Skip to main content

Advertisement

SpringerLink
Log in

GABAA Receptor and Glycine Receptor Activation by Paracrine/Autocrine Release of Endogenous Agonists: More Than a Simple Communication Pathway

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

It is a common and widely accepted assumption that glycine and GABA are the main inhibitory transmitters in the central nervous system (CNS). But, in the past 20 years, several studies have clearly demonstrated that these amino acids can also be excitatory in the immature central nervous system. In addition, it is now established that both GABA receptors (GABARs) and glycine receptors (GlyRs) can be located extrasynaptically and can be activated by paracrine release of endogenous agonists, such as GABA, glycine, and taurine. Recently, non-synaptic release of GABA, glycine, and taurine gained further attention with increasing evidence suggesting a developmental role of these neurotransmitters in neuronal network formation before and during synaptogenesis. This review summarizes recent knowledge about the non-synaptic activation of GABAARs and GlyRs, both in developing and adult CNS. We first present studies that reveal the functional specialization of both non-synaptic GABAARs and GlyRs and we discuss the neuronal versus non-neuronal origin of the paracrine release of GABAAR and GlyR agonists. We then discuss the proposed non-synaptic release mechanisms and/or pathways for GABA, glycine, and taurine. Finally, we summarize recent data about the various roles of non-synaptic GABAergic and glycinergic systems during the development of neuronal networks and in the adult.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Nguyen L, Rigo JM, Rocher V et al (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 305:187–202

    Article  PubMed  CAS  Google Scholar 

  2. Angulo MC, Le Meur K, Kozlov AS, Charpak S, Audinat E (2008) GABA, a forgotten gliotransmitter. Prog Neurobiol 86:297–303

    Article  PubMed  CAS  Google Scholar 

  3. Hamilton NB, Attwell D (2010) Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11:227–238

    Article  PubMed  CAS  Google Scholar 

  4. Represa A, Ben-Ari Y (2005) Trophic actions of GABA on neuronal development. Trends Neurosci 28:278–283

    Article  PubMed  CAS  Google Scholar 

  5. Warskulat U, Heller-Stilb B, Oermann E et al (2007) Phenotype of the taurine transporter knockout mouse. Meth Enzymol 428:439–458

    Article  PubMed  CAS  Google Scholar 

  6. Nguyen L, Malgrange B, Breuskin I et al (2003) Autocrine/paracrine activation of the GABA(A) receptor inhibits the proliferation of neurogenic polysialylated neural cell adhesion molecule-positive (PSA-NCAM+) precursor cells from postnatal striatum. J Neurosci 23:3278–3294

    PubMed  CAS  Google Scholar 

  7. Wang DD, Kriegstein AR (2009) Defining the role of GABA in cortical development. J Physiol 587:1873–1879

    Article  PubMed  CAS  Google Scholar 

  8. Hanson MG, Landmesser LT (2003) Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 23:587–600

    PubMed  CAS  Google Scholar 

  9. Scain AL, Le Corronc H, Allain AE et al (2010) Glycine release from radial cells modulates the spontaneous activity and its propagation during early spinal cord development. J Neurosci 30:390–403

    Article  PubMed  CAS  Google Scholar 

  10. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353–360

    Article  PubMed  CAS  Google Scholar 

  11. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416:303–325

    PubMed  CAS  Google Scholar 

  12. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87:1215–1284

    Article  PubMed  CAS  Google Scholar 

  13. Watt AJ, Cuntz H, Mori M, Nusser Z, Sjostrom PJ, Hausser M (2009) Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity. Nat Neurosci 12:463–473

    Article  PubMed  CAS  Google Scholar 

  14. Owens DF, Boyce LH, Davis MB, Kriegstein AR (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16:6414–6423

    PubMed  CAS  Google Scholar 

  15. Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728–739

    Article  PubMed  CAS  Google Scholar 

  16. Delpy A, Allain AE, Meyrand P, Branchereau P (2008) NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron. J Physiol 586:1059–1075

    Article  PubMed  CAS  Google Scholar 

  17. Demarque M, Represa A, Becq H, Khalilov I, Ben-Ari Y, Aniksztejn L (2002) Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36:1051–1061

    Article  PubMed  CAS  Google Scholar 

  18. Flint AC, Liu X, Kriegstein AR (1998) Nonsynaptic glycine receptor activation during early neocortical development. Neuron 20:43–53

    Article  PubMed  CAS  Google Scholar 

  19. Lynch JW (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol Rev 84:1051–1095

    Article  PubMed  CAS  Google Scholar 

  20. Grudzinska J, Schemm R, Haeger S et al (2005) The beta subunit determines the ligand binding properties of synaptic glycine receptors. Neuron 45:727–739

    Article  PubMed  CAS  Google Scholar 

  21. Kirsch J, Betz H (1993) Widespread expression of gephyrin, a putative glycine receptor–tubulin linker protein, in rat brain. Brain Res 621:301–310

    Article  PubMed  CAS  Google Scholar 

  22. Legendre P (2001) The glycinergic inhibitory synapse. Cell Mol Life Sci 58:760–793

    Article  PubMed  CAS  Google Scholar 

  23. Becker CM, Schmieden V, Tarroni P, Strasser U, Betz H (1992) Isoform-selective deficit of glycine receptors in the mouse mutant spastic. Neuron 8:283–289

    Article  PubMed  CAS  Google Scholar 

  24. Kuhse J, Kuryatov A, Maulet Y, Malosio ML, Schmieden V, Betz H (1991) Alternative splicing generates two isoforms of the alpha 2 subunit of the inhibitory glycine receptor. FEBS Lett 283:73–77

    Article  PubMed  CAS  Google Scholar 

  25. Racca C, Gardiol A, Triller A (1998) Cell-specific dendritic localization of glycine receptor alpha subunit messenger RNAs. Neuroscience 84:997–1012

    Article  PubMed  CAS  Google Scholar 

  26. Malosio ML, Marqueze-Pouey B, Kuhse J, Betz H (1991) Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J 10:2401–2409

    PubMed  CAS  Google Scholar 

  27. Piechotta K, Weth F, Harvey RJ, Friauf E (2001) Localization of rat glycine receptor alpha1 and alpha2 subunit transcripts in the developing auditory brainstem. J Comp Neurol 438:336–352

    Article  PubMed  CAS  Google Scholar 

  28. Singer JH, Talley EM, Bayliss DA, Berger AJ (1998) Development of glycinergic synaptic transmission to rat brain stem motoneurons. J Neurophysiol 80:2608–2620

    PubMed  CAS  Google Scholar 

  29. Sato K, Kiyama H, Tohyama M (1992) Regional distribution of cells expressing glycine receptor alpha 2 subunit mRNA in the rat brain. Brain Res 590:95–108

    Article  PubMed  CAS  Google Scholar 

  30. Heinze L, Harvey RJ, Haverkamp S, Wassle H (2007) Diversity of glycine receptors in the mouse retina: localization of the alpha4 subunit. J Comp Neurol 500:693–707

    Article  PubMed  CAS  Google Scholar 

  31. Macdonald RL, Olsen RW (1994) GABAA receptor channels. Annu Rev Neurosci 17:569–602

    Article  PubMed  CAS  Google Scholar 

  32. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215–229

    Article  PubMed  CAS  Google Scholar 

  33. Enz R, Cutting GR (1999) GABAC receptor rho subunits are heterogeneously expressed in the human CNS and form homo- and heterooligomers with distinct physical properties. Eur J Neurosci 11:41–50

    Article  PubMed  CAS  Google Scholar 

  34. Koulen P, Brandstatter JH, Enz R, Bormann J, Wassle H (1998) Synaptic clustering of GABA(C) receptor rho-subunits in the rat retina. Eur J Neurosci 10:115–127

    Article  PubMed  CAS  Google Scholar 

  35. Rozzo A, Armellin M, Franzot J, Chiaruttini C, Nistri A, Tongiorgi E (2002) Expression and dendritic mRNA localization of GABAC receptor rho1 and rho2 subunits in developing rat brain and spinal cord. Eur J Neurosci 15:1747–1758

    Article  PubMed  Google Scholar 

  36. Wegelius K, Pasternack M, Hiltunen JO et al (1998) Distribution of GABA receptor rho subunit transcripts in the rat brain. Eur J Neurosci 10:350–357

    Article  PubMed  CAS  Google Scholar 

  37. Jost B, Grabert J, Patz S, Schmidt M, Wahle P (2006) GABAC receptor subunit mRNA expression in the rat superior colliculus is regulated by calcium channels, neurotrophins, and GABAC receptor activity. Brain Cell Biol 35:251–266

    Article  PubMed  CAS  Google Scholar 

  38. Tretter V, Ehya N, Fuchs K, Sieghart W (1997) Stoichiometry and assembly of a recombinant GABAA receptor subtype. J Neurosci 17:2728–2737

