laskaris, L.; Zalesky, A.; Weickert, C.S.; Di Biase, M.A.; Chana, G.; Baune, B.T.; Bousman, C.; Nelson, B.; McGorry, P.; Everall, I.; Pantelis, C.; Cropley, V. Investigation of pe-ripheral complement factors across stages of psychosis. Schizophr. Res., 2018, 204, 30-37.
[PMID: 30527272]
[311]
Martins-de-Souza, D.; Gattaz, W.F.; Schmitt, A.; Rewerts, C.; Maccarrone, G.; Dias-Neto, E.; Turck, C.W. Prefrontal cortex shotgun proteome analysis reveals altered calcium homeostasis and immune system imbalance in schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci., 2009, 259(3), 151-163.
[http://dx.doi.org/10.1007/s00406-008-0847-2] [PMID: 19165527]
[312]
Gupta, D.S.; McCullumsmith, R.E.; Beneyto, M.; Haroutunian, V.; Davis, K.L.; Meador-Woodruff, J.H. Metabotropic glutamate receptor protein expression in the prefrontal cortex and striatum in schizophrenia. Synapse, 2005, 57(3), 123-131.
[http://dx.doi.org/10.1002/syn.20164] [PMID: 15945063]
[313]
Ayoub, M.A.; Angelicheva, D.; Vile, D.; Chandler, D.; Morar, B.; Cavanaugh, J.A.; Visscher, P.M.; Jablensky, A.; Pfleger, K.D.; Kalaydjieva, L. Deleterious GRM1 mutations in schizophrenia. PLoS One, 2012, 7(3)e32849
[http://dx.doi.org/10.1371/journal.pone.0032849] [PMID: 22448230]
[314]
Kovács, T.; Kelemen, O.; Kéri, S. Decreased fragile X mental retardation protein (FMRP) is associated with lower IQ and earlier illness onset in patients with schizophrenia. Psychiatry Res., 2013, 210(3), 690-693.
[http://dx.doi.org/10.1016/j.psychres.2012.12.022] [PMID: 23333116]
[315]
Pouget, J.G.; Goncalves, V.F. Schizophrenia Working Group of the Psychiatric Genomics, C.; Spain, S. L.; Finucane, H. K.; Raychaudhuri, S.; Kennedy, J. L.; Knight, J., Genome-Wide Association Studies Suggest Limited Immune Gene Enrich-ment in Schizophrenia Compared to 5 Autoimmune Diseases. Schizophr. Bull., 2016, 42(5), 1176-1184.
[http://dx.doi.org/10.1093/schbul/sbw059] [PMID: 27242348]
[316]
Rajarajan, P.; Borrman, T.; Liao, W.; Schrode, N.; Flaherty, E.; Casiño, C.; Powell, S.; Yashaswini, C.; LaMarca, E.A.; Kassim, B.; Javidfar, B.; Espeso-Gil, S.; Li, A.; Won, H.; Geschwind, D.H.; Ho, S.M.; MacDonald, M.; Hoffman, G.E.; Roussos, P.; Zhang, B.; Hahn, C.G.; Weng, Z.; Brennand, K.J.; Akbarian, S. Neuron-specific signatures in the chromosomal connectome associated with schizophrenia risk. Science, 2018, 362(6420)eaat4311
[http://dx.doi.org/10.1126/science.aat4311] [PMID: 30545851]
[317]
Schwarz, E.; Izmailov, R.; Liò, P.; Meyer-Lindenberg, A. Protein Interaction Networks Link Schizophrenia Risk Loci to Synaptic Function. Schizophr. Bull., 2016, 42(6), 1334-1342.
[http://dx.doi.org/10.1093/schbul/sbw035] [PMID: 27056717]
[318]
Bergon, A.; Belzeaux, R.; Comte, M.; Pelletier, F.; Hervé, M.; Gardiner, E.J.; Beveridge, N.J.; Liu, B.; Carr, V.; Scott, R.J.; Kelly, B.; Cairns, M.J.; Kumarasinghe, N.; Schall, U.; Blin, O.; Boucraut, J.; Tooney, P.A.; Fakra, E.; Ibrahim, E.C. CX3CR1 is dysregulated in blood and brain from schizophrenia patients. Schizophr. Res., 2015, 168(1-2), 434-443.
