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Glutamate‐mediated neuronal–glial transmission
Open accessAbstract
The brain is the most complex organ of the human body. It is composed of several highly specialized and heterogeneous populations of cells, represented by neurones (e.g. motoneurons, projection neurons or interneurons), and glia represented by astrocytes, oligodendrocytes and microglia. In recent years there have been numerous studies demonstrating close bidirectional communication of neurons and glia at structural and functional levels. In particular, the excitatory transmitter glutamate has been shown to evoke a variety of responses in astrocytes and oligodendrocytes in the healthy as well as the diseased brain. Here we overview the multitude of glutamate sensing molecules expressed in glia and describe some general experiments which have been performed to identify the glutamate‐responsive molecules, i.e. the ionotropic and metabotropic glutamate receptors as well as the glutamate transporters. We also discuss a transgenic mouse model that permits detailed and specific investigations of the role of glial glutamate receptors.
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“This process can be adjusted on demand either through modulation of neurovascular coupling15–17 or via neuronal signaling to astrocytes18.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [17]
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BackgroundMechanisms of ATP‐ and glutamate‐mediated calcium signaling in white matter astrocytes
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Self-citationComplex and region-specific changes in astroglial markers in the aging brain
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InfluentialP2X Receptors and Their Roles in Astroglia in the Central and Peripheral Nervous System
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Exacerbation of Epilepsy by Astrocyte Alkalization and Gap Junction Uncoupling
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“It has been suggested that this gap junction coupling enables direct exchange of various substances, such as ions, transmitters, and metabolites (Verkhratsky and Kettenmann, 1996; Hirase et al., 2004; Verkhratsky and Kirchhoff, 2007; Escartin and Rouach, 2013; Verkhratsky and Nedergaard, 2018).”
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“mGlu5 receptors are also expressed in glia, particularly in astrocytes, and the expression of the mGlu5 receptor subtype in astrocytes has been highlighted with respect to a number of potential physiological and pathophysiological roles (Verkhratsky and Kirchhoff, 2007; Wierońska and Pilc, 2009).”
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“…glutamate release from astrocytes via activation of Ca2+ permeable ionotropic AMPA receptors and group 1 metabotropic glutamate receptors (mGluRs), which release Ca2+ from internal stores through 1,4,5-inositol-trisphosphate (InsP3) signaling (Hansson et al., 2000; Verkhratsky and Kirchhoff, 2007).”
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“NMDA-activated currents can be recorded from astrocytes in cortical slices at resting membrane potentials (-80 mV) in the presence of physiological concentration (1 mM) of extracellular Mg [41, 55].”
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“The roles of glial mGluRs are not yet fully elucidated but likely involve the regulation of glial activities in response to the local excitatory tone (D’Antoni et al., 2008; Verkhratsky and Kirchhoff, 2007), thereby contributing to glia–neuron interactions.”
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“In addition, the astrocytes can also absorb the glutamate released during neurotransmission and convert it to glutamine to eliminate glutamate toxicity (12,13).”
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“assuring a fine glutamate regulation through specific astrocytic transporters [glial transporter (GTs)], like GLT-1 and GLAST (Verkhratsky and Kirchhoff, 2007).”
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“For example, astrocytes express an array of glutamate receptors, although these differ profoundly depending upon brain region (Verkhratsky and Kirchhoff, 2007; Molders et al., 2018).”
BackgroundPathological potential of astroglia
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“Astrocytes are the main sink of glutamate in the brain; from the bulk of glutamate released during synaptic transmission, about 20 % is accumulated into postsynaptic neurons and the remaining 80 % is taken up by perisynaptic astrocytes (Verkhratsky and Kirchhoff 2007).”
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“Regardless of their position, Ca influx through AMPARs has been reported in different types of astrocytes both in cultures and in brain slices (Verkhratsky and Kirchhoff, 2007).”
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“In particular, the excitatory transmitter glutamate has been shown to evoke a variety of responses in astrocytes and oligodendrocytes in the diseased brain (Verkhratsky and Kirchhoff, 2007).”
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“Glutamate increases intracellular Ca in astrocytes via activation of Ca permeable ionotropic glutamate receptors, which respond to AMPA, and metabotropic glutamate receptors, which release Ca from internal stores through 1,4,5-inositol-trisphosphate signaling (Hansson et al., 2000; Verkhratsky and Kirchhoff, 2007).”
