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Sodium Fluxes and Astroglial Function

  • Alexei Verkhratsky
  • Mami Noda
  • Vladimir Parpura
  • Sergei Kirischuk
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 961)

Abstract

Astrocytes exhibit their excitability based on variations in cytosolic Ca2+ levels, which leads to variety of signalling events. Only recently, however, intracellular fluctuations of more abundant cation Na+ are brought in the limelight of glial signalling. Indeed, astrocytes possess several plasmalemmal molecular entities that allow rapid transport of Na+ across the plasma membrane: (1) ionotropic receptors, (2) canonical transient receptor potential cation channels, (3) neurotransmitter transporters and (4) sodium-calcium exchanger. Concerted action of these molecules in controlling cytosolic Na+ may complement Ca2+ signalling to provide basis for complex bidirectional astrocyte-neurone communication at the tripartite synapse.

Keywords

Ionotropic receptors Sodium-calcium exchanger Sodium potassium pump Glutamate transporter Sodium signalling 

References

  1. C. Agulhon, J. Petravicz, A.B. McMullen, E.J. Sweger, S.K. Minton, S.R. Taves, K.B. Casper, T.A. Fiacco, K.D. McCarthy, What is the role of astrocyte calcium in neurophysiology? Neuron 59, 932–946 (2008)PubMedCrossRefGoogle Scholar
  2. F. Ashour, J. Deuchars, Electron microscopic localisation of P2X4 receptor subunit immunoreactivity to pre- and post-synaptic neuronal elements and glial processes in the dorsal vagal complex of the rat. Brain Res. 1026, 44–55 (2004)PubMedCrossRefGoogle Scholar
  3. A.M. Benjamin, Influence of Na+, K+, and Ca2+ on glutamine synthesis and distribution in rat brain cortex slices: a possible linkage of glutamine synthetase with cerebral transport processes and energetics in the astrocytes. J. Neurochem. 48, 1157–1164 (1987)PubMedCrossRefGoogle Scholar
  4. M. Bennay, J. Langer, S.D. Meier, K.W. Kafitz, C.R. Rose, Sodium signals in cerebellar Purkinje neurons and Bergmann glial cells evoked by glutamatergic synaptic transmission. Glia 56, 1138–1149 (2008)PubMedCrossRefGoogle Scholar
  5. B. Benz, G. Grima, K.Q. Do, Glutamate-induced homocysteic acid release from astrocytes: possible implication in glia-neuron signaling. Neuroscience 124, 377–386 (2004)PubMedCrossRefGoogle Scholar
  6. Y. Bernardinelli, P.J. Magistretti, J.Y. Chatton, Astrocytes generate Na+-mediated metabolic waves. Proc. Natl. Acad. Sci. U. S. A. 101, 14937–14942 (2004)PubMedCrossRefGoogle Scholar
  7. M.P. Blaustein, M. Juhaszova, V.A. Golovina, P.J. Church, E.F. Stanley, Na/Ca exchanger and PMCA localization in neurons and astrocytes: functional implications. Ann. N. Y. Acad. Sci. 976, 356–366 (2002)PubMedCrossRefGoogle Scholar
  8. N. Burnashev, A. Villarroel, B. Sakmann, Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J. Physiol. (Lond.) 496, 165–173 (1996)Google Scholar
  9. J.Y. Chatton, L. Pellerin, P.J. Magistretti, GABA uptake into astrocytes is not associated with significant metabolic cost: implications for brain imaging of inhibitory transmission. Proc. Natl. Acad. Sci. U. S. A. 100, 12456–12461 (2003)PubMedCrossRefGoogle Scholar
