Regulation of synaptic connectivity by glia.
Open accessAbstract
The human brain contains more than 100 trillion (10(14)) synaptic connections, which form all of its neural circuits. Neuroscientists have long been interested in how this complex synaptic web is weaved during development and remodelled during learning and disease. Recent studies have uncovered that glial cells are important regulators of synaptic connectivity. These cells are far more active than was previously thought and are powerful controllers of synapse formation, function, plasticity and elimination, both in health and disease. Understanding how signalling between glia and neurons regulates synaptic development will offer new insight into how the nervous system works and provide new targets for the treatment of neurological diseases.
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Astrocytes are directly involved in synaptic connections and control, ranging from ionic balance to the genesis and behavior of synapses.
“Evidence now shows that astrocytes are directly involved in synaptic connections and control, ranging from ionic balance to the genesis and behavior of synapses”
From Interlaminar and varicose-projection astrocytes: toward a new understanding of the primate brain (2024) · cites this paper as Eroglu and Barres, 2010
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Taniguchi, H., Gollan, L., Scholl, F. G., Mahadomrongkul, V., Dobler, E., Limthong, N., Peck, M., Aoki, C. J., & Scheiffele, P. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0032-07.2007 · Cited by 144 · cited 1× · see citing works
“, where neurexin functions as an inhibitor of synapse formation by interacting in cis with the postsynaptic adhesion molecule neuroligi”
BackgroundHughes, 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 · cited 1× · see citing works
“TSP1 did not induce inhibitory synapse formation in this culture system, although it facilitated excitatory synapse formation and neurite outgrowt”
BackgroundIndependent mechanisms for long-term depression of AMPA and NMDA responses.
Selig, D. K., Hjelmstad, G., Herron, C., Nicoll, R., & Malenka, R. (1995) · Neuron · doi:10.1016/0896-6273(95)90045-4 · Cited by 137 · cited 1× · see citing works
“The main mechanisms regulating these processes involved in plasticity are thought to be changes in the cell-surface delivery, retention and Ca 2+ -channel properties of the postsynaptic ionotropic glutamate receptors, AMPA receptors and NMDA ( N -methyl- D -aspartate) receptor”
BackgroundIntegrin-Mediated Regulation of Synaptic Morphology, Transmission, and Plasticity
Rohrbough, J., Grotewiel, M., Davis, R. L., & Broadie, K. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-18-06868.2000 · Cited by 135 · see citing works
Valder, C. R., Liu, J.-J., Song, Y.-H., & Luo, Z. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02016.x · Cited by 120 · see citing works
Presynaptic α2δ-3 is required for synaptic morphogenesis independent of its Ca2+ - channel functions
Kurshan, P. T., Oztan, A., & Schwarz, T. (2009) · Nature Neuroscience · doi:10.1038/nn.2417 · Cited by 119 · cited 1× · see citing works
“Moreover, a Drosophila homologue of α2δ-1, Cacna2d3, is required for presynaptic maturation at the neuromuscular junctio”
BackgroundD‐Serine as a glial modulator of nerve cells
Miller, R. F. (2004) · Glia · doi:10.1002/glia.20073 · Cited by 116 · cited 1× · see citing works
“The amino acid D -serine, which is produced exclusively by astrocytes, is a potent agonist for this sit”
BackgroundIncreased Cortical Expression of Two Synaptogenic Thrombospondins in Human Brain Evolution
Cáceres, M., Suwyn, C. R., Maddox, M., Thomas, J. W., & Preuss, T. M. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl140 · Cited by 114 · cited 1× · see citing works
“Interestingly, two isoforms of TSP (TSP2 and TSP4) are among the few genes that are substantially upregulated in the human brain compared with the primate and mouse brai”
BackgroundSeeking long‐term relationship: axon and target communicate to organize synaptic differentiation
Fox, M. A., & Umemori, H. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03834.x · Cited by 107 · see citing works
Lysosomal Activity Associated with Developmental Axon Pruning
