Do glia drive synaptic and cognitive impairment in disease?
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Synaptic dysfunction is a hallmark of many neurodegenerative and psychiatric brain disorders, yet we know little about the mechanisms that underlie synaptic vulnerability. Although neuroinflammation and reactive gliosis are prominent in virtually every CNS disease, glia are largely viewed as passive responders to neuronal damage rather than drivers of synaptic dysfunction. This perspective is changing with the growing realization that glia actively signal with neurons and influence synaptic development, transmission and plasticity through an array of secreted and contact-dependent signals. We propose that disruptions in neuron-glia signaling contribute to synaptic and cognitive impairment in disease. Illuminating the mechanisms by which glia influence synapse function may lead to the development of new therapies and biomarkers for synaptic dysfunction.
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During normal brain development, microglia engulf synapses and sculpt synaptic connections via a role for complement.
“During normal brain development, mounting evidence indicates that microglia engulf synapses and sculpt synaptic connections via a novel role for complement, a component of the innate immune system that enhances the clearance of microbes or damaged cells by phagocytes (Boulanger, 2009; Stephan et al., 2012; Chung et al., 2015).”
From Microglia in Alzheimer’s disease (2018) · cites this paper as Chung et al., 2015
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Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
Glutamate neurotoxicity and diseases of the nervous system
Choi, D. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90162-6 · Cited by 8,152 · see citing works
Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo
Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005) · Science · doi:10.1126/science.1110647 · Cited by 5,827 · see citing works
Fate Mapping Analysis Reveals That Adult Microglia Derive from Primitive Macrophages
Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M. F., Conway, S. J., Ng, L. G., Stanley, E. R., et al. (2010) · Science · doi:10.1126/science.1194637 · Cited by 5,175 · see citing works
Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., Phatnani, H. P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1860-14.2014 · Cited by 4,875 · see citing works
Self-citationTerry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., & Katzman, R. (1991) · Annals of Neurology · doi:10.1002/ana.410300410 · Cited by 4,397 · see citing works
Meta-Analysis of 74,046 Individuals Identifies 11 New Susceptibility Loci for Alzheimer’s Disease
(EADI), E. A. D. I., Lambert, J.-C., (GERAD), G. A. E. R. I. A. D., Alzheimer's Disease Genetic Consortium (ADGC), (CHARGE), C. F. H. A. A. R. I. G. E., Ibrahim-Verbaas, C. A., Harold, D., Naj, A. C., Sims, R., Bellenguez, C., et al. (2013) · Nature Genetics · doi:10.1038/ng.2802 · Cited by 4,336 · see citing works
Synaptic Pruning by Microglia Is Necessary for Normal Brain Development
Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L., et al. (2011) · Science · doi:10.1126/science.1202529 · Cited by 4,244 · see citing works
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
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. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · see citing works
Self-citationApolipoprotein E and Alzheimer disease: risk, mechanisms and therapy
Liu, C.-C., Kanekiyo, T., Xu, H., & Bu, G. (2013) · Nature Reviews Neurology · doi:10.1038/nrneurol.2012.263 · Cited by 3,459 · see citing works
The Classical Complement Cascade Mediates CNS Synapse Elimination
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., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313 · see citing works
Self-citation<i>TREM2</i> Variants in Alzheimer's Disease
Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., Cruchaga, C., Sassi, C., Kauwe, J. S. K., Younkin, S., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211851 · Cited by 3,020 · see citing works
Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor
Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R., Lafaille, J. J., Hempstead, B. L., Littman, D. R., & Gan, W.-B. (2013) · Cell · doi:10.1016/j.cell.2013.11.030 · Cited by 2,599 · see citing works
A Lineage of Myeloid Cells Independent of Myb and Hematopoietic Stem Cells