  10. B.A. Clark, B. Barbour, Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J. Physiol. (Lond.) 502(Pt 2), 335–350 (1997)CrossRefGoogle Scholar
  11. D.F. Condorelli, F. Conti, V. Gallo, F. Kirchhoff, G. Seifert, C. Steinhauser, A. Verkhratsky, X. Yuan, Expression and functional analysis of glutamate receptors in glial cells. Adv. Exp. Med. Biol. 468, 49–67 (1999)PubMedCrossRefGoogle Scholar
  12. F. Conti, A. Minelli, N.C. Brecha, Cellular localization and laminar distribution of AMPA glutamate receptor subunits mRNAs and proteins in the rat cerebral cortex. J. Comp. Neurol. 350, 241–259 (1994)PubMedCrossRefGoogle Scholar
  13. F. Conti, S. DeBiasi, A. Minelli, M. Melone, Expression of NR1 and NR2A/B subunits of the NMDA receptor in cortical astrocytes. Glia 17, 254–258 (1996)PubMedCrossRefGoogle Scholar
  14. N.C. Danbolt, Glutamate uptake. Prog. Neurobiol. 65, 1–105 (2001)PubMedCrossRefGoogle Scholar
  15. J.W. Deitmer, C.R. Rose, Ion changes and signalling in perisynaptic glia. Brain Res. Rev. 63, 113–129 (2010)PubMedCrossRefGoogle Scholar
  16. R. DiPolo, L. Beauge, The calcium pump and sodium-calcium exchange in squid axons. Annu. Rev. Physiol. 45, 313–324 (1983)PubMedCrossRefGoogle Scholar
  17. C.L. Floyd, F.A. Gorin, B.G. Lyeth, Mechanical strain injury increases intracellular sodium and reverses Na+/Ca2+ exchange in cortical astrocytes. Glia 51, 35–46 (2005)PubMedCrossRefGoogle Scholar
  18. H. Franke, J. Grosche, H. Schadlich, U. Krugel, C. Allgaier, P. Illes, P2X receptor expression on astrocytes in the nucleus accumbens of rats. Neuroscience 108, 421–429 (2001)PubMedCrossRefGoogle Scholar
  19. H. Franke, A. Gunther, J. Grosche, R. Schmidt, S. Rossner, R. Reinhardt, H. Faber-Zuschratter, D. Schneider, P. Illes, P2X7 receptor expression after ischemia in the cerebral cortex of rats. J. Neuropathol. Exp. Neurol. 63, 686–699 (2004)PubMedGoogle Scholar
  20. M. Fumagalli, R. Brambilla, N. D’Ambrosi, C. Volonte, M. Matteoli, C. Verderio, M.P. Abbracchio, Nucleotide-mediated calcium signaling in rat cortical astrocytes: role of P2X and P2Y receptors. Glia 43, 218–230 (2003)PubMedCrossRefGoogle Scholar
  21. A. Gadea, A.M. Lopez-Colome, Glial transporters for glutamate, glycine and GABA I. Glutamate transporters. J. Neurosci. Res. 63, 453–460 (2001)PubMedCrossRefGoogle Scholar
  22. V. Gallo, C.A. Ghiani, Glutamate receptors in glia: new cells, new inputs and new functions. Trends Pharmacol. Sci. 21, 252–258 (2000)PubMedCrossRefGoogle Scholar
  23. J.R. Geiger, T. Melcher, D.S. Koh, B. Sakmann, P.H. Seeburg, P. Jonas, H. Monyer, Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193–204 (1995)PubMedCrossRefGoogle Scholar
  24. W.F. Goldman, P.J. Yarowsky, M. Juhaszova, B.K. Krueger, M.P. Blaustein, Sodium/calcium exchange in rat cortical astrocytes. J. Neurosci. 14, 5834–5843 (1994)PubMedGoogle Scholar
  25. V.A. Golovina, Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J. Physiol. (Lond.) 564, 737–749 (2005)CrossRefGoogle Scholar
  26. M. Grimaldi, M. Maratos, A. Verma, Transient receptor potential channel activation causes a novel form of [Ca 2+]I oscillations and is not involved in capacitative Ca 2+ entry in glial cells. J. Neurosci. 23, 4737–4745 (2003)PubMedGoogle Scholar
