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Cited by 22Neuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanismsPain Mechanisms and Treatments

Developmental Formation of the GABAergic and Glycinergic Networks in the Mouse Spinal Cord

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Shimizu-Okabe, Chigusa, Kobayashi, Shiori, Kim, Jeongtae, Kosaka, Yoshinori, Sunagawa, Masanobu, Okabe, Akihito, Takayama, Chitoshi·2022·International Journal of Molecular Sciences
DOI 10.3390/ijms23020834PMC PMC8776010

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Abstract

Gamma-aminobutyric acid (GABA) and glycine act as inhibitory neurotransmitters. Three types of inhibitory neurons and terminals, GABAergic, GABA/glycine coreleasing, and glycinergic, are orchestrated in the spinal cord neural circuits and play critical roles in regulating pain, locomotive movement, and respiratory rhythms. In this study, we first describe GABAergic and glycinergic transmission and inhibitory networks, consisting of three types of terminals in the mature mouse spinal cord. Second, we describe the developmental formation of GABAergic and glycinergic networks, with a specific focus on the differentiation of neurons, formation of synapses, maturation of removal systems, and changes in their action. GABAergic and glycinergic neurons are derived from the same domains of the ventricular zone. Initially, GABAergic neurons are differentiated, and their axons form synapses. Some of these neurons remain GABAergic in lamina I and II. Many GABAergic neurons convert to a coreleasing state. The coreleasing neurons and terminals remain in the dorsal horn, whereas many ultimately become glycinergic in the ventral horn. During the development of terminals and the transformation from radial glia to astrocytes, GABA and glycine receptor subunit compositions markedly change, removal systems mature, and GABAergic and glycinergic action shifts from excitatory to inhibitory.

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  • GABAergic neurons, glutamatergic neurons, and mixed GABAergic/glutamatergic neurons form an interconnected inhibitory neural network.

    “Study showed that GABAergic neurons, glutamatergic neurons, and mixed GABAergic/glutamatergic neurons form an interconnected inhibitory neural network.”

    From Nociplastic pain: the prominent role of non-neuronal cells in central and peripheral sensitization (2026) · cites this paper as [181]

    The Introduction (section 1; page not provided) identifies the three types of inhibitory neurons and terminals as GABAergic, GABA/glycine-coreleasing, and glycinergic—not glutamatergic or mixed GABAergic/glutamatergic. Section 2.1 discusses glutamate as a precursor from which GABA is synthesized, not as a neurotransmitter coreleased in the inhibitory network. (LLM, conf=0.90)

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  • GABA-ARs, GlyRs, and the synaptic scaffold protein gephyrin jointly constitute inhibitory synapses that suppress neural excitability.

    “Together with GABA-ARs, GlyRs and the synaptic scaffold protein gephyrin jointly constitute inhibitory synapses that suppress neural excitability (181).”

    From Nociplastic pain: the prominent role of non-neuronal cells in central and peripheral sensitization (2026) · cites this paper as [181]

  • Gly and its receptor GlyR inhibit synaptic excitability.

    “In line with the roles of GABA and GABARs, neurotransmitter Gly and its receptor GlyR is the other couple of typical signaling pathway that can inhibit synaptic excitability.”

    From Nociplastic pain: the prominent role of non-neuronal cells in central and peripheral sensitization (2026) · cites this paper as [181]