    PubMed  CAS  Google Scholar 

  39. Farrar SJ, Whiting PJ, Bonnert TP, McKernan RM (1999) Stoichiometry of a ligand-gated ion channel determined by fluorescence energy transfer. J Biol Chem 274:10100–10104

    Article  PubMed  CAS  Google Scholar 

  40. Wisden W, Cope D, Klausberger T et al (2002) Ectopic expression of the GABA(A) receptor alpha6 subunit in hippocampal pyramidal neurons produces extrasynaptic receptors and an increased tonic inhibition. Neuropharmacology 43:530–549

    Article  PubMed  CAS  Google Scholar 

  41. Fritschy JM, Mohler H (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154–194

    Article  PubMed  CAS  Google Scholar 

  42. Ma W, Saunders PA, Somogyi R, Poulter MO, Barker JL (1993) Ontogeny of GABAA receptor subunit mRNAs in rat spinal cord and dorsal root ganglia. J Comp Neurol 338:337–359

    Article  PubMed  CAS  Google Scholar 

  43. Wisden W, Laurie DJ, Monyer H, Seeburg PH (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040–1062

    PubMed  CAS  Google Scholar 

  44. Laurie DJ, Wisden W, Seeburg PH (1992) The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain III. Embryonic and postnatal development. J Neurosci 12:4151–4172

    PubMed  CAS  Google Scholar 

  45. Sieghart W, Sperk G (2002) Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem 2:795–816

    Article  PubMed  CAS  Google Scholar 

  46. Whiting PJ (2003) GABA-A receptor subtypes in the brain: a paradigm for CNS drug discovery? Drug Discov Today 8:445–450

    Article  PubMed  CAS  Google Scholar 

  47. Paysan J, Fritschy JM (1998) GABAA-receptor subtypes in developing brain. Actors or spectators? Perspect Dev Neurobiol 5:179–192

    PubMed  CAS  Google Scholar 

  48. Mohler H, Knoflach F, Paysan J et al (1995) Heterogeneity of GABAA-receptors: cell-specific expression, pharmacology, and regulation. Neurochem Res 20:631–636

    Article  PubMed  CAS  Google Scholar 

  49. Wisden W, Gundlach AL, Barnard EA, Seeburg PH, Hunt SP (1991) Distribution of GABAA receptor subunit mRNAs in rat lumbar spinal cord. Brain Res Mol Brain Res 10:179–183

    Article  PubMed  CAS  Google Scholar 

  50. Clements JD (1996) Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19:163–171

    Article  PubMed  CAS  Google Scholar 

  51. Miller PS, Harvey RJ, Smart TG (2004) Differential agonist sensitivity of glycine receptor alpha2 subunit splice variants. Br J Pharmacol 143:19–26

    Article  PubMed  CAS  Google Scholar 

  52. Mangin JM, Baloul M, Prado De Carvalho L, Rogister B, Rigo JM, Legendre P (2003) Kinetic properties of the alpha2 homo-oligomeric glycine receptor impairs a proper synaptic functioning. J Physiol 553:369–386

    Article  PubMed  CAS  Google Scholar 

  53. Nusser Z, Sieghart W, Somogyi P (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18:1693–1703

    PubMed  CAS  Google Scholar 

  54. Brunig I, Scotti E, Sidler C, Fritschy JM (2002) Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443:43–55

    Article  PubMed  CAS  Google Scholar 

  55. Crestani F, Keist R, Fritschy JM et al (2002) Trace fear conditioning involves hippocampal alpha5 GABA(A) receptors. Proc Natl Acad Sci USA 99:8980–8985

    Article  PubMed  CAS  Google Scholar 

  56. Storustovu SI, Ebert B (2006) Pharmacological characterization of agonists at delta-containing GABAA receptors: functional selectivity for extrasynaptic receptors is dependent on the absence of gamma2. J Pharmacol Exp Ther 316:1351–1359

    Article  PubMed  CAS  Google Scholar 

  57. Gingrich KJ, Roberts WA, Kass RS (1995) Dependence of the GABAA receptor gating kinetics on the alpha-subunit isoform: implications for structure–function relations and synaptic transmission. J Physiol 489(Pt 2):529–543

    PubMed  CAS  Google Scholar 

  58. Koch U, Magnusson AK (2009) Unconventional GABA release: mechanisms and function. Curr Opin Neurobiol 19:305–310

    Article  PubMed  CAS  Google Scholar 

  59. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287–1298

    Article  PubMed  CAS  Google Scholar 

  60. Cope DW, Hughes SW, Crunelli V (2005) GABAA receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25:11553–11563

    Article  PubMed  CAS  Google Scholar 

  61. Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87:2624–2628

    PubMed  CAS  Google Scholar 

  62. Brickley SG, Cull-Candy SG, Farrant M (1996) Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J Physiol 497(Pt 3):753–759

    PubMed  CAS  Google Scholar 

  63. Salin PA, Prince DA (1996) Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol 75:1573–1588

    PubMed  CAS  Google Scholar 

  64. Bieda MC, MacIver MB (2004) Major role for tonic GABAA conductances in anesthetic suppression of intrinsic neuronal excitability. J Neurophysiol 92:1658–1667

    Article  PubMed  CAS  Google Scholar 

  65. Marchionni I, Omrani A, Cherubini E (2007) In the developing rat hippocampus a tonic GABAA-mediated conductance selectively enhances the glutamatergic drive of principal cells. J Physiol 581:515–528

    Article  PubMed  CAS  Google Scholar 

  66. Olah S, Fule M, Komlosi G et al (2009) Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461:1278–1281

    Article  PubMed  CAS  Google Scholar 

  67. Durkin MM, Smith KE, Borden LA, Weinshank RL, Branchek TA, Gustafson EL (1995) Localization of messenger RNAs encoding three GABA transporters in rat brain: an in situ hybridization study. Brain Res Mol Brain Res 33:7–21

    Article  PubMed  CAS  Google Scholar 

  68. Neal MJ, Cunningham JR, Shah MA (1989) Excitatory amino acid receptors and transmitter release in the retina. Neurochem Int 14:407–412

    Article  PubMed  CAS  Google Scholar 

  69. Benagiano V, Flace P, Virgintino D, Rizzi A, Roncali L, Ambrosi G (2000) Immunolocalization of glutamic acid decarboxylase in postmortem human cerebellar cortex. A light microscopy study. Histochem Cell Biol 114:191–195

    PubMed  CAS  Google Scholar 

  70. Lee M, Schwab C, McGeer PL (2011) Astrocytes are GABAergic cells that modulate microglial activity. Glia 59:152–165

    Article  PubMed  Google Scholar 

  71. Martinez-Rodriguez R, Tonda A, Gragera RR et al (1993) Synaptic and non-synaptic immunolocalization of GABA and glutamate acid decarboxylase (GAD) in cerebellar cortex of rat. Cell Mol Biol (Noisy-le-grand) 39:115–123

    CAS  Google Scholar 

  72. Ochi S, Lim JY, Rand MN, During MJ, Sakatani K, Kocsis JD (1993) Transient presence of GABA in astrocytes of the developing optic nerve. Glia 9:188–198

    Article  PubMed  CAS  Google Scholar 

  73. Watanabe M, Maemura K, Kanbara K, Tamayama T, Hayasaki H (2002) GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 213:1–47

    Article  PubMed  CAS  Google Scholar 

  74. Kwakowsky A, Schwirtlich M, Zhang Q et al (2007) GAD isoforms exhibit distinct spatiotemporal expression patterns in the developing mouse lens: correlation with Dlx2 and Dlx5. Dev Dyn 236:3532–3544

    Article  PubMed  CAS  Google Scholar 

  75. Szabo G, Katarova Z, Greenspan R (1994) Distinct protein forms are produced from alternatively spliced bicistronic glutamic acid decarboxylase mRNAs during development. Mol Cell Biol 14:7535–7545

    PubMed  CAS  Google Scholar 

  76. Varju P, Katarova Z, Madarasz E, Szabo G (2001) GABA signalling during development: new data and old questions. Cell Tissue Res 305:239–246

    Article  PubMed  CAS  Google Scholar 

  77. Varju P, Katarova Z, Madarasz E, Szabo G (2002) Sequential induction of embryonic and adult forms of glutamic acid decarboxylase during in vitro-induced neurogenesis in cloned neuroectodermal cell-line, NE-7C2. J Neurochem 80:605–615

    Article  PubMed  CAS  Google Scholar 

  78. Behar T, Ma W, Hudson L, Barker JL (1994) Analysis of the anatomical distribution of GAD67 mRNA encoding truncated glutamic acid decarboxylase proteins in the embryonic rat brain. Brain Res Dev Brain Res 77:77–87

    Article  PubMed  CAS  Google Scholar 

  79. Katarova Z, Sekerkova G, Prodan S, Mugnaini E, Szabo G (2000) Domain-restricted expression of two glutamic acid decarboxylase genes in midgestation mouse embryos. J Comp Neurol 424:607–627