  27. N. Hamilton, S. Vayro, F. Kirchhoff, A. Verkhratsky, J. Robbins, D.C. Gorecki, A.M. Butt, Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 56, 734–749 (2008)PubMedCrossRefGoogle Scholar
  28. L. Heja, P. Barabas, G. Nyitrai, K.A. Kekesi, B. Lasztoczi, O. Toke, G. Tarkanyi, K. Madsen, A. Schousboe, A. Dobolyi, M. Palkovits, J. Kardos, Glutamate uptake triggers transporter-mediated GABA release from astrocytes. PLoS One 4, e7153 (2009)PubMedCrossRefGoogle Scholar
  29. M.T. Heneka, J.J. Rodriguez, A. Verkhratsky, Neuroglia in neurodegeneration. Brain Res. Rev. 63, 189–211 (2010)PubMedCrossRefGoogle Scholar
  30. L. Hertz, H.R. Zielke, Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci. 27, 735–743 (2004)PubMedCrossRefGoogle Scholar
  31. P. Illes, A. Verkhratsky, G. Burnstock, H. Franke, P2X receptors and their roles in astroglia in the central and peripheral nervous system. Neuroscientist (2011 in press; doi 1073858411418524)Google Scholar
  32. T. Isa, S. Itazawa, M. Iino, K. Tsuzuki, S. Ozawa, Distribution of neurones expressing inwardly rectifying and Ca2+-permeable AMPA receptors in rat hippocampal slices. J. Physiol. (Lond.) 491, 719–733 (1996)Google Scholar
  33. S.I. Itazawa, T. Isa, S. Ozawa, Inwardly rectifying and Ca2+-permeable AMPA-type glutamate receptor channels in rat neocortical neurons. J. Neurophysiol. 78, 2592–2601 (1997)PubMedGoogle Scholar
  34. R. Jabs, E. Guenther, K. Marquordt, T.H. Wheeler-Schilling, Evidence for P2X3, P2X4, P2X5 but not for P2X7 containing purinergic receptors in Muller cells of the rat retina. Brain Res. Mol. Brain Res. 76, 205–210 (2000)PubMedCrossRefGoogle Scholar
  35. G. James, A.M. Butt, P2X and P2Y purinoreceptors mediate ATP-evoked calcium signalling in optic nerve glia in situ. Cell Calcium 30, 251–259 (2001)PubMedCrossRefGoogle Scholar
  36. M. Juhaszova, M.P. Blaustein, Na+ pump low and high ouabain affinity alpha subunit isoforms are differently distributed in cells. Proc. Natl. Acad. Sci. U. S. A. 94, 1800–1805 (1997)PubMedCrossRefGoogle Scholar
  37. R. Kanjhan, G.D. Housley, P.R. Thorne, D.L. Christie, D.J. Palmer, L. Luo, A.F. Ryan, Localization of ATP-gated ion channels in cerebellum using P2x2R subunit-specific antisera. Neuroreport 7, 2665–2669 (1996)PubMedCrossRefGoogle Scholar
  38. R. Karadottir, P. Cavelier, L.H. Bergersen, D. Attwell, NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438, 1162–1166 (2005)PubMedCrossRefGoogle Scholar
  39. H. Kettenmann, B.R. Ransom (eds.), Neuroglia (OUP, Oxford, 2005)Google Scholar
  40. L. Kiedrowski, J.T. Wroblewski, E. Costa, Intracellular sodium concentration in cultured cerebellar granule cells challenged with glutamate. Mol. Pharmacol. 45, 1050–1054 (1994)PubMedGoogle Scholar
  41. H.K. Kimelberg, M. Nedergaard, Functions of astrocytes and their potential as therapeutic targets. Neurotherapeutics 7, 338–353 (2010)PubMedCrossRefGoogle Scholar
  42. H.K. Kimelberg, S. Pang, D.H. Treble, Excitatory amino acid-stimulated uptake of 22Na+ in primary astrocyte cultures. J. Neurosci. 9, 1141–1149 (1989)PubMedGoogle Scholar
