Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T09:34:29.113Z Has data issue: false hasContentIssue false
  • English
  • Français

Is astrocyte calcium signaling relevant for synaptic plasticity?

Published online by Cambridge University Press:  02 December 2010

Sarrah Ben Achour ,
Lorena Pont-Lezica ,
Catherine Béchade  and
Olivier Pascual
Sarrah Ben Achour
Affiliation:
Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS, Paris, France Inserm, U1024, Paris, France CNRS, UMR 8197, Paris, France
Lorena Pont-Lezica
Affiliation:
Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS, Paris, France Inserm, U1024, Paris, France CNRS, UMR 8197, Paris, France
Catherine Béchade
Affiliation:
Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS, Paris, France Inserm, U1024, Paris, France CNRS, UMR 8197, Paris, France
Olivier Pascual*
Affiliation:
Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS, Paris, France Inserm, U1024, Paris, France CNRS, UMR 8197, Paris, France
*
Correspondence should be addressed to: Olivier Pascual, Ecole Normale Supérieure, 46 rue d'Ulm, 75005Paris email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Astrocytes constitute a major group of glial cells which were long regarded as passive elements, fulfilling nutritive and structural functions for neurons. Calcium rise in astrocytes propagating to neurons was the first demonstration of direct interaction between the two cell types. Since then, calcium has been widely used, not only as an indicator of astrocytic activity but also as a stimulator switch to control astrocyte physiology. As a result, astrocytes have been elevated from auxiliaries to neurons, to cells involved in processing synaptic information. Curiously, while there is evidence that astrocytes play an important role in synaptic plasticity, the data relating to calcium's pivotal role are inconsistent. In this review, we will detail the various mechanisms of calcium flux in astrocytes, then briefly present the calcium-dependent mechanisms of gliotransmitter release. Finally, we will discuss the role of calcium in plasticity and present alternative explanations that could reconcile the conflicting results published recently.

Keywords

LTPglutamateIP3G-protein coupled receptorD-serine
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 3 , August 2010 , pp. 147 - 155
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

REFERENCES

Agulhon, C., Fiacco, T.A. and McCarthy, K.D. (2010) Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science 327, 1250–1254.CrossRefGoogle Scholar
Akopian, G., Kressin, K., Derouiche, A. and Steinhauser, C. (1996) Identified glial cells in the early postnatal mouse hippocampus display different types of Ca2+ currents. Glia 17, 181–194.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Alloisio, S., Aiello, R., Ferroni, S. and Nobile, M. (2006) Potentiation of native and recombinant P2X7-mediated calcium signaling by arachidonic acid in cultured cortical astrocytes and human embryonic kidney 293 cells. Molecular Pharmacology 69, 1975–1983.CrossRefGoogle ScholarPubMed
Angulo, M.C., Kozlov, A.S., Charpak, S. and Audinat, E. (2004) Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. Journal of Neuroscience 24, 6920–6927.CrossRefGoogle ScholarPubMed
Araque, A., Li, N., Doyle, R.T. and Haydon, P.G. (2000) SNARE protein-dependent glutamate release from astrocytes. Journal of Neuroscience 20, 666–673.CrossRefGoogle ScholarPubMed