Song, J. W., Misgeld, T., Kang, H., Knecht, S., Lu, J., Cao, Y., Cotman, S. L., Bishop, D. L., & Lichtman, J. W. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0720-08.2008 · Cited by 107 · cited 1× · see citing works
“This experiment directly showed that axosome shedding occurs entirely within the confines of Schwann cells and depends on glial lysosome functio”
BackgroundUrade, Y., Oberdick, J., Molinar-Rode, R., & Morgan, J. I. (1991) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.88.3.1069 · Cited by 105 · cited 1× · see citing works
“Interestingly, homologues of C1q, such as precerebellin”
Iijima, T., Miura, E., Watanabe, M., & Yuzaki, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07202.x · Cited by 101 · see citing works
Purinergic signaling induces thrombospondin-1 expression in astrocytes
Tran, M. D., & Neary, J. T. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603146103 · Cited by 100 · see citing works
Physiological characteristics of NG2-expressing glial cells
Lin, S.-C., & Bergles, D. (2002) · Journal of Neurocytology · doi:10.1023/a:1025799816285 · Cited by 96 · cited 1× · see citing works
“In addition, a new class of glial cell, oligodendrocyte precursor cells (OPCs) that express the proteoglycan NG2, has recently been identified and has morphological and physiological features that are distinct from those of other gli”
BackgroundSculpting the nervous system: glial control of neuronal development
Freeman, M. R. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.12.004 · Cited by 94 · cited 1× · see citing works
“Developmental axon pruning is widely used in Drosophila metamorphosis, which involves major pruning events that require the breakdown and reconstruction of synaptic network”
MethodNeurotrophin signaling among neurons and glia during formation of tripartite synapses
Elmariah, S. B., Hughes, E. G., Oh, E. J., & Balice‐Gordon, R. J. (2004) · Neuron Glia Biology · doi:10.1017/s1740925x05000189 · Cited by 85 · cited 1× · see citing works
“They do this by modulating inhibitory postsynaptic development, by stimulating neuron–neuron signalling through the neurotrophic receptor tyrosine kinase Trk”
BackgroundDevelopmental Control of Synaptic Receptivity
Barker, A., Koch, S. M., Reed, J., Barres, B., & Ullian, E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1744-08.2008 · Cited by 80 · cited 1× · see citing works
“In the retina, there is a developmental switch in which the ability of RGCs to respond to soluble synaptogenic signals from astrocytes is induced by contact with astrocytes themselve”
BackgroundSelf-citationTheodosis, D. T., Koksma, J.-J., Trailin, A., Langle, S. L., Piet, R., Lodder, J. C., Timmerman, J. A., Mansvelder, H., Poulain, D., Oliet, S., et al. (2006) · Molecular and cellular neurosciences · doi:10.1016/j.mcn.2006.01.006 · Cited by 65 · see citing works
Neuronal Pentraxins Mediate Silent Synapse Conversion in the Developing Visual System
Koch, S. M., & Ullian, E. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4893-09.2010 · Cited by 55 · see citing works
Structural and functional organization of the synapse
Hell, J., & Ehlers, M. (2008) · Springer eBooks · doi:10.1007/978-0-387-77232-5 · Cited by 52 · see citing works
Look who is weaving the neural web: glial control of synapse formation
Bolton, M. M., & Eroğlu, Ç. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.09.007 · Cited by 50 · cited 1× · see citing works
“But the functions of glia are not restricted to supporting neuronal functio”
BackgroundSelf-citationSchwann Cell-Derived Factors Modulate Synaptic Activities at Developing Neuromuscular Synapses
Cao, G., & Ko, C. P. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1329-07.2007 · Cited by 42 · see citing works
Neuronal glia interactions at the vertebrate neuromuscular junction.
Feng, Z., & Ko, C.-P. (2007) · Current opinion in pharmacology (Print) · doi:10.1016/j.coph.2006.12.003 · Cited by 33 · cited 1×
“In the peripheral nervous system, there are two classes of Schwann cell (myelinating and non-myelinating), which functionally and antigenically resemble the glia of the CN”
BackgroundBuckby, L. E., Jensen, T. P., Smith, P. J. E., & Empson, R. M. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.01.009 · Cited by 32 · see citing works
Modulation of synaptic transmission by astrocytes in the rat supraoptic nucleus.