InfluentialLiu, Y., Ding, X., Wang, X., Zou, X., Li, X., Liu, Y.-Y., Li, J., Qian, X.-Y., & Chen, J. (2019) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-019-2613-6 · Cited by 37
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“Recent evidence suggests macroglial mGluRs to be involved in the communication with neurones [6, 10, 11], whilst stimulation of group II and I/III mGluRs in activated microglia is reported to be neurotoxic and neuroprotective, respectively [12–14].”
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“For example, expression of NMDA receptors has been hitherto described in cortex and spinal cord, but not in other brain regions (Ziak et al. 1998, Seifert & Steinhauser 2001, Lalo et al. 2006, Verkhratsky & Kirchhoff 2007a,b; see also Fig.”
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“These cells also express ionotropic and metabotropic glutamate receptors (Gallo & Ghiani, 2000), thus allowing a high degree of sophistication in deciphering signals carried by external glutamate (Verkhratsky & Kirchhoff, 2007).”
BackgroundGlial and light-dependent glutamate metabolism in the suprachiasmatic nuclei
Leone, M. J., Beaulé, C., Marpegán, L., Simon, T., Herzog, E. D., & Golombek, D. A. (2015) · Chronobiology International · doi:10.3109/07420528.2015.1006328 · Cited by 28
“Astrocytes can release, take up and respond to glutamate (Kettenmann & Steinhäuser, 2005; Verkhratsky & Kirchhoff, 2007a,b; Volterra & Meldolesi, 2005); they play a critical (and almost exclusive) role in the clearance of extracellular glutamate through uptake and degradation (Schousboe &…”
BackgroundLiu, L., Su, Y., Yang, W., Xiao, M., Gao, J., & Hu, G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.028 · Cited by 28
Chen, H., Lin, S.-C., & Chan, M. (2011) · Neurodegenerative Diseases · doi:10.1159/000323872 · Cited by 28
“In addition, glutamate acts as a mediator of both interneuronal and neuronal-glial signaling [”
BackgroundCirillo, G., Colangelo, A. M., De Luca, C., Savarese, L., Barillari, M. R., Alberghina, L., & Papa, M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152750 · Cited by 27
“The glial glutamate transporters (gGTS) (GLT1, GLAST), expressed by perisynaptic astrocytes, are essential for the reuptake of the glutamate released during synaptic transmission, rescuing the extracellular homeostasis of neurotransmission [33].”
BackgroundPurinergic and Glutamatergic Receptors on Astroglia
Verkhratsky, A., & Burnstock, G. (2014) · Advances in neurobiology · doi:10.1007/978-3-319-08894-5_4 · Cited by 27
Self-citationSodium Fluxes and Astroglial Function
Verkhratsky, A., Noda, M., Parpura, V., & Kirischuk, S. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-4756-6_25 · Cited by 27
Self-citationKato, T. A., Watabe, M., & Kanba, S. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00139 · Cited by 29
Local brain environment changes associated with epileptogenesis
Ikoma, Y., Sasaki, D., & Matsui, K. (2023) · Brain · doi:10.1093/brain/awac355 · Cited by 26
Shoji, Y., Yamaguchi‐Yamada, M., & Yamamoto, Y. (2010) · Histochemistry and Cell Biology · doi:10.1007/s00418-010-0711-0 · Cited by 26
“In the central nervous system, it is well-established neuron–glia interaction is mediated by various neurotransmitters, e.g., ATP and glutamate (Fellin 2009 ;K oizumi 2010; Verkhratsky and Kirchhoff 2007 ).”
BackgroundVilar, A., de Lemos, L., Patraca, I., Martínez, N., Folch, J., Junyent, F., Verdaguer, E., Pallàs, M., Auladell, C., & Camins, A. (2013) · Free Radical Research · doi:10.3109/10715762.2013.845295 · Cited by 26
Differential calcium signalling in neuronal-glial networks.
Verkhratsky, A., Anděrová, M., & Chvátal, A. (2009) · Frontiers in Bioscience · doi:10.2741/3359 · Cited by 25
“AMPA receptors expressed in many types of glial cells are devoid of GluR-B subunit and thus have appreciable Ca permeability (PCa/ PNa ~ 1 - (20, 147)).”