Schulz, C., Perdiguero, E. G., Chorro, L., Szabo-Rogers, H., Cagnard, N., Kierdorf, K., Prinz, M., Wu, B., Jacobsen, S. E. W., Pollard, J. W., et al. (2012) · Science · doi:10.1126/science.1219179 · Cited by 2,578 · see citing works
Variant of <i>TREM2</i> Associated with the Risk of Alzheimer's Disease
Jonsson, T., Stefansson, H., Steinberg, S., Jonsdottir, I., Jonsson, P. V., Snaedal, J., Bjornsson, S., Huttenlocher, J., Levey, A. I., Lah, J. J., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211103 · Cited by 2,558 · see citing works
Transcriptomic Analysis of Autistic Brain Reveals Convergent Molecular Pathology
Voineagu, I., Wang, X., Johnston, P., Lowe, J. K., Tian, Y., Horvath, S., Mill, J., Cantor, R. M., Blencowe, B. J., & Geschwind, D. H. (2011) · Nature · doi:10.1038/nature10110 · Cited by 1,874 · see citing works
Microglial physiology: unique stimuli, specialized responses
Ransohoff, R. M., & Perry, V. H. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132528 · Cited by 1,858 · see citing works
Epilepsy and Exacerbation of Brain Injury in Mice Lacking the Glutamate Transporter GLT-1
Tanaka, K., Watase, K., Manabe, T., Yamada, K., Watanabe, M., Takahashi, K., Iwama, H., Nishikawa, T., Ichihara, N., Kikuchi, T., et al. (1997) · Science · doi:10.1126/science.276.5319.1699 · Cited by 1,755 · see citing works
TREM2 Lipid Sensing Sustains the Microglial Response in an Alzheimer’s Disease Model
Wang, Y., Cella, M., Mallinson, K., Ulrich, J. D., Young, K. L., Robinette, M. L., Gilfillan, S., Krishnan, G. M., Sudhakar, S., Zinselmeyer, B. H., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.049 · Cited by 1,736 · see citing works
Synaptic scaling mediated by glial TNF-α
Stellwagen, D., & Malenka, R. C. (2006) · Nature · doi:10.1038/nature04671 · Cited by 1,715 · see citing works
CNS synaptogenesis promoted by glia-derived cholesterol
Mauch, D. H., Nägler, K., Schumacher, S., Göritz, C., Müller, E.-C., Otto, A., & Pfrieger, F. W. (2001) · Science · doi:10.1126/science.294.5545.1354 · Cited by 1,711 · see citing works
Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis
Christopherson, K. S., Ullian, E. M., Stokes, C. C. A., Mullowney, C. E., Hell, J. W., Agah, A., Lawler, J., Mosher, D. F., Bornstein, P., & Barres, B. A. (2005) · Cell · doi:10.1016/j.cell.2004.12.020 · Cited by 1,688 · see citing works
Self-citationIntegrated Systems Approach Identifies Genetic Nodes and Networks in Late-Onset Alzheimer’s Disease
Zhang, B., Gaiteri, C., Bodea, L.-G., Wang, Z., McElwee, J., Podtelezhnikov, A. A., Zhang, C., Xie, T., Tran, L., Dobrin, R., et al. (2013) · Cell · doi:10.1016/j.cell.2013.03.030 · Cited by 1,657 · see citing works
Microglial interactions with synapses are modulated by visual experience
Tremblay, M.-È., Lowery, R. L., & Majewska, A. K. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000527 · Cited by 1,542 · see citing works
Dendritic spine pathology in neuropsychiatric disorders
Penzes, P., Cahill, M. E., Jones, K. A., VanLeeuwen, J.-E., & Woolfrey, K. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2741 · Cited by 1,523 · see citing works
Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways
Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E. G., Wieghofer, P., Heinrich, A., Riemke, P., Hölscher, C., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3318 · Cited by 1,468 · see citing works
Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence?
Feinberg, I. (1982) · Journal of Psychiatric Research · doi:10.1016/0022-3956(82)90038-3 · Cited by 1,395 · see citing works
Long-term potentiation depends on release of d-serine from astrocytes
Henneberger, C., Papouin, T., Oliet, S. H. R., & Rusakov, D. A. (2010) · Nature · doi:10.1038/nature08673 · Cited by 1,389 · see citing works
Control of Synapse Number by Glia
Ullian, E. M., Sapperstein, S. K., Christopherson, K. S., & Barres, B. A. (2001) · Science · doi:10.1126/science.291.5504.657 · Cited by 1,380 · see citing works
Self-citationAstrocytes mediate synapse elimination through MEGF10 and MERTK pathways
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., et al. (2013) · Nature · doi:10.1038/nature12776 · Cited by 1,377 · see citing works
Self-citationZhan, Y., Paolicelli, R. C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., Vyssotski, A. L., Bifone, A., Gozzi, A., Ragozzino, D., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3641 · Cited by 1,236 · see citing works