Araque, A., Parpura, V., Sanzgiri, R.P. and Haydon, P.G. (1999) Tripartite synapses: glia, the unacknowledged partner. Trends in Neurosciences 22, 208–215.CrossRefGoogle ScholarPubMed
Barbour, B. (2001) An evaluation of synapse independence. Journal of Neuroscience 21, 7969–7984.CrossRefGoogle ScholarPubMed
Barres, B.A., Chun, L.L. and Corey, D.P. (1988) Ion channel expression by white matter glia: I. Type 2 astrocytes and oligodendrocytes. Glia 1, 10–30.CrossRefGoogle ScholarPubMed
Ben Achour, S. and Pascual, O. (2010) Glia: the many ways to modulate synaptic plasticity. Neurochemistry International 57, 440–445.CrossRefGoogle ScholarPubMed
Bender, A.S., Reichelt, W. and Norenberg, M.D. (2000) Characterization of cystine uptake in cultured astrocytes. Neurochemistry International 37, 269–276.CrossRefGoogle ScholarPubMed
Bezzi, P., Carmignoto, G., Pasti, L., Vesce, S., Rossi, D., Rizzini, B.L. et al. (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391, 281–285.CrossRefGoogle ScholarPubMed
Bezzi, P., Domercq, M., Brambilla, L., Galli, R., Schols, D., De Clercq, E. et al. (2001) CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nature Neuroscience 4, 702–710.CrossRefGoogle ScholarPubMed
Bezzi, P., Gundersen, V., Galbete, J.L., Seifert, G., Steinhauser, C., Pilati, E. et al. (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nature Neuroscience 7, 613–620.CrossRefGoogle ScholarPubMed
Birnbaumer, L. (2009) The TRPC class of ion channels: a critical review of their roles in slow, sustained increases in intracellular Ca2+ concentrations. Annual Review of Pharmacology and Toxicology 49, 395–426.CrossRefGoogle Scholar
Boulay, G., Brown, D.M., Qin, N., Jiang, M., Dietrich, A., Zhu, M.X. et al. (1999) Modulation of Ca2+ entry by polypeptides of the inositol 1,4, 5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP3R in store depletion-activated Ca2+ entry. Proceedings of the National Academy of Sciences of the U.S.A. 96, 14955–14960.CrossRefGoogle Scholar
Bowser, D.N. and Khakh, B.S. (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. Journal of Neuroscience 24, 8606–8620.CrossRefGoogle ScholarPubMed
Cahoy, J.D., Emery, B., Kaushal, A., Foo, L.C., Zamanian, J.L., Christopherson, K.S. et al. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. Journal of Neuroscience 28, 264–278.CrossRefGoogle Scholar
Carmignoto, G., Pasti, L. and Pozzan, T. (1998) On the role of voltage-dependent calcium channels in calcium signaling of astrocytes in situ. Journal of Neuroscience 18, 4637–4645.CrossRefGoogle ScholarPubMed
Cavelier, P. and Attwell, D. (2005) Tonic release of glutamate by a DIDS-sensitive mechanism in rat hippocampal slices. Journal of Physiology 564, 397–410.CrossRefGoogle ScholarPubMed
Cayouette, S., Lussier, M.P., Mathieu, E.L., Bousquet, S.M. and Boulay, G. (2004) Exocytotic insertion of TRPC6 channel into the plasma membrane upon Gq protein-coupled receptor activation. Journal of Biological Chemistry 279, 7241–7246.CrossRefGoogle ScholarPubMed
Clapham, D., Runnels, L. and Strübing, C. (2001) The TRP ion channel family. Nature Reviews Neuroscience 2, 387–396.CrossRefGoogle ScholarPubMed
Clements, J.D. and Westbrook, G.L. (1991) Activation kinetics reveal the number of glutamate and glycine binding sites on the N-methyl-d-aspartate receptor. Neuron 7, 605–613.CrossRefGoogle ScholarPubMed
Conti, F., Minelli, A. and Brecha, N. (1994) Cellular localization and laminar distribution of AMPA glutamate receptor subunits mRNAs and proteins in the rat cerebral cortex. Journal of Comparative Neurology 350, 241–259.CrossRefGoogle ScholarPubMed