Piet, R., Poulain, D., & Oliet, S. (2002) · Journal of Physiology - Paris · doi:10.1016/s0928-4257(02)00010-4 · Cited by 25 · cited 1× · see citing works
“Concurrently, new inhibitory and excitatory synapses are formed onto these neurons, and these disappear when stimulation ends and the astrocyte processes reinnervate these oxytocinergic neuron”
BackgroundGlia as Active Participants in the Development and Function of Synapses
Eroğlu, Ç., Barres, B. A., & Stevens, B. (2008) · Springer eBooks · doi:10.1007/978-0-387-77232-5_23 · Cited by 17 · see citing works
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5 of the 104 references couldn’t be matched to a known paper.
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Neuroinflammation and microglial activation in Alzheimer disease: where do we go from here?
Leng, F., & Edison, P. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-020-00435-y · Cited by 3,179 · see citing works
Variation in cancer risk among tissues can be explained by the number of stem cell divisions
Tomasetti, C., & Vogelstein, B. (2015) · Science · doi:10.1126/science.1260825 · Cited by 1,927 · see citing works
“Astrocytes are derived from neural stem cells (79), whose proportion has been estimated to be ~0.”
BackgroundVerkhratsky, A., & Nedergaard, M. (2018) · Physiological Reviews · doi:10.1152/physrev.00042.2016 · Cited by 1,678 · see citing works
Diversity of astrocyte functions and phenotypes in neural circuits
Khakh, B. S., & Sofroniew, M. V. (2015) · Nature Neuroscience · doi:10.1038/nn.4043 · Cited by 1,239 · 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
“Immature astrocytes secrete an array of cytokines and other molecules that promote synapse formation and synaptic plasticity (Allen & Barres 2005, Bolton & Eroglu 2009, Eroglu & Barres 2010).”
BackgroundSelf-citationInnate immunity in the central nervous system
Ransohoff, R. M., & Brown, M. A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58644 · Cited by 1,034 · see citing works
Inflammation in CNS neurodegenerative diseases
Stephenson, J., Nutma, E., van der Valk, P., & Amor, S. (2018) · Immunology · doi:10.1111/imm.12922 · Cited by 966 · see citing works
Astrocyte reactivity and reactive astrogliosis: costs and benefits
Pekny, M., & Pekna, M. (2014) · Physiological Reviews · doi:10.1152/physrev.00041.2013 · Cited by 934 · see citing works
“Astrocytes were shown to control formation, maintenance, function, and removal of neuronal synapses (45, 68, 168, 228, 237, 238); help to control blood flow (104, 120, 153, 207, 276); and together with pericytes regulate the bloodbrain barrier (1, 11, 17, 133).”
BackgroundThe Journal of Clinical Investigation
Witkin, E. M. (2016) · Journal of the American Dietetic Association · doi:10.1016/0002-8223(94)92394-9 · Cited by 920 · see citing works
Novel electrode technologies for neural recordings
Hong, G., & Lieber, C. M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0140-6 · Cited by 695 · see citing works
The dual role of astrocyte activation and reactive gliosis
Pekny, M., Wilhelmsson, U., & Pekna, M. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2013.12.071 · Cited by 666 · 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
“Astrocyte ensheathment of excitatory synapses is thought to be critical for the stability andmaturation of the synapse (2).”
BackgroundSelf-citationThe Cell Biology of Synaptic Plasticity
Ho, V. M., Lee, J.-A., & Martin, K. C. (2011) · Science · doi:10.1126/science.1209236 · Cited by 573 · see citing works
The immune system and developmental programming of brain and behavior
Bilbo, S. D., & Schwarz, J. M. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.08.006 · Cited by 579 · see citing works
“Astrocytes have a crucial function in synaptogenesis and synaptic scaling, through the release of diffusible factors and the production of extracellular matrix proteins (see [86] for review).”