[http://dx.doi.org/10.1016/j.schres.2015.08.010] [PMID: 26285829]
[319]
Ishizuka, K.; Fujita, Y.; Kawabata, T.; Kimura, H.; Iwayama, Y.; Inada, T.; Okahisa, Y.; Egawa, J.; Usami, M.; Kushima, I.; Uno, Y.; Okada, T.; Ikeda, M.; Aleksic, B.; Mori, D.; Someya, T.; Yoshikawa, T.; Iwata, N.; Nakamura, H.; Yamashita, T.; Ozaki, N. Rare genetic variants in CX3CR1 and their contribution to the increased risk of schizophrenia and autism spectrum disorders. Transl. Psychiatry, 2017, 7(8)e1184
[http://dx.doi.org/10.1038/tp.2017.173] [PMID: 28763059]
[320]
Stefansson, H.; Ophoff, R.A.; Steinberg, S.; Andreassen, O.A.; Cichon, S.; Rujescu, D.; Werge, T.; Pietilainen, O.P.; Mors, O.; Mortensen, P.B.; Sigurdsson, E.; Gustafsson, O.; Nyegaard, M.; Tuulio-Henriksson, A.; Ingason, A.; Hansen, T.; Suvisaari, J.; Lonnqvist, J.; Paunio, T.; Borglum, A.D.; Hartmann, A.; Fink-Jensen, A.; Nordentoft, M.; Hougaard, D.; Norgaard-Pedersen, B.; Bottcher, Y.; Olesen, J.; Breuer, R.; Moller, H.J.; Giegling, I.; Rasmussen, H.B.; Timm, S.; Mat-theisen, M.; Bitter, I.; Rethelyi, J.M.; Magnusdottir, B.B.; Sigmundsson, T.; Olason, P.; Masson, G.; Gulcher, J.R.; Har-aldsson, M.; Fossdal, R.; Thorgeirsson, T.E.; Thorsteinsdot-tir, U.; Ruggeri, M.; Tosato, S.; Franke, B.; Strengman, E.; Kiemeney, L.A.; Genetic, R. Outcome in, P.; Melle, I.; Dju-rovic, S.; Abramova, L.; Kaleda, V.; Sanjuan, J.; de Frutos, R.; Bramon, E.; Vassos, E.; Fraser, G.; Ettinger, U.; Picchioni, M.; Walker, N.; Toulopoulou, T.; Need, A. C.; Ge, D.; Yoon, J. L.; Shianna, K. V.; Freimer, N. B.; Cantor, R. M.; Murray, R.; Kong, A.; Golimbet, V.; Carracedo, A.; Arango, C.; Costas, J.; Jonsson, E. G.; Terenius, L.; Agartz, I.; Petursson, H.; Nothen, M. M.; Rietschel, M.; Matthews, P. M.; Muglia, P.; Peltonen, L.; St Clair, D.; Goldstein, D. B.; Stefansson, K.; Collier, D. A. Common variants conferring risk of schizo-phrenia. Nature, 2009, 460(7256), 744-747.
[http://dx.doi.org/10.1038/nature08186] [PMID: 19571808]
[321]
Purcell, S.M.; Wray, N.R.; Stone, J.L.; Visscher, P.M.; O’Donovan, M.C.; Sullivan, P.F.; Sklar, P. International Schizophrenia ConsortiumCommon polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature, 2009, 460(7256), 748-752.