Corvalan, V., Cole, R., de Vellis, J. and Hagiwara, S. (1990) Neuronal modulation of calcium channel activity in cultured rat astrocytes. Proceedings of the National Academy of Sciences of the U.S.A. 87, 4345–4348.CrossRefGoogle ScholarPubMed
Crippa, D., Schenk, U., Francolini, M., Rosa, P., Verderio, C., Zonta, M. et al. (2006) Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis. Journal of Physiology 570, 567–582.CrossRefGoogle ScholarPubMed
D'Ascenzo, M., Vairano, M., Andreassi, C., Navarra, P., Azzena, G.B. and Grassi, C. (2004) Electrophysiological and molecular evidence of L- (Cav1), N- (Cav2.2), and R- (Cav2.3) type Ca2+ channels in rat cortical astrocytes. Glia 45, 354–363.CrossRefGoogle Scholar
D'Ascenzo, M., Fellin, T., Terunuma, M., Revilla-Sanchez, R., Meaney, D.F., Auberson, Y.P. et al. (2007) mGluR5 stimulates gliotransmission in the nucleus accumbens. Proceedings of the National Academy of Sciences of the U.S.A. 104, 1995–2000.CrossRefGoogle ScholarPubMed
Diamond, J.S. and Jahr, C.E. (2000) Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation. Journal of Neurophysiology 83, 2835–2843.CrossRefGoogle Scholar
Ding, S., Fellin, T., Zhu, Y., Lee, S.-Y., Auberson, Y.P., Meaney, D.F. et al. (2007) Enhanced astrocytic Ca2+ signals contribute to neuronal excitotoxicity after status epilepticus. Journal of Neuroscience 27, 10674–10684.CrossRefGoogle ScholarPubMed
Ding, S., Wang, T., Cui, W. and Haydon, P.G. (2009) Photothrombosis ischemia stimulates a sustained astrocytic Ca2+ signaling in vivo. Glia 57, 767–776.CrossRefGoogle ScholarPubMed
Domercq, M., Brambilla, L., Pilati, E., Marchaland, J., Volterra, A. and Bezzi, P. (2006) P2Y1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-alpha and prostaglandins. Journal of Biological Chemistry 281, 30684–30696.CrossRefGoogle ScholarPubMed
Duan, S., Anderson, C.M., Keung, E.C., Chen, Y., Chen, Y. and Swanson, R.A. (2003) P2X7 receptor-mediated release of excitatory amino acids from astrocytes. Journal of Neuroscience 23, 1320–1328.CrossRefGoogle ScholarPubMed
Duffy, S. and MacVicar, B.A. (1994) Potassium-dependent calcium influx in acutely isolated hippocampal astrocytes. Neuroscience 61, 51–61.CrossRefGoogle ScholarPubMed
Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P.G. and Carmignoto, G. (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729–743.CrossRefGoogle ScholarPubMed
Fellin, T., Sul, J.Y., D'Ascenzo, M., Takano, H., Pascual, O. and Haydon, P.G. (2006) Bidirectional astrocyte-neuron communication: the many roles of glutamate and ATP. Novartis Foundation symposium 276, 208–217; discussion 217–221, 233–207, 275–281.CrossRefGoogle ScholarPubMed
Fiacco, T.A. and McCarthy, K.D. (2004) Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous ampa receptor currents in CA1 pyramidal neurons. Journal of Neuroscience 24, 722–732.CrossRefGoogle ScholarPubMed
Fiacco, T.A., Agulhon, C. and McCarthy, K.D. (2009) Sorting out astrocyte physiology from pharmacology. Annual Review of Pharmacology and Toxicology 49, 151–174.CrossRefGoogle ScholarPubMed
Franke, H., Gunther, A., Grosche, J., Schmidt, R., Rossner, S., Reinhardt, R. et al. (2004) P2X7 receptor expression after ischemia in the cerebral cortex of rats. Journal of Neuropathology and Experimental Neurology 63, 686–699.CrossRefGoogle ScholarPubMed
Goloniva, V. (2005) Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. Journal of Physiology 564, 737–749.Google Scholar