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  1. [1]Macdonald R.L. Olsen R.W. GABAA receptor channels Annu. Rev. Neurosci. 1994 17 569 602 10.1146/annurev.ne.17.030194.003033 7516126 · DOI · Paper page
  2. [2]Olsen R.W. Tobin A.J. Molecular biology of GABAA receptors FASEB J. 1990 4 1469 1480 10.1096/fasebj.4.5.2155149 2155149 · DOI
  3. [3]Kirsch J. Glycinergic transmission Cell Tissue Res. 2006 326 535 540 10.1007/s00441-006-0261-x 16807723 · DOI
  4. [4]Legendre P. The glycinergic inhibitory synapse Cell. Mol. Life Sci. 2001 58 760 793 10.1007/PL00000899 11437237 PMC11337367 · DOI
  5. [5]Tritsch N.X. Granger A.J. Sabatini B.L. Mechanisms and functions of GABA co-release Nat. Rev. Neurosci. 2016 17 139 145 10.1038/nrn.2015.21 26865019 PMC6980171 · DOI
  6. [6]Vaaga C.E. Borisovska M. Westbrook G.L. Dual-transmitter neurons: Functional implications of co-release and co-transmission Curr. Opin. Neurobiol. 2014 29 25 32 10.1016/j.conb.2014.04.010 24816154 PMC4231002 · DOI
  7. [7]Jonas P. Bischofberger J. Sandkuhler J. Corelease of two fast neurotransmitters at a central synapse Science 1998 281 419 424 10.1126/science.281.5375.419 9665886 · DOI · Paper page
  8. [8]Hossaini M. French P.J. Holstege J.C. Distribution of glycinergic neuronal somata in the rat spinal cord Brain Res. 2007 1142 61 69 10.1016/j.brainres.2007.01.078 17336274 · DOI
  9. [9]Todd A.J. Sullivan A.C. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat J. Comp. Neurol. 1990 296 496 505 10.1002/cne.902960312 2358549 · DOI
  10. [10]Zeilhofer H.U. Studler B. Arabadzisz D. Schweizer C. Ahmadi S. Layh B. Bosl M.R. Fritschy J.M. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice J. Comp. Neurol. 2005 482 123 141 10.1002/cne.20349 15611994 · DOI
  11. [11]Barker J.L. Behar T. Li Y.X. Liu Q.Y. Ma W. Maric D. Maric I. Schaffner A.E. Serafini R. Smith S.V. GABAergic cells and signals in CNS development Perspect. Dev. Neurobiol. 1998 5 305 322 9777645
  12. [12]Zafra F. Aragon C. Gimenez C. Molecular biology of glycinergic neurotransmission Mol. Neurobiol. 1997 14 117 142 10.1007/BF02740653 9294860 · DOI
  13. [13]Martin D.L. Rimvall K. Regulation of gamma-aminobutyric acid synthesis in the brain J. Neurochem. 1993 60 395 407 10.1111/j.1471-4159.1993.tb03165.x 8419527 · DOI
  14. [14]Varju P. Katarova Z. Madarasz E. Szabo G. GABA signalling during development: New data and old questions Cell Tissue Res. 2001 305 239 246 10.1007/s004410100356 11545261 · DOI
  15. [15]Bak L.K. Schousboe A. Waagepetersen H.S. The glutamate/GABA-glutamine cycle: Aspects of transport, neurotransmitter homeostasis and ammonia transfer J. Neurochem. 2006 98 641 653 10.1111/j.1471-4159.2006.03913.x 16787421 · DOI · Paper page
  16. [16]Bedet C. Isambert M.F. Henry J.P. Gasnier B. Constitutive phosphorylation of the vesicular inhibitory amino acid transporter in rat central nervous system J. Neurochem. 2000 75 1654 1663 10.1046/j.1471-4159.2000.0751654.x 10987847 · DOI
  17. [17]Sagne C. El Mestikawy S. Isambert M.F. Hamon M. Henry J.P. Giros B. Gasnier B. Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases FEBS Lett. 1997 417 177 183 10.1016/S0014-5793(97)01279-9 9395291 · DOI
  18. [18]Mehta A.K. Ticku M.K. An update on GABAA receptors Brain Res. Brain Res. Rev. 1999 29 196 217 10.1016/S0165-0173(98)00052-6 10209232 · DOI