[http://dx.doi.org/10.1038/nature08185] [PMID: 19571811]
[322]
Galimberti, D.; Dell’Osso, B.; Fenoglio, C.; Villa, C.; Cortini, F.; Serpente, M.; Kittel-Schneider, S.; Weigl, J.; Neuner, M.; Volkert, J.; Leonhard, C.; Olmes, D.G.; Kopf, J.; Cantoni, C.; Ridolfi, E.; Palazzo, C.; Ghezzi, L.; Bresolin, N.; Altamura, A.C.; Scarpini, E.; Reif, A. Progranulin gene variability and plasma levels in bipolar disorder and schizophrenia. PLoS One, 2012, 7(4)e32164
[http://dx.doi.org/10.1371/journal.pone.0032164] [PMID: 22505994]
[323]
Farhy-Tselnicker, I.; van Casteren, A.C.M.; Lee, A.; Chang, V.T.; Aricescu, A.R.; Allen, N.J. Astrocyte-Secreted Glypican 4 Regulates Release of Neuronal Pentraxin 1 from Axons to Induce Functional Synapse Formation. Neuron, 2017, 96(2), 428-445.
[324]
Potkin, S.G.; Macciardi, F.; Guffanti, G.; Fallon, J.H.; Wang, Q.; Turner, J.A.; Lakatos, A.; Miles, M.F.; Lander, A.; Vawter, M.P.; Xie, X. Identifying gene regulatory networks in schizophrenia. Neuroimage, 2010, 53(3), 839-847.
[http://dx.doi.org/10.1016/j.neuroimage.2010.06.036] [PMID: 20600988]
[325]
Laskaris, L.E.; Di Biase, M.A.; Everall, I.; Chana, G.; Christopoulos, A.; Skafidas, E.; Cropley, V.L.; Pantelis, C. Microglial activation and progressive brain changes in schizophrenia. Br. J. Pharmacol., 2016, 173(4), 666-680.
[http://dx.doi.org/10.1111/bph.13364] [PMID: 26455353]
[326]
Trépanier, M.O.; Hopperton, K.E.; Mizrahi, R.; Mechawar, N.; Bazinet, R.P. Postmortem evidence of cerebral inflammation in schizophrenia: a systematic review. Mol. Psychiatry, 2016, 21(8), 1009-1026.
[http://dx.doi.org/10.1038/mp.2016.90] [PMID: 27271499]
[327]
Pasternak, O.; Kubicki, M.; Shenton, M.E. In vivo imaging of neuroinflammation in schizophrenia. Schizophr. Res., 2016, 173(3), 200-212.
[http://dx.doi.org/10.1016/j.schres.2015.05.034] [PMID: 26048294]
[328]
van Kesteren, C.F.; Gremmels, H.; de Witte, L.D.; Hol, E.M.; Van Gool, A.R.; Falkai, P.G.; Kahn, R.S.; Sommer, I.E. Immune involvement in the pathogenesis of schizophrenia: a meta-analysis on postmortem brain studies. Transl. Psychiatry, 2017, 7(3)e1075
[http://dx.doi.org/10.1038/tp.2017.4] [PMID: 28350400]
[329]
Quidé, Y.; Bortolasci, C.C.; Spolding, B.; Kidnapillai, S.; Watkeys, O.J.; Cohen-Woods, S.; Berk, M.; Carr, V.J.; Walder, K.; Green, M.J. Association between childhood trauma exposure and pro-inflammatory cytokines in schizophrenia and bipolar-I disorder. Psychol. Med., 2018, 1-9.
[http://dx.doi.org/10.1017/S0033291718003690] [PMID: 30560764]
[330]
Gallego, J.A.; Blanco, E.A.; Husain-Krautter, S.; Madeline Fagen, E.; Moreno-Merino, P.; Del Ojo-Jiménez, J.A.; Ahmed, A.; Rothstein, T.L.; Lencz, T.; Malhotra, A.K. Cytokines in cerebrospinal fluid of patients with schizophrenia spectrum disorders: New data and an updated meta-analysis. Schizophr. Res., 2018, 202, 64-71.
[http://dx.doi.org/10.1016/j.schres.2018.07.019] [PMID: 30025760]
[331]
Goldsmith, D.R.; Rapaport, M.H.; Miller, B.J. A meta-analysis of blood cytokine network alterations in psychiatric patients: comparisons between schizophrenia, bipolar disorder and depression. Mol. Psychiatry, 2016, 21(12), 1696-1709.