Human ApoE isoforms differentially regulate brain amyloid-β peptide clearance
Castellano, J. M., Kim, J., Stewart, F. R., Jiang, H., DeMattos, R. B., Patterson, B. W., Fagan, A. M., Morris, J. C., Mawuenyega, K. G., Cruchaga, C., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002156 · Cited by 1,227 · see citing works
Harrison, J. K., Jiang, Y., Chen, S., Xia, Y., Maciejewski, D., McNamara, R. K., Streit, W. J., Salafranca, M. N., Adhikari, S., Thompson, D. A., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10896 · Cited by 1,176 · see citing works
The Complement System: An Unexpected Role in Synaptic Pruning During Development and Disease
Stephan, A. H., Barres, B. A., & Stevens, B. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113810 · Cited by 1,113 · see citing works
Self-citationEmerging roles of astrocytes in neural circuit development
Clarke, L. E., & Barres, B. A. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3484 · Cited by 975 · see citing works
Self-citationInflammation in Alzheimer Disease--A Brief Review of the Basic Science and Clinical Literature
Wyss-Coray, T., & Rogers, J. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006346 · Cited by 975 · see citing works
Eroglu, Ç., Allen, N. J., Susman, M. W., O'Rourke, N. A., Park, C. Y., Özkan, E., Chakraborty, C., Mulinyawe, S. B., Annis, D. S., Huberman, A. D., et al. (2009) · Cell · doi:10.1016/j.cell.2009.09.025 · Cited by 893 · see citing works
Self-citationIntegrated Brain Circuits: Astrocytic Networks Modulate Neuronal Activity and Behavior
Halassa, M. M., & Haydon, P. G. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135843 · Cited by 835 · see citing works
GABA from reactive astrocytes impairs memory in mouse models of Alzheimer's disease
Jo, S., Yarishkin, O., Hwang, Y. J., Chun, Y. E., Park, M., Woo, D. H., Bae, J. Y., Kim, T., Lee, J., Chun, H., et al. (2014) · Nature Medicine · doi:10.1038/nm.3639 · Cited by 783 · see citing works
Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors
Allen, N. J., Bennett, M. L., Foo, L. C., Wang, G. X., Chakraborty, C., Smith, S. J., & Barres, B. A. (2012) · Nature · doi:10.1038/nature11059 · Cited by 764 · see citing works
Self-citationTREMs in the immune system and beyond
Colonna, M. (2003) · Nature Reviews Immunology · doi:10.1038/nri1106 · Cited by 701 · see citing works
Lian, H., Yang, L., Cole, A., Sun, L., Chiang, A. C.-A., Fowler, S. W., Shim, D. J., Rodriguez-Rivera, J., Taglialatela, G., Jankowsky, J. L., et al. (2015) · Neuron · doi:10.1016/j.neuron.2014.11.018 · Cited by 697 · see citing works
Paloneva, J., Manninen, T., Christman, G., Hovanes, K., Mandelin, J., Adolfsson, R., Bianchin, M., Bird, T., Miranda, R., Salmaggi, A., et al. (2002) · The American Journal of Human Genetics · doi:10.1086/342259 · Cited by 683 · see citing works
Jay, T. R., Miller, C. M., Cheng, P. J., Graham, L. C., Bemiller, S., Broihier, M. L., Xu, G., Margevicius, D., Karlo, J. C., Sousa, G. L., et al. (2015) · Journal of Experimental Medicine · doi:10.1084/jem.20142322 · Cited by 682 · see citing works
Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC
Kucukdereli, H., Allen, N. J., Lee, A. T., Feng, A., Ozlu, M. I., Conatser, L. M., Chakraborty, C., Workman, G., Weaver, M., Sage, E. H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104977108 · Cited by 642 · see citing works
Self-citationHan, X., Chen, M., Wang, F., Windrem, M., Wang, S., Shanz, S., Xu, Q., Oberheim, N. A., Bekar, L., Betstadt, S., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2012.12.015 · Cited by 635 · see citing works
CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity
Rogers, J. T., Morganti, J. M., Bachstetter, A. D., Hudson, C. E., Peters, M. M., Grimmig, B. A., Weeber, E. J., Bickford, P. C., & Gemma, C. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3667-11.2011 · Cited by 624 · see citing works
Wild-type microglia arrest pathology in a mouse model of Rett syndrome
Derecki, N. C., Cronk, J. C., Lu, Z., Xu, E., Abbott, S. B. G., Guyenet, P. G., & Kipnis, J. (2012) · Nature · doi:10.1038/nature10907 · Cited by 607 · see citing works
van Berckel, B. N. M., Bossong, M. G., Boellaard, R., Kloet, R. W., Schuitemaker, A., Caspers, E., Luurtsema, G., Windhorst, A. D., Cahn, W., Lammertsma, A. A., et al. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.04.025 · Cited by 582 · see citing works