BackgroundSelf-citationMa, Y., Bu, J., Dang, H., Sha, J., Yan, J., Shan-jiang, A., Li, H., & Zhu, Y. (2015) · Brain Research · doi:10.1016/j.brainres.2014.11.030 · Cited by 23
“tion (Verkhratsky, 2010; Verkhratsky and Kirchhoff, 2007), promoting the normal metabolism of neurotransmitters and participating in substance exchange and information communication among neurons (Rossi et al.”
BackgroundThe Circadian Clocks, Oscillations of Pain-Related Mediators, and Pain
Chu, Y., He, H., Liu, Q., Jia, S., Fan, W., & Huang, F. P. (2022) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-022-01205-8 · Cited by 22
“Extracellular glutamate can be cleared by the glutamate transporters (both GLAST and GLT-1) of astrocytes and is converted to glutamine under the action of glutamine synthetase (GS) (Verkhratsky and Kirchhoff 2007; Leone et al. 2015).”
BackgroundPereira, F. C., Rolo, M. R., Marques, E., Mendes, V. M., Ribeiro, C., Ali, S. F., Morgadinho, T., & Macedo, T. R. A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1432.040 · Cited by 20
Segawa, S., Nishiura, T., Furuta, T., Ohsato, Y., Tani, M., Nishida, K., & Nagasawa, K. (2013) · Life Sciences · doi:10.1016/j.lfs.2013.11.007 · Cited by 20
Sühs, K., Wegner, F., Skripuletz, T., Trebst, C., Tayeb, S. B., Raab, P., & Stangel, M. (2015) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2015.2689 · Cited by 20
“Its composition varies between cell type (neuron, oligodendrocyte, astrocyte) and site of expression (20-23).”
BackgroundAnti-inflammatory role of Leptin in glial cells through p38 MAPK pathway inhibition
Patraca, I., Martínez, N., Busquets, O., Navia, A. M., Pedrós, I., Beas‐Zárate, C., Marin, M., Ettcheto, M., Sureda, F. X., Auladell, C., et al. (2016) · Pharmacological Reports · doi:10.1016/j.pharep.2016.12.005 · Cited by 20
“Moreover, glial cells mainly astrocytes exert important functions in the brain, among them synthesis of neurotrophic factors, ion homeostasis, and regulation of extracellular glutamate concentration [7 – 10].”
RetractedARACHNE: A neural-neuroglial network builder with remotely controlled parallel computing
Aleksin, S. G., Zheng, K., Rusakov, D. A., & Savtchenko, L. P. (2017) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005467 · Cited by 18
Zepeda, R. C., Barrera, I., Castelán, F., Suárez‐Pozos, E., Melgarejo, Y., González-Mejía, M. E., Hernández‐Kelly, L. C., López‐Bayghen, E., Aguilera, J., & Ortega, A. (2009) · Neurochemistry International · doi:10.1016/j.neuint.2009.03.011 · Cited by 20
“Glu-dependent increase in intracellular Ca levels, since it is known that in one hand, iGluRs expressed in BGC are permeable to this ion (Muller and Connor, 1992), while in the other hand, group I mGluRs are coupled to phosphatidylinositol metabolism and the release of Ca from the endoplasmic reticulum (Verkhratsky an…”
InfluentialTaber, K. H., & Hurley, R. A. (2008) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.20.2.iv · Cited by 21
Painful Neuron-Microglia Interactions in the Trigeminal Sensory System
Davies, A. J., Kim, Y. H., & Oh, S. B. (2010) · The Open Pain Journal · doi:10.2174/1876386301003010014 · Cited by 19
“Glutamate has in fact been found to play an integral role in direct signaling between astrocytes and neurons [66].”
BackgroundKuzhandaivel, A., Margaryan, G., Nistri, A., & Mladinić, M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.011 · Cited by 19
Pittà, M. D. (2020) · Springer eBooks · doi:10.1007/978-1-4614-7320-6_100691-1 · Cited by 21
Myint, A.-M., & Halaris, A. E. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.913303 · Cited by 18
“NMDA receptors are important in information processing in neurons, as well as in toxicity (17).”