  19. [19]Sieghart W. Structure and pharmacology of gamma-aminobutyric acidA receptor subtypes Pharmacol. Rev. 1995 47 181 234 7568326
  20. [20]Laurie D.J. Seeburg P.H. Wisden W. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum J. Neurosci. 1992 12 1063 1076 10.1523/JNEUROSCI.12-03-01063.1992 1312132 PMC6576040 · DOI
  21. [21]Wisden W. Gundlach A.L. Barnard E.A. Seeburg P.H. Hunt S.P. Distribution of GABAA receptor subunit mRNAs in rat lumbar spinal cord Brain Res. Mol. Brain Res. 1991 10 179 183 10.1016/0169-328X(91)90109-B 1649370 · DOI
  22. [22]Wisden W. Laurie D.J. Monyer H. Seeburg P.H. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon J. Neurosci. 1992 12 1040 1062 10.1523/JNEUROSCI.12-03-01040.1992 1312131 PMC6576059 · DOI
  23. [23]Pritchett D.B. Sontheimer H. Shivers B.D. Ymer S. Kettenmann H. Schofield P.R. Seeburg P.H. Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology Nature 1989 338 582 585 10.1038/338582a0 2538761 · DOI
  24. [24]Vicini S. New perspectives in the functional role of GABA(A) channel heterogeneity Mol. Neurobiol. 1999 19 97 110 10.1007/BF02743656 10371465 · DOI
  25. [25]Bormann J. Feigenspan A. GABAC receptors Trends Neurosci. 1995 18 515 519 10.1016/0166-2236(95)98370-E 8638289 · DOI
  26. [26]Bormann J. The ‘ABC’ of GABA receptors Trends Pharmacol. Sci. 2000 21 16 19 10.1016/S0165-6147(99)01413-3 10637650 · DOI
  27. [27]Bormann J. Electrophysiology of GABAA and GABAB receptor subtypes Trends Neurosci. 1988 11 112 116 10.1016/0166-2236(88)90156-7 2465608 · DOI
  28. [28]Connors B.W. Malenka R.C. Silva L.R. Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat J. Physiol. 1988 406 443 468 10.1113/jphysiol.1988.sp017390 2855437 PMC1191109 · DOI · Paper page
  29. [29]LeVine H. 3rd Structural features of heterotrimeric G-protein-coupled receptors and their modulatory proteins Mol. Neurobiol. 1999 19 111 149 10.1007/BF02743657 10371466 · DOI
  30. [30]Nicoll R.A. The coupling of neurotransmitter receptors to ion channels in the brain Science 1988 241 545 551 10.1126/science.2456612 2456612 · DOI
  31. [31]Jembrek M.J. Vlainic J. GABA Receptors: Pharmacological Potential and Pitfalls Curr. Pharm. Des. 2015 21 4943 4959 10.2174/1381612821666150914121624 26365137 · DOI
  32. [32]Evenseth L.S.M. Gabrielsen M. Sylte I. The GABAB Receptor-Structure, Ligand Binding and Drug Development Molecules 2020 25 3093 10.3390/molecules25133093 PMC7411975 32646032 · DOI
  33. [33]Cherubini E. Conti F. Generating diversity at GABAergic synapses Trends Neurosci. 2001 24 155 162 10.1016/S0166-2236(00)01724-0 11182455 · DOI
  34. [34]Kanner B.I. Sodium-coupled neurotransmitter transport: Structure, function and regulation J. Exp. Biol. 1994 196 237 249 10.1242/jeb.196.1.237 7823025 · DOI
  35. [35]Gadea A. Lopez-Colome A.M. Glial transporters for glutamate, glycine, and GABA: II. GABA transporters J. Neurosci. Res. 2001 63 461 468 10.1002/jnr.1040 11241581 · DOI
  36. [36]Conti F. Zuccarello L.V. Barbaresi P. Minelli A. Brecha N.C. Melone M. Neuronal, glial, and epithelial localization of gamma-aminobutyric acid transporter 2, a high-affinity gamma-aminobutyric acid plasma membrane transporter, in the cerebral cortex and neighboring structures J. Comp. Neurol. 1999 409 482 494 10.1002/(SICI)1096-9861(19990705)409:3<482::AID-CNE11>3.0.CO;2-O 10379832 · DOI