BackgroundLocal generation of glia is a major astrocyte source in postnatal cortex
Ge, W.-P., Miyawaki, A., Gage, F. H., Jan, Y. N., & Jan, L. Y. (2012) · Nature · doi:10.1038/nature10959 · Cited by 507 · see citing works
Theories of pain: from specificity to gate control.
Moayedi, M., & Davis, K. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00457.2012 · Cited by 503 · see citing works
Modeling Alzheimer’s disease with iPSC-derived brain cells
Penney, J., Ralvenius, W. T., & Tsai, L.-H. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0468-3 · Cited by 471 · see citing works
Isolation and Culture of Mouse Cortical Astrocytes
Schildge, S., Bohrer, C., Beck, K., & Schachtrup, K. (2013) · Journal of Visualized Experiments · doi:10.3791/50079 · Cited by 453 · see citing works
Cell biology of spinal cord injury and repair
O’Shea, T. M., Burda, J. E., & Sofroniew, M. V. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90608 · Cited by 590 · see citing works
Astrocytes in chronic pain and itch
Ji, R., Donnelly, C. R., & Nedergaard, M. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0218-1 · Cited by 553 · see citing works
An Efficient Platform for Astrocyte Differentiation from Human Induced Pluripotent Stem Cells
TCW, J., Wang, M., Pimenova, A. A., Bowles, K. R., Hartley, B. J., Lacin, E., Machlovi, S. I., Abdelaal, R., Karch, C. M., Phatnani, H., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.06.018 · Cited by 435 · see citing works
“Within the human brain, astrocytes have a variety of essential functions including glutamate biology, axonal guidance, trophic support, inflammatory response and wound healing, formation of the blood-brain barrier, and neuronal synapse formation, and plasticity (Barres, 2008; Eroglu and Barres, 2010; Freeman and Rowit…”
BackgroundDevelopment of a Method for the Purification and Culture of Rodent Astrocytes
Foo, L. C., Allen, N. J., Bushong, E. A., Ventura, P. B., Chung, W.-S., Zhou, L., Cahoy, J. D., Daneman, R., Zong, H., Ellisman, M. H., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.022 · Cited by 433 · see citing works
Self-citationNeuron–glia interactions in the pathophysiology of epilepsy
Patel, D. C., Tewari, B. P., Chaunsali, L., & Sontheimer, H. W. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0126-4 · Cited by 461 · see citing works
Shigetomi, E., Bushong, E. A., Haustein, M. D., Tong, X., Jackson‐Weaver, O., Kracun, S., Xu, J. P., Sofroniew, M. V., Ellisman, M. H., & Khakh, B. S. (2013) · The Journal of General Physiology · doi:10.1085/jgp.201210949 · Cited by 378 · see citing works
“We are particularly excited by a new possibility raised by our work, namely that the equally sized Ca microdomains (in terms of dF/F), with spacing independent of location within an astrocyte’s territory, may be adept at locally restricted regulation of vital contributions of astrocytes in the functioning of the brain…”
BackgroundAstrocytes Mediate In Vivo Cholinergic-Induced Synaptic Plasticity
Navarrete, M., Perea, G., de Sevilla, D. F., Gómez-Gonzalo, M., Núñez, A., Martín, E. D., & Araque, A. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001259 · Cited by 387 · see citing works
“function [1–4].”
Neuronal Exosomal miRNA-dependent Translational Regulation of Astroglial Glutamate Transporter GLT1
Morel, L., Regan, M., Higashimori, H., Ng, S. K., Esau, C., Vidensky, S., Rothstein, J., & Yang, Y. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.410944 · Cited by 390 · see citing works
“Because astrocytes are known to release various signals tomodulate synaptic/neuronal functions (49, 50) and survival (51, 52), it is likely that astroglial exosomes may also play a modulatory role in synaptic functions.”