BackgroundConstantinou, S., & Fern, R. F. (2009) · Glia · doi:10.1002/glia.20839 · Cited by 18
“Ionotropic glutamatergic receptors are expressed by both astrocytes (e.g., Gallo and Ghiani, 2000; Verkhratsky and Kirchhoff, 2007) and oligodendroglia (e.g., Fern and Moller, 2000; Follett et al., 2000; Gallo and Ghiani, 2000; Karadottir et al., 2005; McDonald et al., 1998; Micu et al., 2006;…”
BackgroundBudni, J., Molz, S., Dal-Cim, T. A., Martin‐de‐Saavedra, M. D., Egea, J., López, M. G., Tasca, C. I., & Rodrigues, A. L. S. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0425-6 · Cited by 18
Domingues, A. M. D. J., Neugebauer, K. M., & Fern, R. F. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07212.x · Cited by 21
“The best-studied example is the NMDA-type glutamate receptor that mediates post-synaptic potentials in astrocytes (Verkhratsky and Kirchhoff 2007) and oligodendroglia (Karadottir et al. 2005).”
BackgroundLee, K., Lee, J. M., Phan, T. T., Lee, C. J., Park, J. M., & Park, J. (2023) · Brain stimulation · doi:10.1016/j.brs.2023.08.002 · Cited by 17
Vergouts, M., Doyen, P. J., Peeters, M., Opsomer, R., & Hermans, E. (2017) · Glia · doi:10.1002/glia.23279 · Cited by 17
“The best characterized of these metabotropic receptors is the type 5 receptor (mGluR5) which is expressed in cultured astrocytes where it contributes to the regulation of glial responses to changes in local excitatory tone (D’Antoni et al., 2008; Verkhratsky & Kirchhoff, 2007).”
BackgroundInvolvement of Connexin43 in the Infrasonic Noise-Induced Glutamate Release by Cultured Astrocytes
Jiang, S., Wang, Y.-Q., Xu, C., Li, Y., Guo, R., & Li, L. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1277-3 · Cited by 16
“As the most numerous glial cell type in the central nervous system, astrocytes are critical for glutamate cycling [15].”
Cerebral and Retinal Neurovascular Changes: A Biomarker for Alzheimer’s Disease
Teja, K. V. R., Berendschot, T. T. J. M., Steinbusch, H. W. M., Webers, C. A. B., Praveen Murthy, R., & Mathuranath, P. S. (2017) · Journal of Gerontology & Geriatric Research · doi:10.4172/2167-7182.1000447 · Cited by 16
“In principal, synaptic activity increases the level of neurotransmitter specifically glutamate, which is taken by the NMDA receptors on the neuron and mGlu receptors on the astrocytes [15].”
BackgroundVallejo, R., Platt, D. C., Rink, J. A., Jones, M. A., Kelley, C. A., Gupta, A., Cass, C. L., Eichenberg, K., Vallejo, A., Smith, W. J., et al. (2019) · Brain Sciences · doi:10.3390/brainsci9110303 · Cited by 15
“The initiation, propagation, and perception of acute pain has been traditionally described in terms of the excitation of neuronal transmission pathways [1].”
Background
Metadata
- Authors
- Verkhratsky, A., & Kirchhoff, F.
- Affiliations
- University of Manchester (GB)
- Max Planck Society (DE)
- Venue
- Journal of Anatomy
- Publisher
- Wiley
- Published
- 2007-05-15
- Volume
- 210
- Issue
- 6
- Pages
- 651-660
- ISSN
- 0021-8782 (ISSN-L)
- 1469-7580
- PMC
- PMC2375757
- OpenAlex
- W2050984501
- Semantic Scholar
- e1c37e40facf7bda28434bf975bf96308daffcdd
- Cited by
- 156
- References
- 103
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 1 · 2023: 5 · 2022: 10 · 2021: 10 · 2020: 8 · 2019: 8 · 2018: 5 · 2017: 9 · 2016: 7 · 2015: 10 · 2014: 5 · 2013: 12 · 2012: 11
- FWCI
- 1.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Anatomy (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Wellcome Trust
- Deutsche Forschungsgemeinschaft
- National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- glutamate, astrocytes, oligodendrocytes, microglia, ionotropic glutamate receptors, metabotropic glutamate receptors, glutamate transporters, transgenic mouse model
- MeSH terms
- Animals, Brain, Glutamates, Humans, Mice, Transgenic, Neuroglia, Neurons, Receptors, Glutamate, Models, Animal, Amino Acid Transport System X-AG, Mice
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