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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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“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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Citations
Cites
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BackgroundAstroglial atrophy in Alzheimer’s disease
Verkhratsky, A., Rodriguez, J. J., Pivoriūnas, A., Zorec, R., & Semyanov, A. V. (2019) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-019-02310-2 · Cited by 150
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“Because neurotransmission and synaptic connectivity are dynamically regulated (28, 35), dynamic sialylation observed in this study may play an important role in these processes.”
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“For example, astrocytes and microglia interact with neurons at the synapse to modulate synaptic function and plasticity (Eroglu and Barres, 2010; Tremblay et al., 2011) and are also vital for host defense mechanisms and response to stress (Ransohoff and Perry, 2009).”
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“Astrocytes have a crucial role in synaptogenesis and maintenance of synapses (Eroglu and Barres, 2010; Verkhratsky and Nedergaard, 2014).”
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YAP Is a Critical Inducer of SOCS3, Preventing Reactive Astrogliosis
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Lipid Metabolism and Glial Lipoproteins in the Central Nervous System
Hayashi, H. (2011) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.34.453 · Cited by 80
Gut-Brain Axis in the Early Postnatal Years of Life: A Developmental Perspective
Jena, A., Montoya, C. A., Mullaney, J. A., Dilger, R. N., Young, W., McNabb, W. C., & Roy, N. C. (2020) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2020.00044 · Cited by 98
“, section “Immune Mediators”) astrocytes support formation and plasticity of the synapse while the oligodendrocytes form myelin (Eroglu and Barres, 2010).”
BackgroundPitt, J. E., Wilcox, K. C., Tortelli, V., Diniz, L. P., Oliveira, M. S., Dobbins, C., Yu, X., Nandamuri, S., Gomes, F. C. A., DiNunno, N., et al. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-06-0416 · Cited by 87
“We focused on astrocytes because of their well-established trophic functions (Chernausek, 1993; Grunblatt et al., 2007; Eroglu and Barres, 2010; Diniz et al., 2014).”
BackgroundControl of immune-mediated pathology via the aryl hydrocarbon receptor
Wheeler, M. A., Rothhammer, V., & Quintana, F. J. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.767723 · Cited by 95
Kozłowska, U., Nichols, C. D., Wiatr, K., & Figiel, M. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15509 · Cited by 86
“Errors in this process during childhood may lead to the development of autism, schizophrenia, or mental retardation, and in adult also result in degenerative diseases (Eroglu & Barres, 2010; Presumey et al., 2017).”
BackgroundBioinspired Materials for In Vivo Bioelectronic Neural Interfaces
Woods, G. A., Rommelfanger, N. J., & Hong, G. (2020) · Matter · doi:10.1016/j.matt.2020.08.002 · Cited by 89
Zhang, M., Piskuric, N. A., Vollmer, C., & Nurse, C. (2012) · Journal of Physiology · doi:10.1113/jphysiol.2012.236265 · Cited by 76
“Indeed, in the central nervous system (CNS), glial cells are now known to play an active role in synapse integration and may act as modulators of synaptic transmission via gliotransmission at tripartite synapses (Eroglu & Barres, 2010; Parpura et al. 2012).”
BackgroundAstrocyte regulation of synaptic signaling in psychiatric disorders
Kruyer, A., Kalivas, P. W., & Scofield, M. D. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01338-w · Cited by 83
“Accordingly, reorganization of astroglial morphology can have a direct impact on the profile of synaptic and extrasynaptic neurotransmitter receptor activation during synaptic transmission, with severe retraction allowing glutamate to engage in inter-synaptic signaling [53, 56].”
BackgroundTakahashi, S. (2020) · Neuropathology · doi:10.1111/neup.12639 · Cited by 77
“Thus, synapses composed of presynaptic and postsynaptic neurons as well as astroglial end-feet are known as tripartite synapses.(4,5,8,9) Moreover, astroglial cells are connected to each other via gap junctions with connexin 43 channels, forming a functional syncytium overall.”