  43. S. Kirischuk, H. Kettenmann, A. Verkhratsky, Na+/Ca2+ exchanger modulates kainate-triggered Ca2+ signaling in Bergmann glial cells in situ. FASEB J. 11, 566–572 (1997)PubMedGoogle Scholar
  44. S. Kirischuk, H. Kettenmann, A. Verkhratsky, Membrane currents and cytoplasmic sodium transients generated by glutamate transport in Bergmann glial cells. Pflugers Arch. 454, 245–252 (2007)PubMedCrossRefGoogle Scholar
  45. T. Knopfel, E. Guatteo, G. Bernardi, N.B. Mercuri, Hyperpolarization induces a rise in intracellular sodium concentration in dopamine cells of the substantia nigra pars compacta. Eur. J. Neurosci. 10, 1926–1929 (1998)PubMedCrossRefGoogle Scholar
  46. T. Kondoh, T. Nishizaki, H. Aihara, N. Tamaki, NMDA-responsible, APV-insensitive receptor in cultured human astrocytes. Life Sci. 68, 1761–1767 (2001)PubMedCrossRefGoogle Scholar
  47. M. Kukley, J.A. Barden, C. Steinhauser, R. Jabs, Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 36, 11–21 (2001)PubMedCrossRefGoogle Scholar
  48. U. Lalo, Y. Pankratov, F. Kirchhoff, R.A. North, A. Verkhratsky, NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. J. Neurosci. 26, 2673–2683 (2006)PubMedCrossRefGoogle Scholar
  49. U. Lalo, Y. Pankratov, S.P. Wichert, M.J. Rossner, R.A. North, F. Kirchhoff, A. Verkhratsky, P2X1 and P2X5 subunits form the functional P2X receptor in mouse cortical astrocytes. J. Neurosci. 28, 5473–5480 (2008)PubMedCrossRefGoogle Scholar
  50. U. Lalo, O. Palygin, R.A. North, A. Verkhratsky, Y. Pankratov, Age-dependent remodelling of ionotropic signalling in cortical astroglia. Aging Cell 10, 392–402 (2011a)PubMedCrossRefGoogle Scholar
  51. U. Lalo, Y. Pankratov, V. Parpura, A. Verkhratsky, Ionotropic receptors in neuronal-astroglial signalling: what is the role of “excitable” molecules in non-excitable cells. Biochim. Biophys. Acta 1813, 992–1002 (2011b)PubMedCrossRefGoogle Scholar
  52. U. Lalo, A. Verkhratsky, Y. Pankratov, Ionotropic ATP receptors in neuronal-glial communication. Semin. Cell Dev. Biol. 22, 220–228 (2011c)PubMedCrossRefGoogle Scholar
  53. A. Loesch, G. Burnstock, Electron-immunocytochemical localization of P2X1 receptors in the rat cerebellum. Cell Tissue Res. 294, 253–260 (1998)PubMedCrossRefGoogle Scholar
  54. T. Lopez, A.M. Lopez-Colome, A. Ortega, NMDA receptors in cultured radial glia. FEBS Lett. 405, 245–248 (1997)PubMedCrossRefGoogle Scholar
  55. P.J. Magistretti, Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209, 2304–2311 (2006)PubMedCrossRefGoogle Scholar
  56. P.J. Magistretti, Role of glutamate in neuron-glia metabolic coupling. Am. J. Clin. Nutr. 90, 875S–880S (2009)PubMedCrossRefGoogle Scholar
  57. E.B. Malarkey, Y. Ni, V. Parpura, Ca2+ entry through TRPC1 channels contributes to intracellular Ca2+ dynamics and consequent glutamate release from rat astrocytes. Glia 56, 821–835 (2008)PubMedCrossRefGoogle Scholar
  58. T. Matsuda, K. Takuma, E. Nishiguchi, H. Hashimoto, J. Azuma, A. Baba, Involvement of Na+-Ca2+ exchanger in reperfusion-induced delayed cell death of cultured rat astrocytes. Eur. J. Neurosci. 8, 951–958 (1996)PubMedCrossRefGoogle Scholar