    Article  PubMed  CAS  Google Scholar 

  80. Ma W, Behar T, Chang L, Barker JL (1994) Transient increase in expression of GAD65 and GAD67 mRNAs during postnatal development of rat spinal cord. J Comp Neurol 346:151–160

    Article  PubMed  CAS  Google Scholar 

  81. Fenalti G, Law RH, Buckle AM et al (2007) GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop. Nat Struct Mol Biol 14:280–286

    Article  PubMed  CAS  Google Scholar 

  82. Battaglioli G, Liu H, Martin DL (2003) Kinetic differences between the isoforms of glutamate decarboxylase: implications for the regulation of GABA synthesis. J Neurochem 86:879–887

    Article  PubMed  CAS  Google Scholar 

  83. Christgau S, Aanstoot HJ, Schierbeck H et al (1992) Membrane anchoring of the autoantigen GAD65 to microvesicles in pancreatic beta-cells by palmitoylation in the NH2-terminal domain. J Cell Biol 118:309–320

    Article  PubMed  CAS  Google Scholar 

  84. Christgau S, Schierbeck H, Aanstoot HJ et al (1991) Pancreatic beta cells express two autoantigenic forms of glutamic acid decarboxylase, a 65-kDa hydrophilic form and a 64-kDa amphiphilic form which can be both membrane-bound and soluble. J Biol Chem 266:21257–21264

    PubMed  CAS  Google Scholar 

  85. Shi Y, Veit B, Baekkeskov S (1994) Amino acid residues 24–31 but not palmitoylation of cysteines 30 and 45 are required for membrane anchoring of glutamic acid decarboxylase, GAD65. J Cell Biol 124:927–934

    Article  PubMed  CAS  Google Scholar 

  86. Kanaani J, Patterson G, Schaufele F, Lippincott-Schwartz J, Baekkeskov S (2008) A palmitoylation cycle dynamically regulates partitioning of the GABA-synthesizing enzyme GAD65 between ER-Golgi and post-Golgi membranes. J Cell Sci 121:437–449

    Article  PubMed  CAS  Google Scholar 

  87. Dirkx R Jr, Thomas A, Li L et al (1995) Targeting of the 67-kDa isoform of glutamic acid decarboxylase to intracellular organelles is mediated by its interaction with the NH2-terminal region of the 65-kDa isoform of glutamic acid decarboxylase. J Biol Chem 270:2241–2246

    Article  PubMed  CAS  Google Scholar 

  88. Solimena M, Aggujaro D, Muntzel C et al (1993) Association of GAD-65, but not of GAD-67, with the Golgi complex of transfected Chinese hamster ovary cells mediated by the N-terminal region. Proc Natl Acad Sci USA 90:3073–3077

    Article  PubMed  CAS  Google Scholar 

  89. Kanaani J, Lissin D, Kash SF, Baekkeskov S (1999) The hydrophilic isoform of glutamate decarboxylase, GAD67, is targeted to membranes and nerve terminals independent of dimerization with the hydrophobic membrane-anchored isoform, GAD65. J Biol Chem 274:37200–37209

    Article  PubMed  CAS  Google Scholar 

  90. Asada H, Kawamura Y, Maruyama K et al (1996) Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem Biophys Res Commun 229:891–895

    Article  PubMed  CAS  Google Scholar 

  91. Kanaani J, Kolibachuk J, Martinez H, Baekkeskov S (2010) Two distinct mechanisms target GAD67 to vesicular pathways and presynaptic clusters. J Cell Biol 190:911–925

    Article  PubMed  CAS  Google Scholar 

  92. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14:1834–1855

    PubMed  CAS  Google Scholar 

  93. Houser CR, Esclapez M (1994) Localization of mRNAs encoding two forms of glutamic acid decarboxylase in the rat hippocampal formation. Hippocampus 4:530–545

    Article  PubMed  CAS  Google Scholar 

  94. Dupuy ST, Houser CR (1996) Prominent expression of two forms of glutamate decarboxylase in the embryonic and early postnatal rat hippocampal formation. J Neurosci 16:6919–6932

    PubMed  CAS  Google Scholar 

  95. Kaufman DL, Houser CR, Tobin AJ (1991) Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neurochem 56:720–723

    Article  PubMed  CAS  Google Scholar 

  96. Martin DL, Rimvall K (1993) Regulation of gamma-aminobutyric acid synthesis in the brain. J Neurochem 60:395–407

    Article  PubMed  CAS  Google Scholar 

  97. Eliasson MJ, McCaffery P, Baughman RW, Drager UC (1997) A ventrodorsal GABA gradient in the embryonic retina prior to expression of glutamate decarboxylase. Neuroscience 79:863–869

    Article  PubMed  CAS  Google Scholar 

  98. Seiler N, Al-Therib MJ, Kataoka K (1973) Formation of GABA from putrescine in the brain of fish (Salmo irideus Gibb.). J Neurochem 20:699–708

    Article  PubMed  CAS  Google Scholar 

  99. Seiler N, Knodgen B (1971) Transformation of glutamic acid, putrescine and ornithine into gamma-aminobutyric acid in brain. Hoppe Seylers Z Physiol Chem 352:97–105

    Article  PubMed  CAS  Google Scholar 

  100. Kremzner LT, Hiller JM, Simon EJ (1975) Metabolism of polyamines in mouse neuroblastoma cells in culture: formation of GABA and putreanine. J Neurochem 25:889–894

    Article  PubMed  CAS  Google Scholar 

  101. Konishi H, Nakajima T, Sano I (1977) Metabolism of putrescine in the central nervous system. J Biochem 81:355–360

    PubMed  CAS  Google Scholar 

  102. Seiler N, Bink G, Grove J (1980) Relationships between GABA and polyamines in developing rat brain. Neuropharmacology 19:251–258

    Article  PubMed  CAS  Google Scholar 

  103. Laschet J, Grisar T, Bureau M, Guillaume D (1992) Characteristics of putrescine uptake and subsequent GABA formation in primary cultured astrocytes from normal C57BL/6J and epileptic DBA/2J mouse brain cortices. Neuroscience 48:151–157

    Article  PubMed  CAS  Google Scholar 

  104. Sequerra EB, Gardino P, Hedin-Pereira C, de Mello FG (2007) Putrescine as an important source of GABA in the postnatal rat subventricular zone. Neuroscience 146:489–493

    Article  PubMed  CAS  Google Scholar 

  105. Barres BA, Koroshetz WJ, Swartz KJ, Chun LL, Corey DP (1990) Ion channel expression by white matter glia: the O-2A glial progenitor cell. Neuron 4:507–524

    Article  PubMed  CAS  Google Scholar 

  106. Doretto MC, Burger RL, Mishra PK, Garcia-Cairasco N, Dailey JW, Jobe PC (1994) A microdialysis study of amino acid concentrations in the extracellular fluid of the substantia nigra of freely behaving GEPR-9s: relationship to seizure predisposition. Epilepsy Res 17:157–165

    Article  PubMed  CAS  Google Scholar 

  107. Dopico JG, Gonzalez-Hernandez T, Perez IM et al (2006) Glycine release in the substantia nigra: interaction with glutamate and GABA. Neuropharmacology 50:548–557

    Article  PubMed  CAS  Google Scholar 

  108. Martina M, B-Turcotte ME, Halman S et al (2005) Reduced glycine transporter type 1 expression leads to major changes in glutamatergic neurotransmission of CA1 hippocampal neurones in mice. J Physiol 563:777–793

    Article  PubMed  CAS  Google Scholar 

  109. Martina M, Gorfinkel Y, Halman S et al (2004) Glycine transporter type 1 blockade changes NMDA receptor-mediated responses and LTP in hippocampal CA1 pyramidal cells by altering extracellular glycine levels. J Physiol 557:489–500

    Article  PubMed  CAS  Google Scholar 

  110. Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325:529–531

    Article  PubMed  CAS  Google Scholar 

  111. Keck T, Lillis KP, Zhou YD, White JA (2008) Frequency-dependent glycinergic inhibition modulates plasticity in hippocampus. J Neurosci 28:7359–7369

    Article  PubMed  CAS  Google Scholar 

  112. Luna-Munguia H, Meneses A, Pena-Ortega F, Gaona A, Rocha L (2010) Effects of hippocampal high-frequency electrical stimulation in memory formation and their association with amino acid tissue content and release in normal rats. Hippocampus [Epub ahead of print]

  113. Huang H, Barakat L, Wang D, Bordey A (2004) Bergmann glial GlyT1 mediates glycine uptake and release in mouse cerebellar slices. J Physiol 560:721–736

    Article  PubMed  CAS  Google Scholar 

  114. Zafra F, Aragon C, Olivares L, Danbolt NC, Gimenez C, Storm-Mathisen J (1995) Glycine transporters are differentially expressed among CNS cells. J Neurosci 15:3952–3969