Gordon, G.R.J., Iremonger, K.J., Kantevari, S., Ellis-Davies, G.C.R., MacVicar, B.A. and Bains, J.S. (2009) Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64, 391–403.CrossRefGoogle ScholarPubMed
Grimaldi, M., Maratos, M. and Verma, A. (2003) Transient receptor potential channel activation causes a novel form of [Ca2+]i oscillations and is not involved in capacitative Ca2+ entry in glial cells. Journal of Neuroscience 23, 4737–4745.CrossRefGoogle ScholarPubMed
Grosche, J., Matyash, V., Moller, T., Verkhratsky, A., Reichenbach, A. and Kettenmann, H. (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nature Neuroscience 2, 139–143.CrossRefGoogle ScholarPubMed
Hamilton, N.B. and Attwell, D. (2010) Do astrocytes really exocytose neurotransmitters? Nature Reviews 11, 227–238.CrossRefGoogle ScholarPubMed
Harteneck, C., Plant, T.D. and Schultz, G. (2000) From worm to man: three subfamilies of TRP channels. Trends in Neuroscience 23, 159–166.CrossRefGoogle Scholar
Hay, J.C. (2007) Calcium: a fundamental regulator of intracellular membrane fusion? EMBO Reports 8, 236–240.CrossRefGoogle ScholarPubMed
Hayashi, Y., Momiyama, A., Takahashi, T., Ohishi, H., Ogawa-Meguro, R., Shigemoto, R. et al. (1993) Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb. Nature 366, 687–690.CrossRefGoogle ScholarPubMed
Haydon, P.G. (2001) GLIA: listening and talking to the synapse. Nature Reviews 2, 185–193.CrossRefGoogle Scholar
Henneberger, C., Papouin, T., Oliet, S.H. and Rusakov, D.A. (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232–236.CrossRefGoogle ScholarPubMed
Hepp, R., Perraut, M., Chasserot-Golaz, S., Galli, T., Aunis, D., Langley, K. et al. (1999) Cultured glial cells express the SNAP-25 analogue SNAP-23. Glia 27, 181–187.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Hofmann, T., Obukhov, A.G., Schaefer, M., Harteneck, C., Gudermann, T. and Schultz, G. (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397, 259–263.CrossRefGoogle ScholarPubMed
Jabs, R., Matthias, K., Grote, A., Grauer, M., Seifert, G. and Steinhauser, C. (2007) Lack of P2X receptor mediated currents in astrocytes and GluR type glial cells of the hippocampal CA1 region. Glia 55, 1648–1655.CrossRefGoogle ScholarPubMed
Jaiswal, J.K., Fix, M., Takano, T., Nedergaard, M. and Simon, S.M. (2007) Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes. Proceedings of the National Academy of Sciences of the U.S.A. 104, 14151–14156.CrossRefGoogle ScholarPubMed
Jourdain, P., Bergersen, L.H., Bhaukaurally, K., Bezzi, P., Santello, M., Domercq, M. et al. (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nature Neuroscience 10, 331–339.CrossRefGoogle ScholarPubMed
Kang, J., Kang, N., Lovatt, D., Torres, A., Zhao, Z., Lin, J. et al. (2008) Connexin 43 hemichannels are permeable to ATP. Journal of Neuroscience 28, 4702–4711.CrossRefGoogle ScholarPubMed
Kimelberg, H.K., Goderie, S.K., Higman, S., Pang, S. and Waniewski, R.A. (1990) Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. Journal of Neuroscience 10, 1583–1591.CrossRefGoogle ScholarPubMed
Kiselyov, K., Xu, X., Mozhayeva, G., Kuo, T., Pessah, I., Mignery, G. et al. (1998) Functional interaction between InsP3 receptors and store-operated Htrp3 channels. Nature 396, 478–482.CrossRefGoogle ScholarPubMed
Kukley, M., Barden, J.A., Steinhauser, C. and Jabs, R. (2001) Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 36, 11–21.CrossRefGoogle ScholarPubMed
Lalo, U., Pankratov, Y., Kirchhoff, F., North, R.A. and Verkhratsky, A. (2006) NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. Journal of Neuroscience 26, 2673–2683.CrossRefGoogle ScholarPubMed