[http://dx.doi.org/10.1038/mp.2016.3] [PMID: 26903267]
[332]
Miller, B.J.; Buckley, P.; Seabolt, W.; Mellor, A.; Kirkpatrick, B. Meta-analysis of cytokine alterations in schizophrenia: Clinical status and antipsychotic effects. Biol. Psychiatry, 2011, 70(7), 663-671.
[http://dx.doi.org/10.1016/j.biopsych.2011.04.013] [PMID: 21641581]
[333]
Brown, A.S. Prenatal infection as a risk factor for schizophrenia. Schizophr. Bull., 2006, 32(2), 200-202.
[http://dx.doi.org/10.1093/schbul/sbj052] [PMID: 16469941]
[334]
Mattei, D.; Ivanov, A.; Ferrai, C.; Jordan, P.; Guneykaya, D.; Buonfiglioli, A.; Schaafsma, W.; Przanowski, P.; Deuther-Conrad, W.; Brust, P.; Hesse, S.; Patt, M.; Sabri, O.; Ross, T.L.; Eggen, B.J.L.; Boddeke, E.W.G.M.; Kaminska, B.; Beule, D.; Pombo, A.; Kettenmann, H.; Wolf, S.A. Maternal immune activation results in complex microglial transcriptome signature in the adult offspring that is reversed by minocycline treatment. Transl. Psychiatry, 2017, 7(5)e1120
[http://dx.doi.org/10.1038/tp.2017.80] [PMID: 28485733]
[335]
Coiro, P.; Padmashri, R.; Suresh, A.; Spartz, E.; Pendyala, G.; Chou, S.; Jung, Y.; Meays, B.; Roy, S.; Gautam, N.; Alnouti, Y.; Li, M.; Dunaevsky, A. Impaired synaptic development in a maternal immune activation mouse model of neurodevelopmental disorders. Brain Behav. Immun., 2015, 50, 249-258.
[http://dx.doi.org/10.1016/j.bbi.2015.07.022] [PMID: 26218293]
[336]
Pendyala, G.; Chou, S.; Jung, Y.; Coiro, P.; Spartz, E.; Pad-mashri, R.; Li, M.; Dunaevsky, A. Maternal immune Activation causes Behavioral impairments and altered cerebellar cytokine and synaptic protein expression. Neuropsychopharmacology, 2017, 42(7), 1435-1446.
[337]
Brennand, K.J.; Simone, A.; Jou, J.; Gelboin-Burkhart, C.; Tran, N.; Sangar, S.; Li, Y.; Mu, Y.; Chen, G.; Yu, D.; McCarthy, S.; Sebat, J.; Gage, F.H. Modelling schizophrenia using human induced pluripotent stem cells. Nature, 2011, 473(7346), 221-225.
[http://dx.doi.org/10.1038/nature09915] [PMID: 21490598]
[338]
Sellgren, C.M.; Gracias, J.; Watmuff, B.; Biag, J.D.; Thanos, J.M.; Whittredge, P.B.; Fu, T.; Worringer, K.; Brown, H.E.; Wang, J.; Kaykas, A.; Karmacharya, R.; Goold, C.P.; Sheridan, S.D.; Perlis, R.H. Increased synapse elimination by microglia in schizophrenia patient-derived models of synaptic pruning. Nat. Neurosci., 2019, 22(3), 374-385.
[http://dx.doi.org/10.1038/s41593-018-0334-7] [PMID: 30718903]
[339]
Chen, X.; Xiong, Z.; Li, Z.; Yang, Y.; Zheng, Z.; Li, Y.; Xie, Y.; Li, Z. Minocycline as adjunct therapy for a male patient with deficit schizophrenia. Neuropsychiatr. Dis. Treat., 2018, 14, 2697-2701.
[http://dx.doi.org/10.2147/NDT.S179658] [PMID: 30349268]

© 2024 Bentham Science Publishers | Privacy Policy