  59. V. Matyash, H. Kettenmann, Heterogeneity in astrocyte morphology and physiology. Brain Res. Rev. 63, 2–10 (2010)PubMedCrossRefGoogle Scholar
  60. I. Micu, Q. Jiang, E. Coderre, A. Ridsdale, L. Zhang, J. Woulfe, X. Yin, B.D. Trapp, J.E. McRory, R. Rehak, G.W. Zamponi, W. Wang, P.K. Stys, NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439, 988–992 (2006)PubMedGoogle Scholar
  61. A. Minelli, P. Castaldo, P. Gobbi, S. Salucci, S. Magi, S. Amoroso, Cellular and subcellular localization of Na+-Ca2+ exchanger protein isoforms, NCX1, NCX2, and NCX3 in cerebral cortex and hippocampus of adult rat. Cell Calcium 41, 221–234 (2007)PubMedCrossRefGoogle Scholar
  62. T. Muller, T. Moller, T. Berger, J. Schnitzer, H. Kettenmann, Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells. Science 256, 1563–1566 (1992)PubMedCrossRefGoogle Scholar
  63. M. Nedergaard, J.J. Rodriguez, A. Verkhratsky, Glial calcium and diseases of the nervous system. Cell Calcium 47, 140–149 (2010)PubMedCrossRefGoogle Scholar
  64. T. Nishizaki, T. Matsuoka, T. Nomura, T. Kondoh, N. Tamaki, Y. Okada, Store Ca2+ depletion enhances NMDA responses in cultured human astrocytes. Biochem. Biophys. Res. Commun. 259, 661–664 (1999)PubMedCrossRefGoogle Scholar
  65. N.A. Oberheim, X. Wang, S. Goldman, M. Nedergaard, Astrocytic complexity distinguishes the human brain. Trends Neurosci. 29, 547–553 (2006)PubMedCrossRefGoogle Scholar
  66. J.F. Oliveira, T. Riedel, A. Leichsenring, C. Heine, H. Franke, U. Krugel, W. Norenberg, P. Illes, Rodent cortical astroglia express in situ functional P2X7 receptors sensing pathologically high ATP concentrations. Cereb. Cortex 21, 806–820 (2011)PubMedCrossRefGoogle Scholar
  67. S.G. Owe, P. Marcaggi, D. Attwell, The ionic stoichiometry of the GLAST glutamate transporter in salamander retinal glia. J. Physiol. (Lond.) 577, 591–599 (2006)CrossRefGoogle Scholar
  68. S. Paluzzi, S. Alloisio, S. Zappettini, M. Milanese, L. Raiteri, M. Nobile, G. Bonanno, Adult astroglia is competent for Na+/Ca2+ exchanger-operated exocytotic glutamate release triggered by mild depolarization. J. Neurochem. 103, 1196–1207 (2007)PubMedCrossRefGoogle Scholar
  69. O. Palygin, U. Lalo, A. Verkhratsky, Y. Pankratov, Ionotropic NMDA and P2X1/5 receptors mediate synaptically induced Ca2+ signalling in cortical astrocytes. Cell Calcium 48, 225–231 (2010)PubMedCrossRefGoogle Scholar
  70. O. Palygin, U. Lalo, Y. Pankratov, Distinct pharmacological and functional properties of NMDA receptors in mouse cortical astrocytes. Br. J. Pharmacol. 163, 1755–1766 (2011)PubMedCrossRefGoogle Scholar
  71. Y. Pankratov, U. Lalo, O.A. Krishtal, A. Verkhratsky, P2X receptors and synaptic plasticity. Neuroscience 158, 137–148 (2009)PubMedCrossRefGoogle Scholar
  72. V. Parpura, V. Grubisic, A. Verkhratsky, Ca2+ sources for the exocytotic release of glutamate from astrocytes. Biochim. Biophys. Acta 1813, 984–991 (2011)PubMedCrossRefGoogle Scholar
  73. O. Peters, S.L. Palay, H. deF Webster, The Fine Structure of the Nervous System (Oxford University Press, Oxford, 1991)Google Scholar