Latour, I., Hamid, J., Beedle, A.M., Zamponi, G.W. and Macvicar, B.A. (2003) Expression of voltage-gated Ca2+ channel subtypes in cultured astrocytes. Glia 41, 347–353.CrossRefGoogle ScholarPubMed
Li, D., Ropert, N., Koulakoff, A., Giaume, C. and Oheim, M. (2008) Lysosomes are the major vesicular compartment undergoing Ca2+-regulated exocytosis from cortical astrocytes. Journal of Neuroscience 28, 7648–7658.CrossRefGoogle ScholarPubMed
Liu, Q.S., Xu, Q., Arcuino, G., Kang, J. and Nedergaard, M. (2004a) Astrocyte-mediated activation of neuronal kainate receptors. Proceedings of the National Academy of Sciences of the U.S.A. 101, 3172–3177.CrossRefGoogle ScholarPubMed
Liu, Q.S., Xu, Q., Kang, J. and Nedergaard, M. (2004b) Astrocyte activation of presynaptic metabotropic glutamate receptors modulates hippocampal inhibitory synaptic transmission. Neuron Glia Biology 1, 307–316.CrossRefGoogle ScholarPubMed
Longuemare, M.C. and Swanson, R.A. (1997) Net glutamate release from astrocytes is not induced by extracellular potassium concentrations attainable in brain. Journal of Neurochemistry 69, 879–882.CrossRefGoogle Scholar
Lu, W., Man, H., Ju, W., Trimble, W.S., MacDonald, J.F. and Wang, Y.T. (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243–254.CrossRefGoogle ScholarPubMed
Ma, H.T., Patterson, R.L., van Rossum, D.B., Birnbaumer, L., Mikoshiba, K. and Gill, D.L. (2000) Requirement of the inositol trisphosphate receptor for activation of store-operated Ca2+ channels. Science 287, 1647–1651.CrossRefGoogle ScholarPubMed
MacVicar, B.A. (1984) Voltage-dependent calcium channels in glial cells. Science 226, 1345–1347.CrossRefGoogle ScholarPubMed
MacVicar, B.A. and Tse, F.W. (1988) Norepinephrine and cyclic adenosine 3′:5′-cyclic monophosphate enhance a nifedipine-sensitive calcium current in cultured rat astrocytes. Glia 1, 359–365.CrossRefGoogle ScholarPubMed
MacVicar, B.A., Hochman, D., Delay, M.J. and Weiss, S. (1991) Modulation of intracellular Ca++ in cultured astrocytes by influx through voltage-activated Ca++ channels. Glia 4, 448–455.CrossRefGoogle ScholarPubMed
Maienschein, V., Marxen, M., Volknandt, W. and Zimmermann, H. (1999) A plethora of presynaptic proteins associated with ATP-storing organelles in cultured astrocytes. Glia 26, 233–244.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Malarkey, E.B. and Parpura, V. (2008) Mechanisms of glutamate release from astrocytes. Neurochemistry International 52, 142–154.CrossRefGoogle ScholarPubMed
Malarkey, E., Ni, Y. and Parpura, V. (2008) Ca2+ entry through TRPC1 channels contributes to intracellular Ca2+ dynamics and consequent glutamate release from rat astrocytes. Glia 56, 821–835.CrossRefGoogle ScholarPubMed
Martineau, M., Galli, T., Baux, G. and Mothet, J.-P. (2008) Confocal imaging and tracking of the exocytotic routes for D-serine-mediated gliotransmission. Glia 56, 1271–1284.CrossRefGoogle ScholarPubMed
Matthias, K., Kirchhoff, F., Seifert, G., Huttmann, K., Matyash, M., Kettenmann, H. et al. (2003) Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. Journal of Neuroscience 23, 1750–1758.CrossRefGoogle ScholarPubMed
Metea, M.R. and Newman, E.A. (2006) Calcium signaling in specialized glial cells. Glia 54, 650–655.CrossRefGoogle ScholarPubMed
Milanese, M., Bonifacino, T., Zappettini, S., Usai, C., Tacchetti, C., Nobile, M. et al. (2009) Glutamate release from astrocytic gliosomes under physiological and pathological conditions. In Begley, T. and Crews, P. (eds) International Review of Neurobiology. Academic Press, pp. 295–318.CrossRefGoogle Scholar