BackgroundAstrocyte Heterogeneity: Impact to Brain Aging and Disease
Matias, I., Morgado, J., & Gomes, F. C. A. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00059 · Cited by 387 · see citing works
González, H., Elgueta, D., Montoya, A., & Pacheco, R. (2014) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2014.07.012 · Cited by 352 · see citing works
“Regarding homeostatic functions of astrocytes, they exert several effects in the healthy brain to support physiological processes, such as the control and formation of neuronal synapses (Eroglu and Barres, 2010), turnover of neurotransmitters (Haydon and Carmignoto, 2006), control of neuronal energy (Rouach et al.”
BackgroundMairet-Coello, G., Courchet, J., Pieraut, S., Courchet, V., Maximov, A., & Polleux, F. (2013) · Neuron · doi:10.1016/j.neuron.2013.02.003 · Cited by 351 · see citing works
“synaptotoxic effects of Ab42 in culture, they did not allow to conclude if CAMKK2 acts pre- or postsynaptically, or even indirectly by acting on nonneuronal cells such as astrocytes, which are critically important for synapse formation and maintenance (Eroglu and Barres, 2010).”
Human Astrocytes Transfer Aggregated Alpha-Synuclein via Tunneling Nanotubes
Rostami, J., Holmqvist, S., Lindström, V., Sigvardson, J., Westermark, G. T., Ingelsson, M., Bergström, J., Roybon, L., & Erlandsson, A. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.0983-17.2017 · Cited by 339 · see citing works
Circuit-specific signaling in astrocyte-neuron networks in basal ganglia pathways
Martín, R., Bajo-Grañeras, R., Moratalla, R., Perea, G., & Araque, A. (2015) · Science · doi:10.1126/science.aaa7945 · Cited by 312 · see citing works
Artifact versus reality—How astrocytes contribute to synaptic events
Nedergaard, M., & Verkhratsky, A. (2012) · Glia · doi:10.1002/glia.22288 · Cited by 304 · see citing works
“A (Eroglu and Barres, 2010), B (Gordon and Bains 2006), C (Koizumi et al., 2005), D (Nadkarni et al., 2008) E (Allen and Barres 2009), F (Sotero and Martinez-Cancino 2010).”
Improved tools to study astrocytes
Yu, X., Nagai, J., & Khakh, B. S. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0264-8 · Cited by 298 · see citing works
Genes, circuits, and precision therapies for autism and related neurodevelopmental disorders
Sahin, M., & Sur, M. (2015) · Science · doi:10.1126/science.aab3897 · Cited by 295 · see citing works
“Astrocyte processes extend into excitatory synapses, and they influence synaptic development (95) and synaptic transmission via uptake of glutamate (96) as well as by calcium-mediated alterations in synaptic function and plasticity (97, 98).”
BackgroundEvaluating cell reprogramming, differentiation and conversion technologies in neuroscience
Mertens, J., Marchetto, M. C., Bardy, C., & Gage, F. H. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.46 · Cited by 301 · see citing works
Generation of vascularized brain organoids to study neurovascular interactions
Sun, X., Ju, X.-C., Li, Y., Zeng, P.-M., Wu, J., Zhou, Y.-Y., Shen, L., Dong, J., Chen, Y., & Luo, Z. (2022) · bioRxiv · doi:10.1101/2022.01.04.474960 · Cited by 292
Behaviorally consequential astrocytic regulation of neural circuits
Nagai, J., Yu, X., Papouin, T., Cheong, E., Freeman, M. R., Monk, K. R., Hastings, M. H., Haydon, P. G., Rowitch, D. H., Shaham, S., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.12.008 · Cited by 311 · see citing works
Weissberg, I., Wood, L., Kamintsky, L., Vazquez, O. N., Milikovsky, D. Z., Alexander, A., Oppenheim, H., Ardizzone, C., Becker, A. J., Frigerio, F., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.02.029 · Cited by 285 · see citing works
Glial and Neuroimmune Mechanisms as Critical Modulators of Drug Use and Abuse
Lacagnina, M. J., Rivera, P. D., & Bilbo, S. D. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.121 · Cited by 271 · see citing works
“…astrocytes can actively regulate many aspects of neuronal function, including neurotransmitter release, gene regulation, electrophysiology, dendritic morphology, synaptic connectivity, and cell viability (Araque et al, 2014; Eroglu and Barres, 2010; Kettenmann et al, 2013; Salter and Beggs, 2014).”