BackgroundMethodAstroglial Responses to Amyloid-Beta Progression in a Mouse Model of Alzheimer’s Disease
Olsen, M., Aguilar, X., Sehlin, D., Fang, X. T., Antoni, G., Erlandsson, A., & Syvänen, S. (2018) · Molecular Imaging and Biology · doi:10.1007/s11307-017-1153-z · Cited by 80
The tripartite glutamatergic synapse
Lalo, U., Koh, W., Lee, C. J., & Pankratov, Y. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108758 · Cited by 87
Astrocytes in Memory Function: Pioneering Findings and Future Directions
Adamsky, A., & Goshen, I. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.05.033 · Cited by 83
“…activity, including regulation of synaptic formation, synaptic transmission, neuromodulation and plasticity (Haydon, 2001; Volterra and Meldolesi, 2005; Eroglu and Barres, 2010; Araque et al., 2014), all of which are considered as the infrastructure for information processing and memory formation.”
Verkhratsky, A., Marutle, A., Rodríguez-Arellano, J. J., & Nordberg, A. (2015) · The Neuroscientist · doi:10.1177/1073858414547132 · Cited by 95
Proteomics Analyses of Human Optic Nerve Head Astrocytes Following Biomechanical Strain
Rogers, R. S., Dharsee, M., Ackloo, S. Z., Sivak, J. M., & Flanagan, J. G. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.012302 · Cited by 75
Structural neural plasticity evoked by rapid-acting antidepressant interventions
Liao, C., Dua, A. N., Wojtasiewicz, C., Liston, C. M., & Kwan, A. C. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00876-0 · Cited by 81
“Synapse formation and elimination are additionally regulated by non-neuronal cells such as astrocytes and microglia 185,186”
Astrocyte‐mediated synapse remodeling in the pathological brain
Kim, S. K., Nabekura, J., & Koizumi, S. (2017) · Glia · doi:10.1002/glia.23169 · Cited by 89
“Astrocytes, the main type of glia in the CNS, have previously been known to serve the supportive roles in neural functions, such as ion homeostasis, neurotransmitter clearance, and energy supply to neurons (Eroglu & Barres, 2010; Freeman, 2010; Khakh & Sofroniew, 2015).”
BackgroundHuman-derived neural progenitors functionally replace astrocytes in adult mice
Chen, H., Qian, K. X., Chen, W., Hu, B., Blackbourn, L., Du, Z., Ma, L., Liu, H., Knobel, K. M., Ayala, M., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci69097 · Cited by 72
“In the adult CNS, each astrocyte and its processes occupy discrete domains, insulating neurons and up to 105 synapses and regulating synaptic activity (1, 2).”
Long-term culture of astrocytes attenuates the readily releasable pool of synaptic vesicles
Kawano, H., Katsurabayashi, S., Kakazu, Y., Yamashita, Y., Kubo, N., Kubo, M., Okuda, H., Takasaki, K., Kubota, K., Mishima, K., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048034 · Cited by 68
“the co-culture of purified retinal ganglion cells with astrocytes [2], [4], [10], acute isolation of aged astrocytes [12] and culturing of induced pluripotent stem cells obtained from aged animals [85], and some of these approaches could theoretically be applied to our system.”
BackgroundInfluentialBeretta, C., Nikitidou, E., Streubel-Gallasch, L., Ingelsson, M., Sehlin, D., & Erlandsson, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-72355-2 · Cited by 71
Bosch, C., Masachs, N., Exposito-Alonso, D., Martínez, A., Teixeira, C. M., Fernaud, I., Pujadas, L., Ulloa, F., Comella, J. X., DeFelipe, J., et al. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw216 · Cited by 70
Sárvári, M., Hrabovszky, E., Kalló, I., Solymosi, N., Tóth, K., Likó, I., Széles, J., Mahó, S., Molnar, B. A., & Liposits, Z. (2011) · Journal of Neuroinflammation · doi:10.1186/1742-2094-8-82 · Cited by 84
“It is likely that both astrocytes and microglia are involved in this synapse elimination mechanism [65] which is highly relevant to the layer-specific loss of synapses in the estrogen-deprived, aging female neocortex [66].”