Montell, C. (2001) Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Science STKE 90, re1.Google Scholar
Mothet, J.P., Pollegioni, L., Ouanounou, G., Martineau, M., Fossier, P. and Baux, G. (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proceedings of the National Academy of Sciences of the U.S.A. 102, 5606–5611.CrossRefGoogle ScholarPubMed
Nedergaard, M. (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263, 1768–1771.CrossRefGoogle ScholarPubMed
Newman, E.A. (2001) Calcium signaling in retinal glial cells and its effect on neuronal activity. Progress in Brain Research 132, 241–254.CrossRefGoogle ScholarPubMed
Okubo, Y., Sekiya, H., Namiki, S., Sakamoto, H., Iinuma, S., Yamasaki, M. et al. (2010) Imaging extrasynaptic glutamate dynamics in the brain. Proceedings of the National Academy of Sciences of the U.S.A. 107, 6526–6531.CrossRefGoogle ScholarPubMed
Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S. and Haydon, P.G. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747.CrossRefGoogle ScholarPubMed
Parpura, V., Fang, Y., Basarsky, T., Jahn, R. and Haydon, P.G. (1995) Expression of synaptobrevin II, cellubrevin and syntaxin but not SNAP-25 in cultured astrocytes. FEBS Letters 377, 489–492.Google Scholar
Pasti, L., Zonta, M., Pozzan, T., Vicini, S. and Carmignoto, G. (2001) Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. Journal of Neuroscience 21, 477–484.CrossRefGoogle ScholarPubMed
Perea, G. and Araque, A. (2005) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. Journal of Neuroscience 25, 2192–2203.CrossRefGoogle ScholarPubMed
Perea, G. and Araque, A. (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083–1086.CrossRefGoogle ScholarPubMed
Petralia, R. and Wenthold, R. (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. Journal of Comparative Neurology 318, 329–354.CrossRefGoogle ScholarPubMed
Petravicz, J., Fiacco, T.A. and McCarthy, K.D. (2008) Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. Journal of Neuroscience 28, 4967–4973.CrossRefGoogle Scholar
Phillis, J.W., Song, D. and O'Regan, M.H. (1997) Inhibition by anion channel blockers of ischemia-evoked release of excitotoxic and other amino acids from rat cerebral cortex. Brain Research 758, 9–16.CrossRefGoogle ScholarPubMed
Pizzo, P., Burgo, A., Pozzan, T. and Fasolato, C. (2001) Role of capacitative calcium entry on glutamate-induced calcium influx in type-I rat cortical astrocytes. Journal of Neurochemistry 79, 98–109.CrossRefGoogle ScholarPubMed
Porter, J.T. and McCarthy, K.D. (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. Journal of Neuroscience 16, 5073–5081.CrossRefGoogle ScholarPubMed
Proux-Gillardeaux, V., Gavard, J., Irinopoulou, T., Mege, R.M. and Galli, T. (2005) Tetanus neurotoxin-mediated cleavage of cellubrevin impairs epithelial cell migration and integrin-dependent cell adhesion. Proceedings of the National Academy of Sciences of the U.S.A. 102, 6362–6367.CrossRefGoogle ScholarPubMed
Randriamampita, C. and Tsien, R.Y. (1993) Emptying of intracellular Ca2+ stores releases a novel small messenger that stimulates Ca2+ influx. Nature 364, 809–814.CrossRefGoogle ScholarPubMed
Reyes-Haro, D., Muller, J., Boresch, M., Pivneva, T., Benedetti, B., Scheller, A. et al. (2010) Neuron-astrocyte interactions in the medial nucleus of the trapezoid body. Journal of General Physiology 135, 583–594.CrossRefGoogle ScholarPubMed