  74. A. Pisani, P. Calabresi, A. Tozzi, G. Bernardi, T. Knopfel, Early sodium elevations induced by combined oxygen and glucose deprivation in pyramidal cortical neurons. Eur. J. Neurosci. 10, 3572–3574 (1998)PubMedCrossRefGoogle Scholar
  75. P. Pizzo, A. Burgo, T. Pozzan, C. Fasolato, Role of capacitative calcium entry on glutamate-induced calcium influx in type-I rat cortical astrocytes. J. Neurochem. 79, 98–109 (2001)PubMedCrossRefGoogle Scholar
  76. D.G. Puro, J.P. Yuan, N.J. Sucher, Activation of NMDA receptor-channels in human retinal Muller glial cells inhibits inward-rectifying potassium currents. Vis. Neurosci. 13, 319–326 (1996)PubMedCrossRefGoogle Scholar
  77. R.C. Reyes, A. Verkhratsky, V. Parpura, Plasmalemmal Na+/Ca2+ exchanger modulates Ca2+-dependent exocytotic release of glutamate from rat cortical astrocytes ASN Neuro 4(1). pii: e00075. doi: 10.1042/AN20110059 (2012)Google Scholar
  78. J.J. Rodriguez, M. Olabarria, A. Chvatal, A. Verkhratsky, Astroglia in dementia and Alzheimer’s disease. Cell Death Differ. 16, 378–385 (2009)PubMedCrossRefGoogle Scholar
  79. H. Rojas, C. Colina, M. Ramos, G. Benaim, E.H. Jaffe, C. Caputo, R. DiPolo, Na+ entry via glutamate transporter activates the reverse Na+/Ca2+ exchange and triggers Cai2+-induced Ca2+ release in rat cerebellar Type-1 astrocytes. J. Neurochem. 100, 1188–1202 (2007)PubMedCrossRefGoogle Scholar
  80. C.R. Rose, B.R. Ransom, Intracellular sodium homeostasis in rat hippocampal astrocytes. J. Physiol. (Lond.) 491(Pt 2), 291–305 (1996a)Google Scholar
  81. C.R. Rose, B.R. Ransom, Mechanisms of H+ and Na+ changes induced by glutamate, kainate, and D-aspartate in rat hippocampal astrocytes. J. Neurosci. 16, 5393–5404 (1996b)PubMedGoogle Scholar
  82. C.R. Rose, B.R. Ransom, Gap junctions equalize intracellular Na+ concentration in astrocytes. Glia 20, 299–307 (1997)PubMedCrossRefGoogle Scholar
  83. M.G. Salter, R. Fern, NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438, 1167–1171 (2005)PubMedCrossRefGoogle Scholar
  84. C.G. Schipke, C. Ohlemeyer, M. Matyash, C. Nolte, H. Kettenmann, F. Kirchhoff, Astrocytes of the mouse neocortex express functional N-methyl-D-aspartate receptors. FASEB J. 15, 1270–1272 (2001)PubMedGoogle Scholar
  85. G. Seifert, C. Steinhauser, Glial cells in the mouse hippocampus express AMPA receptors with an intermediate Ca2+ permeability. Eur. J. Neurosci. 7, 1872–1881 (1995)PubMedCrossRefGoogle Scholar
  86. G. Seifert, C. Steinhauser, Ionotropic glutamate receptors in astrocytes. Prog. Brain Res. 132, 287–299 (2001)PubMedCrossRefGoogle Scholar
  87. C. Steinhäuser, V. Gallo, News on glutamate receptors in glial cells. Trends Neurosci. 19, 339–345 (1996)PubMedCrossRefGoogle Scholar
  88. C. Strubing, G. Krapivinsky, L. Krapivinsky, D.E. Clapham, TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29, 645–655 (2001)PubMedCrossRefGoogle Scholar
  89. C. Strubing, G. Krapivinsky, L. Krapivinsky, D.E. Clapham, Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J. Biol. Chem. 278, 39014–39019 (2003)PubMedCrossRefGoogle Scholar
  90. K. Takuma, T. Matsuda, H. Hashimoto, S. Asano, A. Baba, Cultured rat astrocytes possess Na+-Ca2+ exchanger. Glia 12, 336–342 (1994)PubMedCrossRefGoogle Scholar