    PubMed  CAS  Google Scholar 

  115. Zafra F, Gomeza J, Olivares L, Aragon C, Gimenez C (1995) Regional distribution and developmental variation of the glycine transporters GLYT1 and GLYT2 in the rat CNS. Eur J Neurosci 7:1342–1352

    Article  PubMed  CAS  Google Scholar 

  116. Poyatos I, Ponce J, Aragon C, Gimenez C, Zafra F (1997) The glycine transporter GLYT2 is a reliable marker for glycine-immunoreactive neurons. Brain Res Mol Brain Res 49:63–70

    Article  PubMed  CAS  Google Scholar 

  117. Aragon C, Lopez-Corcuera B (2003) Structure, function and regulation of glycine neurotransporters. Eur J Pharmacol 479:249–262

    Article  PubMed  CAS  Google Scholar 

  118. Eulenburg V, Armsen W, Betz H, Gomeza J (2005) Glycine transporters: essential regulators of neurotransmission. Trends Biochem Sci 30:325–333

    Article  PubMed  CAS  Google Scholar 

  119. Cubelos B, Gimenez C, Zafra F (2005) Localization of the GLYT1 glycine transporter at glutamatergic synapses in the rat brain. Cereb Cortex 15:448–459

    Article  PubMed  Google Scholar 

  120. Cubelos B, Gonzalez-Gonzalez IM, Gimenez C, Zafra F (2005) The scaffolding protein PSD-95 interacts with the glycine transporter GLYT1 and impairs its internalization. J Neurochem 95:1047–1058

    Article  PubMed  CAS  Google Scholar 

  121. Raiteri L, Stigliani S, Patti L et al (2005) Activation of gamma-aminobutyric acid GAT-1 transporters on glutamatergic terminals of mouse spinal cord mediates glutamate release through anion channels and by transporter reversal. J Neurosci Res 80:424–433

    Article  PubMed  CAS  Google Scholar 

  122. Raiteri L, Stigliani S, Usai C et al (2008) Functional expression of release-regulating glycine transporters GLYT1 on GABAergic neurons and GLYT2 on astrocytes in mouse spinal cord. Neurochem Int 52:103–112

    Article  PubMed  CAS  Google Scholar 

  123. Cowin GJ, Willgoss DA, Bartley J, Endre ZH (1996) Serine isotopmer analysis by 13C-NMR defines glycine–serine interconversion in situ in the renal proximal tubule. Biochim Biophys Acta 1310:32–40

    Article  PubMed  Google Scholar 

  124. Anderson DD, Stover PJ (2009) SHMT1 and SHMT2 are functionally redundant in nuclear de novo thymidylate biosynthesis. PLoS ONE 4:e5839

    Article  PubMed  CAS  Google Scholar 

  125. Kikuchi G (1973) The glycine cleavage system: composition, reaction mechanism, and physiological significance. Mol Cell Biochem 1:169–187

    Article  PubMed  CAS  Google Scholar 

  126. Yoshida T, Kikuchi G (1973) Majors pathways of serine and glycine catabolism in various organs of the rat and cock. J Biochem 73:1013–1022

    PubMed  CAS  Google Scholar 

  127. Dringen R, Verleysdonk S, Hamprecht B, Willker W, Leibfritz D, Brand A (1998) Metabolism of glycine in primary astroglial cells: synthesis of creatine, serine, and glutathione. J Neurochem 70:835–840

    Article  PubMed  CAS  Google Scholar 

  128. Furuya S, Tabata T, Mitoma J et al (2000) L-serine and glycine serve as major astroglia-derived trophic factors for cerebellar Purkinje neurons. Proc Natl Acad Sci USA 97:11528–11533

    Article  PubMed  CAS  Google Scholar 

  129. Sato K, Yoshida S, Fujiwara K, Tada K, Tohyama M (1991) Glycine cleavage system in astrocytes. Brain Res 567:64–70

    Article  PubMed  CAS  Google Scholar 

  130. Yamashita N, Sakai K, Furuya S, Watanabe M (2003) Selective expression of L-serine synthetic enzyme 3PGDH in schwann cells, perineuronal glia, and endoneurial fibroblasts along rat sciatic nerves and its upregulation after crush injury. Arch Histol Cytol 66:429–436

    Article  PubMed  CAS  Google Scholar 

  131. Furuya S, Watanabe M (2003) Novel neuroglial and glioglial relationships mediated by L-serine metabolism. Arch Histol Cytol 66:109–121

    Article  PubMed  CAS  Google Scholar 

  132. Verleysdonk S, Martin H, Willker W, Leibfritz D, Hamprecht B (1999) Rapid uptake and degradation of glycine by astroglial cells in culture: synthesis and release of serine and lactate. Glia 27:239–248

    Article  PubMed  CAS  Google Scholar 

  133. Sakata Y, Owada Y, Sato K et al (2001) Structure and expression of the glycine cleavage system in rat central nervous system. Brain Res Mol Brain Res 94:119–130

    Article  PubMed  CAS  Google Scholar 

  134. Ichinohe A, Kure S, Mikawa S et al (2004) Glycine cleavage system in neurogenic regions. Eur J Neurosci 19:2365–2370

    Article  PubMed  Google Scholar 

  135. Barry D, McDermott K (2005) Differentiation of radial glia from radial precursor cells and transformation into astrocytes in the developing rat spinal cord. Glia 50:187–197

    Article  PubMed  Google Scholar 

  136. Kure S, Koyata H, Kume A, Ishiguro Y, Hiraga K (1991) The glycine cleavage system. The coupled expression of the glycine decarboxylase gene and the H-protein gene in the chicken. J Biol Chem 266:3330–3334

    PubMed  CAS  Google Scholar 

  137. Oliet SH, Mothet JP (2006) Molecular determinants of D-serine-mediated gliotransmission: from release to function. Glia 54:726–737

    Article  PubMed  Google Scholar 

  138. Palkovits M, Elekes I, Lang T, Patthy A (1986) Taurine levels in discrete brain nuclei of rats. J Neurochem 47:1333–1335

    Article  PubMed  CAS  Google Scholar 

  139. Oja SS, Saransaari P (2000) Modulation of taurine release by glutamate receptors and nitric oxide. Prog Neurobiol 62:407–425

    Article  PubMed  CAS  Google Scholar 

  140. Huxtable RJ (1989) Taurine in the central nervous system and the mammalian actions of taurine. Prog Neurobiol 32:471–533

    Article  PubMed  CAS  Google Scholar 

  141. Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101–163

    PubMed  CAS  Google Scholar 

  142. Hussy N, Deleuze C, Desarmenien MG, Moos FC (2000) Osmotic regulation of neuronal activity: a new role for taurine and glial cells in a hypothalamic neuroendocrine structure. Prog Neurobiol 62:113–134

    Article  PubMed  CAS  Google Scholar 

  143. Pow DV, Sullivan R, Reye P, Hermanussen S (2002) Localization of taurine transporters, taurine, and (3)H taurine accumulation in the rat retina, pituitary, and brain. Glia 37:153–168

    Article  PubMed  Google Scholar 

  144. Mangin JM, Guyon A, Eugene D, Paupardin-Tritsch D, Legendre P (2002) Functional glycine receptor maturation in the absence of glycinergic input in dopaminergic neurones of the rat substantia nigra. J Physiol 542:685–697

    Article  PubMed  CAS  Google Scholar 

  145. Mellor JR, Gunthorpe MJ, Randall AD (2000) The taurine uptake inhibitor guanidinoethyl sulphonate is an agonist at gamma-aminobutyric acid(A) receptors in cultured murine cerebellar granule cells. Neurosci Lett 286:25–28

    Article  PubMed  CAS  Google Scholar 

  146. Madsen S, Ottersen OP, Storm-Mathisen J (1987) Immunocytochemical demonstration of taurine. Adv Exp Med Biol 217:275–284

    PubMed  CAS  Google Scholar 

  147. Magnusson KR, Clements JR, Wu JY, Beitz AJ (1989) Colocalization of taurine- and cysteine sulfinic acid decarboxylase-like immunoreactivity in the hippocampus of the rat. Synapse 4:55–69

    Article  PubMed  CAS  Google Scholar 

  148. Storm-Mathisen J, Ottersen OP, Fu-Long T, Gundersen V, Laake JH, Nordbo G (1986) Metabolism and transport of amino acids studied by immunocytochemistry. Med Biol 64:127–132

    PubMed  CAS  Google Scholar 

  149. Madsen S, Ottersen OP, Storm-Mathisen J (1985) Immunocytochemical visualization of taurine: neuronal localization in the rat cerebellum. Neurosci Lett 60:255–260

    Article  PubMed  CAS  Google Scholar 

  150. Bulley S, Shen W (2010) Reciprocal regulation between taurine and glutamate response via Ca2+-dependent pathways in retinal third-order neurons. J Biomed Sci 17(Suppl 1):S5