Maternal infection and immune involvement in autism
Patterson, P. H. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2011.03.001 · Cited by 520 · see citing works
Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts
Paloneva, J., Kestilä, M., Wu, J., Salminen, A., Böhling, T., Ruotsalainen, V., Hakola, P., Bakker, A. B. H., Phillips, J. H., Pekkarinen, P., et al. (2000) · Nature Genetics · doi:10.1038/77153 · Cited by 460 · see citing works
A Dramatic Increase of C1q Protein in the CNS during Normal Aging
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., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1333-13.2013 · Cited by 423 · see citing works
Self-citationCooperative Astrocyte and Dendritic Spine Dynamics at Hippocampal Excitatory Synapses
Haber, M., Zhou, L., & Murai, K. K. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1302-06.2006 · Cited by 413 · see citing works
Structural Correlates of Cognition in Dementia: Quantification and Assessment of Synapse Change
DeKosky, S. T., Scheff, S. W., & Styren, S. D. (1996) · Neurodegeneration · doi:10.1006/neur.1996.0056 · Cited by 405 · see citing works
Rayaprolu, S., Mullen, B., Baker, M., Lynch, T., Finger, E., Seeley, W. W., Hatanpaa, K. J., Lomen-Hoerth, C., Kertesz, A., Bigio, E. H., et al. (2013) · Molecular Neurodegeneration · doi:10.1186/1750-1326-8-19 · Cited by 404 · see citing works
Absence of C1q Leads to Less Neuropathology in Transgenic Mouse Models of Alzheimer's Disease
Fonseca, M. I., Zhou, J., Botto, M., & Tenner, A. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0901-04.2004 · Cited by 345 · see citing works
Plasticity of Astrocytic Coverage and Glutamate Transporter Expression in Adult Mouse Cortex
Genoud, C., Quairiaux, C., Steiner, P., Hirling, H., Welker, E., & Knott, G. W. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040343 · Cited by 304 · see citing works
Altered microglial response to Aβ plaques in APPPS1-21 mice heterozygous for TREM2
Ulrich, J. D., Finn, M. B., Wang, Y., Shen, A., Mahan, T. E., Jiang, H., Stewart, F. R., Piccio, L., Colonna, M., & Holtzman, D. M. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-20 · Cited by 302 · see citing works
Astrocytic adenosine receptor A2A and Gs-coupled signaling regulate memory
Orr, A. G., Hsiao, E. C., Wang, M. M., Ho, K., Kim, D. H., Wang, X., Guo, W., Kang, J., Yu, G.-Q., Adame, A., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3930 · Cited by 289 · see citing works
Ammonia triggers neuronal disinhibition and seizures by impairing astrocyte potassium buffering
Thrane, V. R., Thrane, A. S., Wang, F., Cotrina, M. L., Smith, N., Chen, M. J., Xu, Q., Kang, N., Fujita, T., Nagelhus, E. A., et al. (2013) · Nature Medicine · doi:10.1038/nm.3400 · Cited by 265 · see citing works
Zhang, J., Malik, A., Choi, H. B., Ko, R. W. Y., Dissing-Olesen, L., & MacVicar, B. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.043 · Cited by 234 · see citing works
A Local Glutamate-Glutamine Cycle Sustains Synaptic Excitatory Transmitter Release
Tani, H., Dulla, C. G., Farzampour, Z., Taylor-Weiner, A. N., Huguenard, J. R., & Reimer, R. J. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.026 · Cited by 215 · see citing works
Wild-type microglia do not reverse pathology in mouse models of Rett syndrome
Wang, J., Wegener, E., Huang, T.-W., Sripathy, S. P., Jesús‐Cortés, H. D., Xu, P., Tran, S., Knobbe, W., Leko, V., Britt, J. K., et al. (2015) · Nature · doi:10.1038/nature14444 · Cited by 201 · see citing works
Complement activation by neurofibrillary tangles in Alzheimer's disease
Shen, Y., Lue, L.-F., Yang, L.-B., Roher, A., Kuo, Y.-M., Strohmeyer, R., Goux, W. J., Lee, V., Johnson, G. V. W., Webster, S. D., et al. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01842-0 · Cited by 185 · see citing works
Aida, T., Yoshida, J., Nomura, M., Tanimura, A., Iino, Y., Soma, M., Bai, N., Ito, Y., Cui, W., Aizawa, H., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.26 · Cited by 148 · see citing works
Ma, T., Abazyan, S., Abazyan, B., Nomura, J., Yang, C., Seshadri, S., Sawa, A., Snyder, S. H., & Pletnikov, M. V. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.97 · Cited by 147 · see citing works
Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function
Roumier, A., Pascual, O., Béchade, C., Wakselman, S., Poncer, J.-C., Réal, E., Triller, A., & Bessis, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002595 · Cited by 146 · see citing works