  91. A. Verkhratsky, Calcium ions and integration in neural circuits. Acta Physiol (Oxf.) 187, 357–369 (2006)CrossRefGoogle Scholar
  92. A. Verkhratsky, Neuronismo y reticulismo: neuronal-glial circuits unify the reticular and neuronal theories of brain organization. Acta Physiol (Oxf.) 195, 111–122 (2009)CrossRefGoogle Scholar
  93. A. Verkhratsky, Physiology of neuronal-glial networking. Neurochem. Int. 57, 332–343 (2011)CrossRefGoogle Scholar
  94. A. Verkhratsky, A. Butt, Glial Neurobiology. A textbook (Wiley, Chichester, 2007)CrossRefGoogle Scholar
  95. A. Verkhratsky, F. Kirchhoff, Glutamate-mediated neuronal-glial transmission. J. Anat. 210, 651–660 (2007a)PubMedCrossRefGoogle Scholar
  96. A. Verkhratsky, F. Kirchhoff, NMDA receptors in Glia. Neuroscientist 13, 28–37 (2007b)PubMedCrossRefGoogle Scholar
  97. A. Verkhratsky, C. Steinhauser, Ion channels in glial cells. Brain Res. Brain Res. Rev. 32, 380–412 (2000)PubMedCrossRefGoogle Scholar
  98. A. Verkhratsky, R.K. Orkand, H. Kettenmann, Glial calcium: homeostasis and signaling function. Physiol. Rev. 78, 99–141 (1998)PubMedGoogle Scholar
  99. A. Verkhratsky, O.A. Krishtal, G. Burnstock, Purinoceptors on neuroglia. Mol. Neurobiol. 39, 190–208 (2009)PubMedCrossRefGoogle Scholar
  100. A. Verkhratsky, V. Parpura, J.J. Rodriguez, Where the thoughts dwell: the physiology of neuronal-glial “diffuse neural net”. Brain Res. Rev. 66, 133–151 (2011)PubMedCrossRefGoogle Scholar
  101. B. Voutsinos-Porche, G. Bonvento, K. Tanaka, P. Steiner, E. Welker, J.Y. Chatton, P.J. Magistretti, L. Pellerin, Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 37, 275–286 (2003)PubMedCrossRefGoogle Scholar
  102. Y. Wu, W. Wang, A. Diez-Sampedro, G.B. Richerson, Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56, 851–865 (2007)PubMedCrossRefGoogle Scholar
  103. N. Zerangue, M.P. Kavanaugh, Flux coupling in a neuronal glutamate transporter. Nature 383, 634–637 (1996)PubMedCrossRefGoogle Scholar
  104. D. Ziak, A. Chvatal, E. Sykova, Glutamate-, kainate- and NMDA-evoked membrane currents in identified glial cells in rat spinal cord slice. Physiol. Res. 47, 365–375 (1998)PubMedGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Alexei Verkhratsky
    • 1
    • 2
    • 3
  • Mami Noda
    • 4
  • Vladimir Parpura
    • 2
    • 3
    • 5
    • 6
  • Sergei Kirischuk
    • 7
  1. 1.Faculty of Life SciencesThe University of ManchesterManchesterUK
  2. 2.IKERBASQUE, Basque Foundation for ScienceBilbaoSpain
  3. 3.Department of NeurosciencesUniversity of the Basque Country UPV/EHULeioaSpain
  4. 4.Laboratory of Pathophysiology, Graduate School of Pharmaceutical SciencesKyushu UniversityFukuokaJapan
  5. 5.Department of Neurobiology, Center for Glial Biology in Medicine, Civitan International Research Center, Atomic Force Microscopy & Nanotechnology Laboratories, and Evelyn F. McKnight Brain InstituteUniversity of AlabamaBirminghamUSA
  6. 6.Department of BiotechnologyUniversity of RijekaRijekaCroatia
  7. 7.Institute of Physiology and PathophysiologyUniversal Medical Center of the Johannes Gutenberg, University MainzMainzGermany

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