    Article  PubMed  CAS  Google Scholar 

  151. Clements JR, Magnusson KR, Beitz AJ (1989) Ultrastructural description of taurine-like immunoreactive cells and processes in the rat hippocampus. Synapse 4:70–79

    Article  PubMed  CAS  Google Scholar 

  152. Yingcharoen K, Rinvik E, Storm-Mathisen J, Ottersen OP (1989) GABA, glycine, glutamate, aspartate and taurine in the perihypoglossal nuclei: an immunocytochemical investigation in the cat with particular reference to the issue of amino acid colocalization. Exp Brain Res 78:345–357

    Article  PubMed  CAS  Google Scholar 

  153. Decavel C, Hatton GI (1995) Taurine immunoreactivity in the rat supraoptic nucleus: prominent localization in glial cells. J Comp Neurol 354:13–26

    Article  PubMed  CAS  Google Scholar 

  154. Miyata S, Matsushima O, Hatton GI (1997) Taurine in rat posterior pituitary: localization in astrocytes and selective release by hypoosmotic stimulation. J Comp Neurol 381:513–523

    Article  PubMed  CAS  Google Scholar 

  155. Pow DV (1993) Immunocytochemistry of amino-acids in the rodent pituitary using extremely specific, very high titre antisera. J Neuroendocrinol 5:349–356

    Article  PubMed  CAS  Google Scholar 

  156. Hussy N, Bres V, Rochette M et al (2001) Osmoregulation of vasopressin secretion via activation of neurohypophysial nerve terminals glycine receptors by glial taurine. J Neurosci 21:7110–7116

    PubMed  CAS  Google Scholar 

  157. Hausser MA, Yung WH, Lacey MG (1992) Taurine and glycine activate the same Cl− conductance in substantia nigra dopamine neurones. Brain Res 571:103–108

    Article  PubMed  CAS  Google Scholar 

  158. Rampon C, Luppi PH, Fort P, Peyron C, Jouvet M (1996) Distribution of glycine-immunoreactive cell bodies and fibers in the rat brain. Neuroscience 75:737–755

    Article  PubMed  CAS  Google Scholar 

  159. Junyent F, De Lemos L, Utrera J et al (2011) Content and traffic of taurine in hippocampal reactive astrocytes. Hippocampus 21:185–197

    Article  PubMed  CAS  Google Scholar 

  160. Jourdain P, Bergersen LH, Bhaukaurally K et al (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 10:331–339

    Article  PubMed  CAS  Google Scholar 

  161. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317:1083–1086

    Article  PubMed  CAS  Google Scholar 

  162. Cousin MA, Nicholls DG (1997) Synaptic vesicle recycling in cultured cerebellar granule cells: role of vesicular acidification and refilling. J Neurochem 69:1927–1935

    Article  PubMed  CAS  Google Scholar 

  163. Pascual O, Casper KB, Kubera C et al (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113–116

    Article  PubMed  CAS  Google Scholar 

  164. Sagne C, El Mestikawy S, Isambert MF et al (1997) Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett 417:177–183

    Article  PubMed  CAS  Google Scholar 

  165. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870–876

    Article  PubMed  CAS  Google Scholar 

  166. Chaudhry FA, Reimer RJ, Bellocchio EE et al (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733–9750

    PubMed  CAS  Google Scholar 

  167. Dumoulin A, Rostaing P, Bedet C et al (1999) Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci 112(Pt 6):811–823

    PubMed  CAS  Google Scholar 

  168. Muller E, Le Corronc H, Triller A, Legendre P (2006) Developmental dissociation of presynaptic inhibitory neurotransmitter and postsynaptic receptor clustering in the hypoglossal nucleus. Mol Cell Neurosci 32:254–273

    Article  PubMed  CAS  Google Scholar 

  169. Echigo N, Moriyama Y (2004) Vesicular inhibitory amino acid transporter is expressed in gamma-aminobutyric acid (GABA)-containing astrocytes in rat pineal glands. Neurosci Lett 367:79–84

    Article  PubMed  CAS  Google Scholar 

  170. Oh WJ, Noggle SA, Maddox DM, Condie BG (2005) The mouse vesicular inhibitory amino acid transporter gene: expression during embryogenesis, analysis of its core promoter in neural stem cells and a reconsideration of its alternate splicing. Gene 351:39–49

    Article  PubMed  CAS  Google Scholar 

  171. Kozlov AS, Angulo MC, Audinat E, Charpak S (2006) Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci USA 103:10058–10063

    Article  PubMed  CAS  Google Scholar 

  172. Jones SM, Palmer MJ (2009) Activation of the tonic GABAC receptor current in retinal bipolar cell terminals by nonvesicular GABA release. J Neurophysiol 102:691–699

    Article  PubMed  CAS  Google Scholar 

  173. Barakat L, Bordey A (2002) GAT-1 and reversible GABA transport in Bergmann glia in slices. J Neurophysiol 88:1407–1419

    PubMed  CAS  Google Scholar 

  174. Richerson GB, Wu Y (2003) Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 90:1363–1374

    Article  PubMed  CAS  Google Scholar 

  175. Wu Y, Wang W, Diez-Sampedro A, Richerson GB (2007) Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56:851–865

    Article  PubMed  CAS  Google Scholar 

  176. Wu Y, Wang W, Richerson GB (2006) The transmembrane sodium gradient influences ambient GABA concentration by altering the equilibrium of GABA transporters. J Neurophysiol 96:2425–2436

    Article  PubMed  CAS  Google Scholar 

  177. Moran J, Morales-Mulia S, Hernandez-Cruz A, Pasantes-Morales H (1997) Regulatory volume decrease and associated osmolyte fluxes in cerebellar granule neurons are calcium independent. J Neurosci Res 47:144–154

    Article  PubMed  CAS  Google Scholar 

  178. Pasantes-Morales H, Moran J, Schousboe A (1990) Volume-sensitive release of taurine from cultured astrocytes: properties and mechanism. Glia 3:427–432

    Article  PubMed  CAS  Google Scholar 

  179. Sanchez-Olea R, Moran J, Schousboe A, Pasantes-Morales H (1991) Hyposmolarity-activated fluxes of taurine in astrocytes are mediated by diffusion. Neurosci Lett 130:233–236

    Article  PubMed  CAS  Google Scholar 

  180. Schousboe A, Pasantes-Morales H (1992) Role of taurine in neural cell volume regulation. Can J Physiol Pharmacol 70(Suppl):S356–S361

    Article  PubMed  CAS  Google Scholar 

  181. Schousboe A, Sanchez Olea R, Moran J, Pasantes-Morales H (1991) Hyposmolarity-induced taurine release in cerebellar granule cells is associated with diffusion and not with high-affinity transport. J Neurosci Res 30:661–665

    Article  PubMed  CAS  Google Scholar 

  182. Rodriguez-Navarro JA, Gonzalo-Gobernado R, Herranz AS, Gonzlez-Vigueras JM, Solis JM (2009) High potassium induces taurine release by osmosensitive and osmoresistant mechanisms in the rat hippocampus in vivo. J Neurosci Res 87:208–217

    Article  PubMed  CAS  Google Scholar 

  183. Supplisson S, Roux MJ (2002) Why glycine transporters have different stoichiometries. FEBS Lett 529:93–101

    Article  PubMed  CAS  Google Scholar 

  184. Otsuka M, Obata K, Miyata Y, Tanaka Y (1971) Measurement of gamma-aminobutyric acid in isolated nerve cells of cat central nervous system. J Neurochem 18:287–295

    Article  PubMed  CAS  Google Scholar 

  185. Schwartz EA (1987) Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science 238:350–355

    Article  PubMed  CAS  Google Scholar 

  186. Takayama C, Inoue Y (2005) Developmental expression of GABA transporter-1 and 3 during formation of the GABAergic synapses in the mouse cerebellar cortex. Brain Res Dev Brain Res 158:41–49

    Article  PubMed  CAS  Google Scholar 

  187. Morara S, Brecha NC, Marcotti W, Provini L, Rosina A (1996) Neuronal and glial localization of the GABA transporter GAT-1 in the cerebellar cortex. Neuroreport 7:2993–2996

    Article  PubMed  CAS  Google Scholar 

  188. Swan M, Najlerahim A, Watson RE, Bennett JP (1994) Distribution of mRNA for the GABA transporter GAT-1 in the rat brain: evidence that GABA uptake is not limited to presynaptic neurons. J Anat 185(Pt 2):315–323

    PubMed  CAS  Google Scholar 

  189. Biedermann B, Bringmann A, Reichenbach A (2002) High-affinity GABA uptake in retinal glial (Muller) cells of the guinea pig: electrophysiological characterization, immunohistochemical localization, and modeling of efficiency. Glia 39:217–228

    Article  PubMed  Google Scholar 

  190. Guo C, Stella SL Jr, Hirano AA, Brecha NC (2009) Plasmalemmal and vesicular gamma-aminobutyric acid transporter expression in the developing mouse retina. J Comp Neurol 512:6–26