Rosado, J.A., Brownlow, S.L. and Sage, S.O. (2002) Endogenously expressed Trp1 is involved in store-mediated Ca2+ entry by conformational coupling in human platelets. Journal of Biological Chemistry 277, 42157–42163.CrossRefGoogle ScholarPubMed
Rosenberg, D., Kartvelishvily, E., Shleper, M., Klinker, C.M., Bowser, M.T. and Wolosker, H. (2010) Neuronal release of D-serine: a physiological pathway controlling extracellular D-serine concentration. FASEB Journal 24, 2951–2961.CrossRefGoogle ScholarPubMed
Rossi, D.J., Oshima, T. and Attwell, D. (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403, 316–321.CrossRefGoogle ScholarPubMed
Schipke, C., Ohlemeyer, O., Matyash, M., Nolte, C., Kettenmann, H. and Kirchhoff, F. (2001) Astrocytes of the mouse neocortex express functional N-methyl-d-aspartate receptors. FASEB Journal 15, 1270–1277.CrossRefGoogle ScholarPubMed
Seki, Y., Feustel, P.J., Keller, R.W. Jr, Tranmer, B.I. and Kimelberg, H.K. (1999) Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker. Stroke 30, 433–440.CrossRefGoogle Scholar
Serrano, A., Haddjeri, N., Lacaille, J.C. and Robitaille, R. (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. Journal of Neuroscience 26, 5370–5382.CrossRefGoogle ScholarPubMed
Serrano, A., Robitaille, R. and Lacaille, J.C. (2008) Differential NMDA-dependent activation of glial cells in mouse hippocampus. Glia 56, 1648–1663.CrossRefGoogle ScholarPubMed
Sheppard, C.A., Simpson, P.B., Sharp, A.H., Nucifora, F.C., Ross, C.A. and Lange, G.D. (1997) Comparison of type 2 inositol 1,4,5-trisphosphate receptor distribution and subcellular Ca2+ release sites that support Ca2+ waves in cultured astrocytes. Journal of Neurochemistry 68, 2317–2327.CrossRefGoogle ScholarPubMed
Shigetomi, E., Bowser, D.N., Sofroniew, M.V. and Khakh, B.S. (2008) Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. Journal of Neuroscience 28, 6659–6663.CrossRefGoogle ScholarPubMed
Shigetomi, E., Kracun, S., Sofroniew, M.V. and Khakh, B.S. (2010) A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nature Neuroscience 13, 759–766.CrossRefGoogle ScholarPubMed
Singh, B.B., Lockwich, T.P., Bandyopadhyay, B.C., Liu, X., Bollimuntha, S., Brazer, S.C. et al. (2004) VAMP2-dependent exocytosis regulates plasma membrane insertion of TRPC3 channels and contributes to agonist-stimulated Ca2+ influx. Molecular Cell 15, 635–646.CrossRefGoogle ScholarPubMed
Smani, T., Zakharov, S.I., Csutora, P., Leno, E., Trepakova, E.S. and Bolotina, V.M. (2004) A novel mechanism for the store-operated calcium influx pathway. Nature Cell Biology 6, 113–120.CrossRefGoogle ScholarPubMed
Steinhäuser, C. and Gallo, V. (1996) News on glutamate receptors in glial cells. Trends in Neurosciences 19, 339–345.CrossRefGoogle ScholarPubMed
Stenovec, M., Kreft, M., Grilc, S., Pangrsic, T. and Zorec, R. (2008) EAAT2 density at the astrocyte plasma membrane and Ca(2+)-regulated exocytosis. Molecular Membrane Biology 25, 203–215.CrossRefGoogle ScholarPubMed
Stern, P., Edwards, F.A. and Sakmann, B. (1992) Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. Journal of Physiology 449, 247–278.CrossRefGoogle ScholarPubMed
Stout, C.E., Costantin, J.L., Naus, C.C. and Charles, A.C. (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. Journal of Biological Chemistry 277, 10482–10488.CrossRefGoogle ScholarPubMed
Suadicani, S.O., Brosnan, C.F. and Scemes, E. (2006) P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. Journal of Neuroscience 26, 1378–1385.CrossRefGoogle ScholarPubMed
Szatkowski, M., Barbour, B. and Attwell, D. (1990) Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348, 443–446.CrossRefGoogle ScholarPubMed