  37. [37]Minelli A. Brecha N.C. Karschin C. DeBiasi S. Conti F. GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex J. Neurosci. 1995 15 7734 7746 10.1523/JNEUROSCI.15-11-07734.1995 7472524 PMC6578038 · DOI
  38. [38]Minelli A. DeBiasi S. Brecha N.C. Zuccarello L.V. Conti F. GAT-3, a high-affinity GABA plasma membrane transporter, is localized to astrocytic processes, and it is not confined to the vicinity of GABAergic synapses in the cerebral cortex J. Neurosci. 1996 16 6255 6264 10.1523/JNEUROSCI.16-19-06255.1996 8815906 PMC6579190 · DOI
  39. [39]Itouji A. Sakai N. Tanaka C. Saito N. Neuronal and glial localization of two GABA transporters (GAT1 and GAT3) in the rat cerebellum Brain Res. Mol. Brain Res. 1996 37 309 316 10.1016/0169-328X(95)00342-P 8738166 · DOI
  40. [40]Takayama C. Inoue Y. Developmental expression of GABA transporter-1 and 3 during formation of the GABAergic synapses in the mouse cerebellar cortex Brain Res. Dev. Brain Res. 2005 158 41 49 10.1016/j.devbrainres.2005.05.007 16024093 · DOI
  41. [41]Kolker S. Metabolism of amino acid neurotransmitters: The synaptic disorder underlying inherited metabolic diseases J. Inherit. Metab. Dis. 2018 41 1055 1063 10.1007/s10545-018-0201-4 29869166 · DOI
  42. [42]Verleysdonk S. Martin H. Willker W. Leibfritz D. Hamprecht B. Rapid uptake and degradation of glycine by astroglial cells in culture: Synthesis and release of serine and lactate Glia 1999 27 239 248 10.1002/(SICI)1098-1136(199909)27:3<239::AID-GLIA5>3.0.CO;2-K 10457370 · DOI
  43. [43]Beyoglu D. Idle J.R. The glycine deportation system and its pharmacological consequences Pharmacol. Ther. 2012 135 151 167 10.1016/j.pharmthera.2012.05.003 22584143 PMC3665358 · DOI
  44. [44]Zeilhofer H.U. Wildner H. Yevenes G.E. Fast synaptic inhibition in spinal sensory processing and pain control Physiol. Rev. 2012 92 193 235 10.1152/physrev.00043.2010 22298656 PMC3590010 · DOI
  45. [45]Xu T.L. Gong N. Glycine and glycine receptor signaling in hippocampal neurons: Diversity, function and regulation Prog. Neurobiol. 2010 91 349 361 10.1016/j.pneurobio.2010.04.008 20438799 · DOI
  46. [46]Gomeza J. Ohno K. Hulsmann S. Armsen W. Eulenburg V. Richter D.W. Laube B. Betz H. Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality Neuron 2003 40 797 806 10.1016/S0896-6273(03)00673-1 14622583 · DOI
  47. [47]Latal A.T. Kremer T. Gomeza J. Eulenburg V. Hulsmann S. Development of synaptic inhibition in glycine transporter 2 deficient mice Mol. Cell. Neurosci. 2010 44 342 352 10.1016/j.mcn.2010.04.005 20447457 · DOI
  48. [48]Chalphin A.V. Saha M.S. The specification of glycinergic neurons and the role of glycinergic transmission in development Front. Mol. Neurosci. 2010 3 11 10.3389/fnmol.2010.00011 20461146 PMC2866564 · DOI
  49. [49]Laube B. Maksay G. Schemm R. Betz H. Modulation of glycine receptor function: A novel approach for therapeutic intervention at inhibitory synapses? Trends Pharmacol. Sci. 2002 23 519 527 10.1016/S0165-6147(02)02138-7 12413807 · DOI
  50. [50]Lynch J.W. Molecular structure and function of the glycine receptor chloride channel Physiol. Rev. 2004 84 1051 1095 10.1152/physrev.00042.2003 15383648 · DOI