BackgroundSöllvander, S., Nikitidou, E., Brolin, R., Söderberg, L., Sehlin, D., Lannfelt, L., & Erlandsson, A. (2016) · Molecular Neurodegeneration · doi:10.1186/s13024-016-0098-z · Cited by 267 · see citing works
“Their functions include metabolic support of neurons, modification of synapse signaling, recycling of neurotransmittors, regulation of blood flow and contribution to the blood brain barrier [2, 3].”
BackgroundAstroglial cradle in the life of the synapse
Verkhratsky, A., & Nedergaard, M. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0595 · Cited by 266 · see citing works
Xiao, Q., Yan, P., Ma, X., Liu, H., Perez, R., Zhu, A., Gonzales, E., Burchett, J. M., Schuler, D. R., Cirrito, J. R., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3788-13.2014 · Cited by 266 · see citing works
“Astrocytes are the most abundant cell type in the brain and play a critical role in maintaining synaptic transmission and neuronal health in homeostasis (Eroglu and Barres, 2010).”
BackgroundBi, D., Wen, L., Wu, Z., & Shen, Y. (2020) · Alzheimer's & Dementia · doi:10.1002/alz.12088 · Cited by 232 · see citing works
Nehme, R., Zuccaro, E., Ghosh, S. D., Li, C., Sherwood, J. L., Pietiläinen, O. P. H., Barrett, L. E., Limone, F., Worringer, K. A., Kommineni, S., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.04.066 · Cited by 242 · see citing works
“Consistent with previous reports that glial cells promote neuronal maturation and synaptic activity (Pfrieger, 2009; Eroglu and Barres, 2010; Tang et al., 2013), we found that co-culturing the stem cell-derived neurons with mouse glia resulted in an increase in firing, as well as in synchronous…”
BackgroundReactive gliosis in the pathogenesis of CNS diseases
Pekny, M., & Pekna, M. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.11.014 · Cited by 276 · see citing works
Sex, glia, and development: Interactions in health and disease
Schwarz, J. M., & Bilbo, S. D. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.02.018 · Cited by 247 · see citing works
“Astrocytes have an important function in synaptogenesis and synaptic scaling, either through the release of diffusible factors or the production of extracellular matrix proteins [see (Eroglu and Barres, 2010) for review}.”
Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo
Perea, G., Yang, A., Boyden, E. S., & Sur, M. (2014) · Nature Communications · doi:10.1038/ncomms4262 · Cited by 236 · see citing works
“5a, see Methods Equation (2)) but little change in complementary parameters such as the tuning width.”
BackgroundMethodInfluentialMolecular and Functional Properties of Regional Astrocytes in the Adult Brain
Morel, L., Chiang, M. S. R., Higashimori, H., Shoneye, T., Iyer, L. K., Yelick, J., Tai, A., & Yang, Y. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3956-16.2017 · Cited by 243 · see citing works
Signalling pathways in autism spectrum disorder: mechanisms and therapeutic implications
Jiang, C.-C., Lin, L., Long, S., Ke, X., Fukunaga, K., Lu, Y., & Han, F. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01081-0 · Cited by 272 · see citing works
Liang, Q., Fujita, R., Yamashita, T., Angulo, S. L., Rhinn, H., Rhee, D. B., Doege, C. A., Chau, L., Aubry, L., Vanti, W. B., et al. (2011) · Cell · doi:10.1016/j.cell.2011.07.007 · Cited by 230 · see citing works
“First, as glial cells can play a major role in the regulation of neuronal synaptic development and connectivity (Eroglu and Barres, 2010), hiN cells were cocultured with murine glial cells (obtained from mice ubiquitously expressing red fluorescent protein) (Muzumdar et al.”