    Article  PubMed  CAS  Google Scholar 

  191. Kinney GA (2005) GAT-3 transporters regulate inhibition in the neocortex. J Neurophysiol 94:4533–4537

    Article  PubMed  CAS  Google Scholar 

  192. Kirmse K, Kirischuk S (2006) Ambient GABA constrains the strength of GABAergic synapses at Cajal–Retzius cells in the developing visual cortex. J Neurosci 26:4216–4227

    Article  PubMed  CAS  Google Scholar 

  193. Iovine MK, Gumpert AM, Falk MM, Mendelson TC (2008) Cx23, a connexin with only four extracellular-loop cysteines, forms functional gap junction channels and hemichannels. FEBS Lett 582:165–170

    Article  PubMed  CAS  Google Scholar 

  194. Shestopalov VI, Panchin Y (2008) Pannexins and gap junction protein diversity. Cell Mol Life Sci 65:376–394

    Article  PubMed  CAS  Google Scholar 

  195. Suadicani SO, Brosnan CF, Scemes E (2006) P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 26:1378–1385

    Article  PubMed  CAS  Google Scholar 

  196. Chung MK, Guler AD, Caterina MJ (2008) TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 11:555–564

    Article  PubMed  CAS  Google Scholar 

  197. Stridh MH, Tranberg M, Weber SG, Blomstrand F, Sandberg M (2008) Stimulated efflux of amino acids and glutathione from cultured hippocampal slices by omission of extracellular calcium: likely involvement of connexin hemichannels. J Biol Chem 283:10347–10356

    Article  PubMed  CAS  Google Scholar 

  198. Ye ZC, Oberheim N, Kettenmann H, Ransom BR (2009) Pharmacological “cross-inhibition” of connexin hemichannels and swelling activated anion channels. Glia 57:258–269

    Article  PubMed  Google Scholar 

  199. Kimelberg HK, Macvicar BA, Sontheimer H (2006) Anion channels in astrocytes: biophysics, pharmacology, and function. Glia 54:747–757

    Article  PubMed  Google Scholar 

  200. Sabirov RZ, Dutta AK, Okada Y (2001) Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J Gen Physiol 118:251–266

    Article  PubMed  CAS  Google Scholar 

  201. Sabirov RZ, Okada Y (2005) ATP release via anion channels. Purinergic Signal 1:311–328

    Article  PubMed  CAS  Google Scholar 

  202. Alexander SPH, Mathie A, Peters JA (2009) Guide to receptors and channels (GRAC), 4th edition. Br J Pharmacol 158(Suppl 1):S1–S254

    CAS  Google Scholar 

  203. Nilius B, Eggermont J, Voets T, Buyse G, Manolopoulos V, Droogmans G (1997) Properties of volume-regulated anion channels in mammalian cells. Prog Biophys Mol Biol 68:69–119

    Article  PubMed  CAS  Google Scholar 

  204. Okada Y (1997) Volume expansion-sensing outward-rectifier Cl− channel: fresh start to the molecular identity and volume sensor. Am J Physiol 273:C755–C789

    PubMed  CAS  Google Scholar 

  205. Strange K, Emma F, Jackson PS (1996) Cellular and molecular physiology of volume-sensitive anion channels. Am J Physiol 270:C711–C730

    PubMed  CAS  Google Scholar 

  206. Duran C, Thompson CH, Xiao Q, Hartzell HC (2010) Chloride channels: often enigmatic, rarely predictable. Annu Rev Physiol 72:95–121

    Article  PubMed  CAS  Google Scholar 

  207. De Pinto V, Messina A, Lane DJ, Lawen A (2010) Voltage-dependent anion-selective channel (VDAC) in the plasma membrane. FEBS Lett 584:1793–1799

    Article  PubMed  CAS  Google Scholar 

  208. Sabirov RZ, Sheiko T, Liu H, Deng D, Okada Y, Craigen WJ (2006) Genetic demonstration that the plasma membrane maxianion channel and voltage-dependent anion channels are unrelated proteins. J Biol Chem 281:1897–1904

    Article  PubMed  CAS  Google Scholar 

  209. Parkerson KA, Sontheimer H (2004) Biophysical and pharmacological characterization of hypotonically activated chloride currents in cortical astrocytes. Glia 46:419–436

    Article  PubMed  Google Scholar 

  210. Sabirov RZ, Okada Y (2009) The maxi-anion channel: a classical channel playing novel roles through an unidentified molecular entity. J Physiol Sci 59:3–21

    Article  PubMed  CAS  Google Scholar 

  211. Liu HT, Toychiev AH, Takahashi N, Sabirov RZ, Okada Y (2008) Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res 18:558–565

    Article  PubMed  CAS  Google Scholar 

  212. Decher N, Lang HJ, Nilius B, Bruggemann A, Busch AE, Steinmeyer K (2001) DCPIB is a novel selective blocker of I(Cl, swell) and prevents swelling-induced shortening of guinea-pig atrial action potential duration. Br J Pharmacol 134:1467–1479

    Article  PubMed  CAS  Google Scholar 

  213. Varela D, Simon F, Olivero P et al (2007) Activation of H2O2-induced VSOR Cl− currents in HTC cells require phospholipase Cgamma1 phosphorylation and Ca2+ mobilisation. Cell Physiol Biochem 20:773–780

    Article  PubMed  CAS  Google Scholar 

  214. Haskew-Layton RE, Rudkouskaya A, Jin Y, Feustel PJ, Kimelberg HK, Mongin AA (2008) Two distinct modes of hypoosmotic medium-induced release of excitatory amino acids and taurine in the rat brain in vivo. PLoS ONE 3:e3543

    Article  PubMed  CAS  Google Scholar 

  215. Mongin AA, Kimelberg HK (2005) ATP regulates anion channel-mediated organic osmolyte release from cultured rat astrocytes via multiple Ca2+-sensitive mechanisms. Am J Physiol Cell Physiol 288:C204–C213

    PubMed  CAS  Google Scholar 

  216. Ternovsky VI, Okada Y, Sabirov RZ (2004) Sizing the pore of the volume-sensitive anion channel by differential polymer partitioning. FEBS Lett 576:433–436

    Article  PubMed  CAS  Google Scholar 

  217. Cho H, Shin J, Shin CY, Lee SY, Oh U (2002) Mechanosensitive ion channels in cultured sensory neurons of neonatal rats. J Neurosci 22:1238–1247

    PubMed  CAS  Google Scholar 

  218. Hamill OP, McBride DW Jr (1996) The pharmacology of mechanogated membrane ion channels. Pharmacol Rev 48:231–252

    PubMed  CAS  Google Scholar 

  219. Lee S, Yoon BE, Berglund K et al (2010) Channel-mediated tonic GABA release from glia. Science 330:790–796

    Article  PubMed  CAS  Google Scholar 

  220. Hartzell HC, Qu Z, Yu K, Xiao Q, Chien LT (2008) Molecular physiology of bestrophins: multifunctional membrane proteins linked to best disease and other retinopathies. Physiol Rev 88:639–672

    Article  PubMed  CAS  Google Scholar 

  221. Li G, Olson JE (2008) Purinergic activation of anion conductance and osmolyte efflux in cultured rat hippocampal neurons. Am J Physiol Cell Physiol 295:C1550–C1560

    Article  PubMed  CAS  Google Scholar 

  222. Martin DL, Madelian V, Seligmann B, Shain W (1990) The role of osmotic pressure and membrane potential in K(+)-stimulated taurine release from cultured astrocytes and LRM55 cells. J Neurosci 10:571–577

    PubMed  CAS  Google Scholar 

  223. Pasantes-Morales H, Schousboe A (1989) Release of taurine from astrocytes during potassium-evoked swelling. Glia 2:45–50

    Article  PubMed  CAS  Google Scholar 

  224. Tucker B, Olson JE (2010) Glutamate receptor-mediated taurine release from the hippocampus during oxidative stress. J Biomed Sci 17(Suppl 1):S10

    Article  PubMed  CAS  Google Scholar 

  225. Feustel PJ, Jin Y, Kimelberg HK (2004) Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra. Stroke 35:1164–1168

    Article  PubMed  CAS  Google Scholar 

  226. Jackson PS, Strange K (1993) Volume-sensitive anion channels mediate swelling-activated inositol and taurine efflux. Am J Physiol 265:C1489–C1500

    PubMed  CAS  Google Scholar 

  227. Patel AJ, Lauritzen I, Lazdunski M, Honore E (1998) Disruption of mitochondrial respiration inhibits volume-regulated anion channels and provokes neuronal cell swelling. J Neurosci 18:3117–3123

    PubMed  CAS  Google Scholar 

  228. Roy G (1995) Amino acid current through anion channels in cultured human glial cells. J Membr Biol 147:35–44

    PubMed  CAS  Google Scholar 

  229. Basavappa S, Ellory JC (1996) The role of swelling-induced anion channels during neuronal volume regulation. Mol Neurobiol 13:137–153