Takano, T., Kang, J., Jaiswal, J.K., Simon, S.M., Lin, J.H., Yu, Y. et al. (2005) Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proceedings of the National Academy of Sciences of the U.S.A. 102, 16466–16471.CrossRefGoogle ScholarPubMed
Takano, T., Tian, G.F., Peng, W., Lou, N., Libionka, W., Han, X. et al. (2006) Astrocyte-mediated control of cerebral blood flow. Nature Neuroscience 9, 260–267.CrossRefGoogle ScholarPubMed
Thompson, R.J., Zhou, N. and MacVicar, B.A. (2006) Ischemia opens neuronal gap junction hemichannels. Science 312, 924–927.CrossRefGoogle ScholarPubMed
Trebak, M., Vazquez, G., Bird, G.S. and Putney, J.W. Jr (2003) The TRPC3/6/7 subfamily of cation channels. Cell Calcium 33, 451–461.CrossRefGoogle ScholarPubMed
Venkatachalam, K., van Rossum, D.B., Patterson, R.L., Ma, H.T. and Gill, D.L. (2002) The cellular and molecular basis of store-operated calcium entry. Nature Cell Biology 4, E263–E272.CrossRefGoogle ScholarPubMed
Venkatachalam, K., Zheng, F. and Gill, D.L. (2003) Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. Journal of Biological Chemistry 278, 29031–29040.CrossRefGoogle ScholarPubMed
Verkhratsky, A. (2010) Physiology of neuronal-glial networking. Neurochemistry International 57, 332–343.CrossRefGoogle ScholarPubMed
Verkhratsky, A., Orkand, R.K. and Kettenmann, H. (1998) Glial calcium: homeostasis and signaling function. Physiological Reviews 78, 99–141.CrossRefGoogle ScholarPubMed
Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews 6, 626–640.CrossRefGoogle ScholarPubMed
Williams, S.M., Diaz, C.M., Macnab, L.T., Sullivan, R.K. and Pow, D.V. (2006) Immunocytochemical analysis of D-serine distribution in the mammalian brain reveals novel anatomical compartmentalizations in glia and neurons. Glia 53, 401–411.CrossRefGoogle ScholarPubMed
Yagodin, S., Holtzclaw, L.A. and Russell, J.T. (1995) Subcellular calcium oscillators and calcium influx support agonist-induced calcium waves in cultured astrocytes. Molecular and Cellular Biochemistry 149–150, 137–144.CrossRefGoogle ScholarPubMed
Yamamoto-Hino, M., Miyawaki, A., Kawano, H., Sugiyama, T., Furuichi, T., Hasegawa, M. et al. (1995) Immunohistochemical study of inositol 1,4,5-trisphosphate receptor type 3 in rat central nervous system. Neuroreport 6, 273–276.CrossRefGoogle ScholarPubMed
Yao, Y., Ferrer-Montiel, A.V., Montal, M. and Tsien, R.Y. (1999) Activation of store-operated Ca2+ current in Xenopus oocytes requires SNAP-25 but not a diffusible messenger. Cell 98, 475–485.CrossRefGoogle Scholar
Ye, Z.-C., Wyeth, M.S., Baltan-Tekkok, S. and Ransom, B.R. (2003) Functional hemichannels in astrocytes: a novel mechanism of glutamate release. Journal of Neuroscience 23, 3588–3596.CrossRefGoogle ScholarPubMed
Zhang, J.-M., Wang, H.-K., Ye, C.-Q., Ge, W., Chen, Y., Jiang, Z.-L. et al. (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40, 971–982.CrossRefGoogle ScholarPubMed
Zhang, Q., Fukuda, M., Van Bockstaele, E., Pascual, O. and Haydon, P.G. (2004) Synaptotagmin IV regulates glial glutamate release. Proceedings of the National Academy of Sciences of the U.S.A. 101, 9441–9446.CrossRefGoogle ScholarPubMed
Zhang, Z., Chen, G., Zhou, W., Song, A., Xu, T., Luo, Q. et al. (2007) Regulated ATP release from astrocytes through lysosome exocytosis. Nature Cell Biology 9, 945–953.CrossRefGoogle ScholarPubMed
Zhou, M., Schools, G. and Kimelberg, H. (2006) Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. Journal of Neurophysiology 95, 134–143.CrossRefGoogle ScholarPubMed