RetractedSanacora, G., & Banasr, M. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.032 · Cited by 239 · see citing works
“Disrupted function of any of these cell types is likely to alter normal brain function and possibly contribute to the development of neuropsychiatric disorders (4).”
BackgroundAstrocytes: Orchestrating synaptic plasticity?
Pittà, M. D., Brunel, N., & Volterra, A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.001 · Cited by 263 · see citing works
Infectious immunity in the central nervous system and brain function
Klein, R. S., Garber, C., & Howard, N. (2017) · Nature Immunology · doi:10.1038/ni.3656 · Cited by 235 · see citing works
Myelination, oligodendrocytes, and serious mental illness
Haroutunian, V. H., Katsel, P., Roussos, P., Davis, K. L., Altshuler, L. L., & Bartzokis, G. (2014) · Glia · doi:10.1002/glia.22716 · Cited by 247 · see citing works
Andersen, J. V., Schousboe, A., & Verkhratsky, A. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102331 · Cited by 259 · see citing works
Astrocyte glutamine synthetase: pivotal in health and disease
Rose, C. F., Verkhratsky, A., & Parpura, V. (2013) · Biochemical Society Transactions · doi:10.1042/bst20130237 · Cited by 224 · see citing works
“Astroglial cells are fundamental for brain development being, for example, chief promoters and supporters of synaptogenesis, synaptic maturation and maintenance ([13,14]).”
BackgroundContrasting the Glial Response to Axon Injury in the Central and Peripheral Nervous Systems
Lutz, A. B., & Barres, B. A. (2014) · Developmental Cell · doi:10.1016/j.devcel.2013.12.002 · Cited by 229 · see citing works
Self-citationInnate immunity at the crossroads of healthy brain maturation and neurodevelopmental disorders
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BackgroundSTAT3-dependent reactive astrogliosis in the spinal dorsal horn underlies chronic itch
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“By contrast, however, the formation of functional synapses requires factors secreted by glial cells (Banker, 1980; Eroglu and Barres, 2010; Wu et al, 2007).”
BackgroundNeuronal exosomes facilitate synaptic pruning by up-regulating complement factors in microglia
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“Progress in the field has been comprehensively covered in many outstanding recent reviews (Aguzzi et al., 2013; Attwell et al., 2010; Emery, 2010; Eroglu and Barres, 2010; Freeman, 2010; Molofsky et al., 2012; Nave, 2010).”
Current Advancements in Spinal Cord Injury Research—Glial Scar Formation and Neural Regeneration
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“…recent evidence suggests that glial cells might represent a critical third element of the synapse in addition to the preand the postsynaptic neurons (Eroglu and Barres, 2010) and that immune diffusible mediators such as pro-inflammatory cytokines may play a central role in neuronal-network…”
Stratified medicine for mental disorders
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“These include astrocytes and microglia as well as modulatory influences of peripheral cells such as immune cells (Eroglu and Barres, 2010; Graeber, 2010; Miller et al., 2009).”
BackgroundKim, Y. H., Park, J., & Choi, Y. K. (2019) · Antioxidants · doi:10.3390/antiox8050121 · Cited by 203 · see citing works
“Astrocytes not only regulate blood flow, but also transfer mitochondria to neurons, and supply the building blocks of neurotransmitters, which fuel neuronal metabolism [2,11,57].”
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“On the other hand, it can also handle the formation of synapses (Ullian et al., 2001, 2004; Eroglu and Barres, 2010) and the energy supply of neurons.”
BackgroundHow many neurons do you have? Some dogmas of quantitative neuroscience under revision
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“In adults, they play important roles in synapse physiology (Eroglu & Barres, 2010), neurovascular interactions (Nedergaard et al., 2003), immune mechanisms and circuit stabilization (Graeber, 2010), signal conduction (Yamazaki et al., 2010), fiber maintenance and regeneration (Nave, 2010), and…”
BackgroundCortical astrocytes rewire somatosensory cortical circuits for peripheral neuropathic pain
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“It is well appreciated that glial cells not only play crucial supportive roles in the development and maintenance of neuronal structures, but that they also actively communicate with neurons to enable synapse formation, synaptic transmission, plasticity and synaptic homeostasis [37,38].”