    Article  PubMed  CAS  Google Scholar 

  230. Estevez AY, O’Regan MH, Song D, Phillis JW (1999) Effects of anion channel blockers on hyposmotically induced amino acid release from the in vivo rat cerebral cortex. Neurochem Res 24:447–452

    Article  PubMed  CAS  Google Scholar 

  231. Strange K, Jackson PS (1995) Swelling-activated organic osmolyte efflux: a new role for anion channels. Kidney Int 48:994–1003

    Article  PubMed  CAS  Google Scholar 

  232. Reynolds A, Brustein E, Liao M et al (2008) Neurogenic role of the depolarizing chloride gradient revealed by global overexpression of KCC2 from the onset of development. J Neurosci 28:1588–1597

    Article  PubMed  CAS  Google Scholar 

  233. Wislet-Gendebien S, Hans G, Leprince P, Rigo JM, Moonen G, Rogister B (2005) Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 23:392–402

    Article  PubMed  CAS  Google Scholar 

  234. Ge S, Pradhan DA, G-l M, Song H (2007) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30:1–8

    Article  PubMed  CAS  Google Scholar 

  235. Manent JB, Represa A (2007) Neurotransmitters and brain maturation: early paracrine actions of GABA and glutamate modulate neuronal migration. Neuroscientist 13:268–279

    Article  PubMed  CAS  Google Scholar 

  236. Platel J-C, Stamboulian S, Nguyen I, Bordey A (2010) Neurotransmitter signaling in postnatal neurogenesis: the first leg. Brain Res Rev 63:60–71

    Article  PubMed  CAS  Google Scholar 

  237. Schwirtlich M, Emri Z, Antal K, Mate Z, Katarova Z, Szabo G (2009) GABAA and GABAB receptors of distinct properties affect oppositely the proliferation of mouse embryonic stem cells through synergistic elevation of intracellular Ca2+. FASEB J 24:1218–1228

    Article  PubMed  CAS  Google Scholar 

  238. Andäng M, Hjerling-Leffler J, Moliner A et al (2008) Histone H2AX-dependent GABAA receptor regulation of stem cell proliferation. Nature 451:460–464

    Article  PubMed  CAS  Google Scholar 

  239. Haydar TF, Wang F, Schwartz ML, Rakic P (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20:5764–5774

    PubMed  CAS  Google Scholar 

  240. Fiszman ML, Borodinsky LN, Neale JH (1999) GABA induces proliferation of immature cerebellar granule cells grown in vitro. Brain Res Dev Brain Res 115:1–8

    Article  PubMed  CAS  Google Scholar 

  241. Dave KA, Bordey A (2009) GABA increases Ca2+ in cerebellar granule cell precursors via depolarization: implications for proliferation. IUBMB Life 61:496–503

    Article  PubMed  CAS  Google Scholar 

  242. Cesetti T, Fila T, Obernier K et al (2010) GABAA receptor signaling induces osmotic swelling and cell cycle activation of neonatal prominin+ precursors. Stem Cells 29:307–319

    Article  CAS  Google Scholar 

  243. Heck N, Kilb W, Reiprich P et al (2007) GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb Cortex 17:138–148

    Article  PubMed  Google Scholar 

  244. Bordey A (2007) Enigmatic GABAergic networks in adult neurogenic zones. Brain Res Rev 53:124–134

    Article  PubMed  CAS  Google Scholar 

  245. Behar T, Li Y, Tran HT et al (1996) GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. J Neurosci 16:1808–1818

    PubMed  CAS  Google Scholar 

  246. Behar TN, Schaffner AE, Colton CA et al (1994) GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons. J Neurosci 14:29–38

    PubMed  CAS  Google Scholar 

  247. Behar TN, Schaffner AE, Scott CA, Greene CL, Barker JL (2000) GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb Cortex 10:899–909

    Article  PubMed  CAS  Google Scholar 

  248. Bolteus AJ (2004) GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 24:7623–7631

    Article  PubMed  CAS  Google Scholar 

  249. Liu X, Wang Q, Haydar TF, Bordey A (2005) Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci 8:1179–1187

    Article  PubMed  CAS  Google Scholar 

  250. Denter DG, Heck N, Riedemann T, White R, Kilb W, Luhmann HJ (2010) GABAC receptors are functionally expressed in the intermediate zone and regulate radial migration in the embryonic mouse neocortex. Neuroscience 167:124–134

    Article  PubMed  CAS  Google Scholar 

  251. Cancedda L, Fiumelli H, Chen K, Poo MM (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27:5224–5235

    Article  PubMed  CAS  Google Scholar 

  252. Bortone D, Polleux F (2009) KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 62:53–71

    Article  PubMed  CAS  Google Scholar 

  253. Lopez-Bendito G, Lujan R, Shigemoto R, Ganter P, Paulsen O, Molnar Z (2003) Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. Cereb Cortex 13:932–942

    Article  PubMed  Google Scholar 

  254. Cuzon VC, Yeh PW, Cheng Q, Yeh HH (2006) Ambient GABA promotes cortical entry of tangentially migrating cells derived from the medial ganglionic eminence. Cereb Cortex 16:1377–1388

    Article  PubMed  Google Scholar 

  255. Muth-Köhne E, Terhag J, Pahl S, Werner M, Joshi I, Hollmann M (2010) Functional excitatory GABAA receptors precede ionotropic glutamate receptors in radial glia-like neural stem cells. Mol Cell Neurosci 43:209–221

    Article  PubMed  CAS  Google Scholar 

  256. Sernagor E (2010) GABAergic control of neurite outgrowth and remodeling during development and adult neurogenesis: general rules and differences in diverse systems. Front Cell Neurosci 4:11

    Article  PubMed  CAS  Google Scholar 

  257. Borodinsky LN, O’Leary D, Neale JH, Vicini S, Coso OA, Fiszman ML (2003) GABA-induced neurite outgrowth of cerebellar granule cells is mediated by GABAAreceptor activation, calcium influx and CaMKII and erk1/2 pathways. J Neurochem 84:1411–1420

    Article  PubMed  CAS  Google Scholar 

  258. Barbin G, Pollard H, Gaїarsa JL, Ben-Ari Y (1993) Involvement of GABA A receptors in the outgrowth of cultured hippocampal neurons. Neurosci Lett 152:150–154

    Article  PubMed  CAS  Google Scholar 

  259. Mattson MP, Kater SB (1989) Excitatory and inhibitory neurotransmitters in the generation adn degeneration of hippocampal neuroarchitecture. Brain Res 478:337–348

    Article  PubMed  CAS  Google Scholar 

  260. Michler A (1990) Involvement of GABA receptors in the regulation of neurite growth in cultured embryonic chick tectum. Int J Dev Neurosci 8:463–472

    Article  PubMed  CAS  Google Scholar 

  261. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803–815

    Article  PubMed  CAS  Google Scholar 

  262. Ge S, Goh ELK, Sailor KA, Kitabatake Y, Ming G-L, Song H (2005) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589–593

    Article  PubMed  CAS  Google Scholar 

  263. Schwartzkroin PA (1998) GABA synapses enter the molecular big time. Nat Med 4:1115–1116

    Article  PubMed  CAS  Google Scholar 

  264. Lujan R, Shigemoto R, Lopezbendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567–580

    Article  PubMed  CAS  Google Scholar 

  265. Gascon E, Dayer AG, Sauvain MO et al (2006) GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J Neurosci 26:12956–12966

    Article  PubMed  CAS  Google Scholar 

  266. Bergles DE, Roberts JD, Somogyi P, Jahr CE (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187–191

    Article  PubMed  CAS  Google Scholar 

  267. Belachew S, Malgrange B, Rigo JM et al (2000) Glycine triggers an intracellular calcium influx in oligodendrocyte progenitor cells which is mediated by the activation of both the ionotropic glycine receptor and Na+-dependent transporters. Eur J Neurosci 12:1924–1930

    Article  PubMed  CAS  Google Scholar 

  268. Belachew S, Rogister B, Rigo JM et al (1998) Cultured oligodendrocyte progenitors derived from cerebral cortex express a glycine receptor which is pharmacologically distinct from the neuronal isoform. Eur J Neurosci 10:3556–3564

    Article  PubMed  CAS  Google Scholar 

  269. Luyt K, Slade TP, Dorward JJ et al (2007) Developing oligodendrocytes express functional GABAB receptors that stimulate cell proliferation and migration. J Neurochem 100:822–840

    Article  PubMed  CAS  Google Scholar 

  270. Pastor A, Chvatal A, Sykova E, Kettenmann H (1995) Glycine- and GABA-activated currents in identified glial cells of the developing rat spinal cord slice. Eur J Neurosci 7:1188–1198

    Article  PubMed  CAS  Google Scholar 

  271. Platel JC, Lacar B, Bordey A (2007) GABA and glutamate signaling: homeostatic control of adult forebrain neurogenesis. J Mol Histol 38:303–311