Hughes, E. G., Elmariah, S. B., & Balice‐Gordon, R. J. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.10.004 · Cited by 143 · see citing works
Neuronal Transgene Expression in Dominant-Negative SNARE Mice
Fujita, T., Chen, M. J., Li, B., Smith, N. A., Peng, W., Sun, W., Toner, M. J., Kress, B. T., Wang, L., Benraiss, A., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.2585-14.2014 · Cited by 141 · see citing works
Jones, E. V., Bernardinelli, Y., Tse, Y. C., Chierzi, S., Wong, T. P., & Murai, K. K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4757-10.2011 · Cited by 139 · see citing works
Matute, C., Melone, M., Vallejo‐Illarramendi, A., & Conti, F. (2005) · Glia · doi:10.1002/glia.20119 · Cited by 129 · see citing works
Chemokines and the hippocampus: A new perspective on hippocampal plasticity and vulnerability
Williamson, L. L., & Bilbo, S. D. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.01.077 · Cited by 121 · see citing works
Three‐dimensional relationships between perisynaptic astroglia and human hippocampal synapses
Witcher, M. R., Park, Y. D., Lee, M. R., Sharma, S., Harris, K. M., & Kirov, S. A. (2009) · Glia · doi:10.1002/glia.20946 · Cited by 115 · see citing works
Specific Glial Functions Contribute to Schizophrenia Susceptibility
Goudriaan, A., de Leeuw, C., Ripke, S., Hultman, C. M., Sklar, P., Sullivan, P. F., Smit, A. B., Posthuma, D., & Verheijen, M. H. G. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbt109 · Cited by 114 · see citing works
Complement activation and β-amyloid-mediated neurotoxicity in Alzheimer's disease
Rogers, J., Schultz, J., Brachova, L., Lue, L. F., Webster, S. M., Bradt, B. M., Cooper, N. R., & Moss, D. E. (1992) · Research in Immunology · doi:10.1016/0923-2494(92)80046-n · Cited by 81 · see citing works
Generating Human Neurons In Vitro and Using Them to Understand Neuropsychiatric Disease
Pașca, S. P., Panagiotakos, G., & Dolmetsch, R. E. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170328 · Cited by 64 · see citing works
Gabapentin decreases epileptiform discharges in a chronic model of neocortical trauma
Li, H., Graber, K., Jin, S., McDonald, W. S., Barres, B. A., & Prince, D. A. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.06.019 · Cited by 55 · see citing works
Self-citation<scp>APOE</scp> genotype affects the pre‐synaptic compartment of glutamatergic nerve terminals
Dumanis, S. B., DiBattista, A. M., Miessau, M., Moussa, C. E. H., & Rebeck, G. W. (2013) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07908.x · Cited by 55 · see citing works
Apoptotic Engulfment Pathway and Schizophrenia
Chen, X., Sun, C., Chen, Q., O’Neill, F. A., Walsh, D., Fanous, A. H., Chowdari, K. V., Nimgaonkar, V. L., Scott, A. P., Schwab, S. G., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006875 · Cited by 40 · see citing works
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Chronic Stress Weakens Connectivity in the Prefrontal Cortex: Architectural and Molecular Changes.
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Sun, X., Pan, S., Li, D., Su, M., Zheng, H., Zhang, Y.-W., & Li, Y. (2025) · The Journal of Neuroscience · doi:10.1523/jneurosci.0967-24.2025 · Cited by 4 · see citing works
- Authors
- Chung, W.-S., Welsh, C. A., Barres, B. A., & Stevens, B.
- Affiliations
- Stanford Medicine (US)
- Boston Children's Hospital (US)
- Corresponding author
- Stevens, Beth
- Venue
- Nature Neuroscience
- Published
- 2015-10-27
- Volume
- 18
- Issue
- 11
- Pages
- 1539-1545
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4739631
- OpenAlex
- W1876773427
- Cited by
- 385
- References
- 80
- Citations by year
- 2026: 10 · 2025: 15 · 2024: 26 · 2023: 36 · 2022: 31 · 2021: 43 · 2020: 41 · 2019: 58 · 2018: 41 · 2017: 47 · 2016: 36 · 2015: 1
- FWCI
- 3.32
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (T32AG000222)
- National Institute of Neurological Disorders and Stroke (R01NS071008)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- glia, neuron-glia signaling, synaptic dysfunction, cognitive impairment, neuroinflammation, reactive gliosis, synaptic plasticity, neurodegenerative diseases, mental illness, contact-dependent signaling, biomarkers
- MeSH terms
- Animals, Astrocytes, Cognition Disorders, Humans, Synaptic Transmission, Neuroglia, Neuronal Plasticity, Neurons
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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