BackgroundMetal ions as modulators of protein conformation and misfolding in neurodegeneration
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BackgroundAstrocytes refine cortical connectivity at dendritic spines
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“Soluble oligomers of the amyloid- peptide (A Os) accumulate in AD brains (Gong et al., 2003) and are increasingly considered major toxins leading to neuronal dysfunction in AD (Ferreira and Klein, 2011; Mucke and Selkoe, 2012; Hong et al., 2016).”
BackgroundMesh electronics: a new paradigm for tissue-like brain probes
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“Third, brain tissue comprises organized 3D networks of neurons and non-neuronal cells, such as astrocytes and microglia, which impacts two major points for probe design: firstly, The probe structure should not disrupt the 3D connectivity where each neuron is innervated by as many as 10 000 presynaptic endings [6]; sec…”
The interplay between neurons and glia in synapse development and plasticity
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“Glia control the formation of synaptic circuits In the CNS, glial cells are in tight association with synapses in all brain regions [2].”
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“In this context, astrocytes release neuroactive molecules (such as glutamate, ATP, nitric oxide, prostaglandins, and D-serine) in the presence of elevated Ca2+, which in turn influence neuronal excitability (Araque et al., 1999; Perea et al., 2009; Eroglu and Barres, 2010).”
BackgroundMorphological plasticity of astroglia: Understanding synaptic microenvironment
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“However, the cellular architectural basis and the molecular machinery that are causal to physiological and morphogenetic events inside PAPs remain an enigma.”
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“Previous studies have demonstrated that glial cells are fundamentally important for neuronal synapse formation and plasticity (Banker, 1980; Haydon, 2001; Yang et al., 2003; Hama et al., 2004; Barres, 2008; Eroglu and Barres, 2010).”
Neuron-Glia Interactions in Neurodevelopmental Disorders
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“However, some studies have reported that several functions of glia contribute to the pathogenesis of epilepsy [44,45].”
BackgroundHuntingtin Is Required for Normal Excitatory Synapse Development in Cortical and Striatal Circuits
McKinstry, S. U., Karadeniz, Y., Worthington, A. K., Hayrapetyan, V. Y., Ozlu, M. I., Serafin-Molina, K., Risher, W. C., Ustunkaya, T., Dragatsis, I., Zeitlin, S. O., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4699-13.2014 · Cited by 152 · see citing works
“Two classes of glial cells, astrocytes and microglia, are known to play critical roles in regulating synaptic development and homeostasis (Eroglu and Barres, 2010).”
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Genetics of human brain development
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“However, astrocytes are the largest glial cell population within the brain, and their role in synaptic plasticity mechanisms is now well accepted (reviewed in Eroglu and Barres 2010).”
BackgroundMitochondria as a centrally positioned hub in the innate immune response
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- Authors
- Eroglu, C., & Barres, B. A.
- Affiliations
- Stanford Medicine (US)
- ORCID
- Barres, Ben A.
- Venue
- Nature
- Published
- 2010-11
- Volume
- 468
- Issue
- 7321
- Pages
- 223-231
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4431554
- OpenAlex
- W1973477241
- Cited by
- 813
- References
- 104
- Citations by year
- 2026: 21 · 2025: 46 · 2024: 48 · 2023: 52 · 2022: 54 · 2021: 60 · 2020: 52 · 2019: 52 · 2018: 66 · 2017: 54 · 2016: 50 · 2015: 50 · 2014: 55 · 2013: 58 · 2012: 58
- FWCI
- 4.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Alfred P. Sloan Foundation
- National Institute on Drug Abuse (R01DA015043)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- glial cells, synaptic connectivity, synaptogenesis, synaptic pruning, synaptic plasticity, synaptic development, learning, neurological disorders
- MeSH terms
- Animals, Axons, Central Nervous System Diseases, Drosophila melanogaster, Humans, Synaptic Transmission, Neuroglia, Synapses
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