    Article  PubMed  CAS  Google Scholar 

  272. Aprison MH, Shank RP, Davidoff RA (1969) A comparison of the concentration of glycine, a transmitter suspect, in different areas of the brain and spinal cord in seven different vertebrates. Comp Biochem Physiol 28:1345–1355

    Article  PubMed  CAS  Google Scholar 

  273. Benitez-Diaz P, Miranda-Contreras L, Mendoza-Briceno RV, Pena-Contreras Z, Palacios-Pru E (2003) Prenatal and postnatal contents of amino acid neurotransmitters in mouse parietal cortex. Dev Neurosci 25:366–374

    Article  PubMed  CAS  Google Scholar 

  274. Palackal T, Moretz R, Wisniewski H, Sturman J (1986) Abnormal visual cortex development in the kitten associated with maternal dietary taurine deprivation. J Neurosci Res 15:223–239

    Article  PubMed  CAS  Google Scholar 

  275. Kawakami Y, Yoshida K, Yang JH et al (2009) Impaired neurogenesis in embryonic spinal cord of Phgdh knockout mice, a serine deficiency disorder model. Neurosci Res 63:184–193

    Article  PubMed  CAS  Google Scholar 

  276. Zhang LH, Gong N, Fei D, Xu L, Xu TL (2008) Glycine uptake regulates hippocampal network activity via glycine receptor-mediated tonic inhibition. Neuropsychopharmacology 33:701–711

    Article  PubMed  CAS  Google Scholar 

  277. Allain AE, Bairi A, Meyrand P, Branchereau P (2006) Expression of the glycinergic system during the course of embryonic development in the mouse spinal cord and its co-localization with GABA immunoreactivity. J Comp Neurol 496:832–846

    Article  PubMed  CAS  Google Scholar 

  278. McDearmid JR (2006) Glycine receptors regulate interneuron differentiation during spinal network development. Proc Natl Acad Sci USA 103:9679–9684

    Article  PubMed  CAS  Google Scholar 

  279. Hanson MG, Landmesser LT (2006) Increasing the frequency of spontaneous rhythmic activity disrupts pool-specific axon fasciculation and pathfinding of embryonic spinal motoneurons. J Neurosci 26:12769–12780

    Article  PubMed  CAS  Google Scholar 

  280. Tapia JC, Cardenas AM, Nualart F, Mentis GZ, Navarrete R, Aguayo LG (2000) Neurite outgrowth in developing mouse spinal cord neurons is modulated by glycine receptors. Neuroreport 11:3007–3010

    Article  PubMed  CAS  Google Scholar 

  281. Kirchhoff F, Mulhardt C, Pastor A, Becker CM, Kettenmann H (1996) Expression of glycine receptor subunits in glial cells of the rat spinal cord. J Neurochem 66:1383–1390

    Article  PubMed  CAS  Google Scholar 

  282. Nguyen L, Malgrange B, Belachew S et al (2002) Functional glycine receptors are expressed by postnatal nestin positive neural stem/progenitor cells. Eur J Neurosci 15:1299–1305

    Article  PubMed  Google Scholar 

  283. Maar T, Moran J, Schousboe A, Pasantes-Morales H (1995) Taurine deficiency in dissociated mouse cerebellar cultures affects neuronal migration. Int J Dev Neurosci 13:491–502

    Article  PubMed  CAS  Google Scholar 

  284. Okabe A, Kilb W, Shimizu-Okabe C, Hanganu IL, Fukuda A, Luhmann HJ (2004) Homogenous glycine receptor expression in cortical plate neurons and Cajal–Retzius cells of neonatal rat cerebral cortex. Neuroscience 123:715–724

    Article  PubMed  CAS  Google Scholar 

  285. Yoshida M, Fukuda S, Tozuka Y, Miyamoto Y, Hisatsune T (2004) Developmental shift in bidirectional functions of taurine-sensitive chloride channels during cortical circuit formation in postnatal mouse brain. J Neurobiol 60:166–175

    Article  PubMed  CAS  Google Scholar 

  286. Wang F, Xiao C, Ye JH (2005) Taurine activates excitatory non-synaptic glycine receptors on dopamine neurones in ventral tegmental area of young rats. J Physiol 565:503–516

    Article  PubMed  CAS  Google Scholar 

  287. Cubillos S, Lima L (2006) Taurine trophic modulation of goldfish retinal outgrowth and its interaction with the optic tectum. Amino Acids 31:325–331

    Article  PubMed  CAS  Google Scholar 

  288. Nusetti S, Obregon F, Lim L (2006) Neuritic outgrowth from goldfish retinal explants, interaction of taurine and zinc. Adv Exp Med Biol 583:435–440

    Article  PubMed  CAS  Google Scholar 

  289. Young TL, Cepko CL (2004) A role for ligand-gated ion channels in rod photoreceptor development. Neuron 41:867–879

    Article  PubMed  CAS  Google Scholar 

  290. Oja SS, Saransaari P (1996) Taurine as osmoregulator and neuromodulator in the brain. Metab Brain Dis 11:153–164

    Article  PubMed  CAS  Google Scholar 

  291. Pasantes-Morales H, Maar TE, Moran J (1993) Cell volume regulation in cultured cerebellar granule neurons. J Neurosci Res 34:219–224

    Article  PubMed  CAS  Google Scholar 

  292. Nilius B (2004) Is the volume-regulated anion channel VRAC a “water-permeable” channel? Neurochem Res 29:3–8

    Article  PubMed  CAS  Google Scholar 

  293. Park JB, Skalska S, Stern JE (2006) Characterization of a novel tonic gamma-aminobutyric acidA receptor-mediated inhibition in magnocellular neurosecretory neurons and its modulation by glia. Endocrinology 147:3746–3760

    Article  PubMed  CAS  Google Scholar 

  294. Jiang Z, Krnjevic K, Wang F, Ye JH (2004) Taurine activates strychnine-sensitive glycine receptors in neurons freshly isolated from nucleus accumbens of young rats. J Neurophysiol 91:248–257

    Article  PubMed  CAS  Google Scholar 

  295. Xu H, Wang W, Tang ZQ, Xu TL, Chen L (2006) Taurine acts as a glycine receptor agonist in slices of rat inferior colliculus. Hear Res 220:95–105

    Article  PubMed  CAS  Google Scholar 

  296. Ericson M, Molander A, Stomberg R, Soderpalm B (2006) Taurine elevates dopamine levels in the rat nucleus accumbens; antagonism by strychnine. Eur J Neurosci 23:3225–3229

    Article  PubMed  Google Scholar 

  297. Jia F, Yue M, Chandra D et al (2008) Taurine is a potent activator of extrasynaptic GABA(A) receptors in the thalamus. J Neurosci 28:106–115

    Article  PubMed  CAS  Google Scholar 

  298. Saransaari P, Oja SS (2010) Modulation of taurine release in ischemia by glutamate receptors in mouse brain stem slices. Amino Acids 38:739–746

    Article  PubMed  CAS  Google Scholar 

  299. Rao R, Tkac I, Townsend EL, Ennis K, Gruetter R, Georgieff MK (2007) Perinatal iron deficiency predisposes the developing rat hippocampus to greater injury from mild to moderate hypoxia-ischemia. J Cereb Blood Flow Metab 27:729–740

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut National de la Santé et de la Recherche Médicale (INSERM), U952, Centre National de la Recherche Scientifique (CNRS), UMR 7224, Université Pierre et Marie Curie, 9 quai Saint Bernard, Paris, Ile de France, France

    Herve Le-Corronc

  2. Université d Angers, 40 rue de Rennes, Angers, France

    Herve Le-Corronc

  3. BIOMED—Cell Physiology, Hasselt University, Agoralaan (Gebouw C), 3590, Diepenbeek, Belgium

    Jean-Michel Rigo

  4. Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA), Université Bordeaux et Centre National de la Recherche Scientifique (CNRS), UMR 5287, Av. des Facultés, 4ème étage Est, 33405, Talence, France

    Pascal Branchereau

  5. Institut National de la Santé et de la Recherche Médicale (INSERM), U952, Centre National de la Recherche Scientifique (CNRS), UMR 7224, Université Pierre et Marie Curie, Bâtiment B, étage 2, boite postale 37, 7 quai Saint Bernard, 75005, Paris, France

    Pascal Legendre

Authors
  1. Herve Le-Corronc
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Michel Rigo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pascal Branchereau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pascal Legendre
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pascal Branchereau or Pascal Legendre.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le-Corronc, H., Rigo, JM., Branchereau, P. et al. GABAA Receptor and Glycine Receptor Activation by Paracrine/Autocrine Release of Endogenous Agonists: More Than a Simple Communication Pathway. Mol Neurobiol 44, 28–52 (2011). https://doi.org/10.1007/s12035-011-8185-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-011-8185-1

Keywords

Search

Navigation