BackgroundEmerging evidence for astrocyte dysfunction in schizophrenia
Figueiredo, E. C. D. O., Calì, C., Petrelli, F., & Bezzi, P. (2022) · Glia · doi:10.1002/glia.24221 · Cited by 87
“…play important role both during postnatal development and in the adulthood by regulating the formation and development of neuronal circuits (Eroglu & Barres, 2010) and by regulating multiple homeostatic functions such as the buffering of extra-cellular potassium or the modulation of…”
BackgroundTassoni, A., Farkhondeh, V., Itoh, Y., Itoh, N., Sofroniew, M. V., & Voskuhl, R. R. (2019) · Scientific Reports · doi:10.1038/s41598-019-46232-6 · Cited by 73
Aldh1L1 is expressed by postnatal neural stem cells in vivo
Foo, L. C., & Dougherty, J. D. (2013) · Glia · doi:10.1002/glia.22539 · Cited by 62
“They provide essential metabolic support for neurons, key signals for synaptogenesis (Christopherson et al., 2005; Eroglu and Barres, 2010; Ullian et al., 2001), and actively respond to neurotransmission (Sun et al., 2013).”
Che, D. N., Cho, B. O., Kim, J., Shin, J. Y., Kang, H. J., & Jang, S. I. (2020) · Inflammation · doi:10.1007/s10753-020-01245-6 · Cited by 73
Lang, D. G., Schott, B. H., van Ham, M., Morton, L., Kulikovskaja, L., Herrera‐Molina, R., Pielot, R., Klawonn, F., Montag, D., Jänsch, L., et al. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1242-1 · Cited by 77
From a glial syncytium to a more restricted and specific glial networking
Giaume, C., & Liu, X. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.09.001 · Cited by 77
The role of dopamine in NLRP3 inflammasome inhibition: Implications for neurodegenerative diseases
Possemato, E., Barbera, L. L., Nobili, A., Krashia, P., & D’Amelio, M. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101907 · Cited by 76
MicroRNAs in Neuronal Communication
Higa, G. S. V., de Sousa, É., Walter, L. T., Kinjo, É. R., Resende, R. R., & Kihara, A. H. (2014) · Molecular Neurobiology · doi:10.1007/s12035-013-8603-7 · Cited by 68
“Because astrocytes are known to release various signals to modulate synaptic/neuronal functions [168, 169] and survival [170], it is likely that astroglial exosomes may also play a modulatory role in synaptic functions.”
BackgroundRoles of glial cells in schizophrenia: Possible targets for therapeutic approaches
Takahashi, N., & Sakurai, T. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.11.001 · Cited by 67
Leonard, E., Salman, S., & Nurse, C. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00225 · Cited by 66
“INTRACELLULAR Ca2+ SIGNALING IN TYPE II CELLS There is abundant evidence that glial cells in the CNS contribute to synapse integration by generating intracellular Ca2+ signals and releasing gliotransmitters such as ATP, GABA, and glutamate (Eroglu and Barres, 2010; Bazargani and Attwell, 2016).”
BackgroundInfluentialNovel insights into gliotransmitters
Petrelli, F., & Bezzi, P. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.11.010 · Cited by 66
Pathogenesis of α-Synuclein in Parkinson’s Disease: From a Neuron-Glia Crosstalk Perspective
Yi, S., Wang, L., Wang, H., Ho, M. S.-C., & Zhang, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232314753 · Cited by 96
New roles of reactive astrocytes in the brain; an organizer of cerebral ischemia
Koizumi, S., Hirayama, Y., & Morizawa, Y. M. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.01.007 · Cited by 70
Modulation of Pain and Itch by Spinal Glia
Tsuda, M. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0129-y · Cited by 74
Simone, C., Ramirez, A., Bucchia, M., Rinchetti, P., Rideout, H., Papadimitriou, D., Re, D., & Corti, S. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2106-9 · Cited by 65
“Micro and macroglial cells have an important role in the formation, function and elimination of synapses under normal and pathologic conditions (Figure 1) [68].”
Neuroinflammation and Glial Phenotypic Changes in Alpha-Synucleinopathies
Refolo, V., & Stefanova, N. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00263 · Cited by 72
“Astrocytes have also been shown to play a role in synaptogenesis and in supporting neuronal connectivity (Eroglu and Barres, 2010; Allen and Eroglu, 2017).”
BackgroundKoeppen, J., Nguyen, A. Q., Nikolakopoulou, A. M., Garcia, M. L., Hanna, S., Woodruff, S., Figueroa, Z. A., Obenaus, A., & Ethell, I. M. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3618-17.2018 · Cited by 73
Metadata
- 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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