  51. [51]Lynch J.W. Native glycine receptor subtypes and their physiological roles Neuropharmacology 2009 56 303 309 10.1016/j.neuropharm.2008.07.034 18721822 · DOI
  52. [52]Eulenburg V. Armsen W. Betz H. Gomeza J. Glycine transporters: Essential regulators of neurotransmission Trends Biochem. Sci. 2005 30 325 333 10.1016/j.tibs.2005.04.004 15950877 · DOI
  53. [53]Sunagawa M. Shimizu-Okabe C. Kim J. Kobayashi S. Kosaka Y. Yanagawa Y. Matsushita M. Okabe A. Takayama C. Distinct development of the glycinergic terminals in the ventral and dorsal horns of the mouse cervical spinal cord Neuroscience 2017 343 459 471 10.1016/j.neuroscience.2016.12.032 28039040 · DOI
  54. [54]Zafra F. Aragon C. Olivares L. Danbolt N.C. Gimenez C. Storm-Mathisen J. Glycine transporters are differentially expressed among CNS cells J. Neurosci. 1995 15 3952 3969 10.1523/JNEUROSCI.15-05-03952.1995 7751957 PMC6578198 · DOI
  55. [55]Sato K. Yoshida S. Fujiwara K. Tada K. Tohyama M. Glycine cleavage system in astrocytes Brain Res. 1991 567 64 70 10.1016/0006-8993(91)91436-5 1815830 · DOI
  56. [56]Kikuchi G. Motokawa Y. Yoshida T. Hiraga K. Glycine cleavage system: Reaction mechanism, physiological significance, and hyperglycinemia Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2008 84 246 263 10.2183/pjab.84.246 PMC3666648 18941301 · DOI
  57. [57]Kosaka Y. Kin H. Tatetsu M. Uema I. Takayama C. Distinct development of GABA system in the ventral and dorsal horns in the embryonic mouse spinal cord Brain Res. 2012 1486 39 52 10.1016/j.brainres.2012.10.003 23044470 · DOI
  58. [59]Ottersen O.P. Storm-Mathisen J. Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique J. Comp. Neurol. 1984 229 374 392 10.1002/cne.902290308 6150049 · DOI
  59. [60]Tamamaki N. Yanagawa Y. Tomioka R. Miyazaki J. Obata K. Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse J. Comp. Neurol. 2003 467 60 79 10.1002/cne.10905 14574680 · DOI
  60. [61]Campistron G. Buijs R.M. Geffard M. Glycine neurons in the brain and spinal cord. Antibody production and immunocytochemical localization Brain Res. 1986 376 400 405 10.1016/0006-8993(86)90208-8 3524747 · DOI
  61. [62]Allain A.E. Bairi A. Meyrand P. Branchereau P. 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. 2006 496 832 846 10.1002/cne.20967 16628621 · DOI
  62. [63]Wojcik S.M. Katsurabayashi S. Guillemin I. Friauf E. Rosenmund C. Brose N. Rhee J.S. A shared vesicular carrier allows synaptic corelease of GABA and glycine Neuron 2006 50 575 587 10.1016/j.neuron.2006.04.016 16701208 · DOI · Paper page
  63. [64]Ishibashi H. Yamaguchi J. Nakahata Y. Nabekura J. Dynamic regulation of glycine-GABA co-transmission at spinal inhibitory synapses by neuronal glutamate transporter J. Physiol. 2013 591 3821 3832 10.1113/jphysiol.2012.250647 23690564 PMC3764631 · DOI
  64. [65]Ornung G. Shupliakov O. Linda H. Ottersen O.P. Storm-Mathisen J. Ulfhake B. Cullheim S. Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: A postembedding electron microscopic study J. Comp. Neurol. 1996 365 413 426 10.1002/(SICI)1096-9861(19960212)365:3<413::AID-CNE6>3.0.CO;2-7 8822179 · DOI
  65. [66]Dougherty K.J. Sawchuk M.A. Hochman S. Phenotypic diversity and expression of GABAergic inhibitory interneurons during postnatal development in lumbar spinal cord of glutamic acid decarboxylase 67-green fluorescent protein mice Neuroscience 2009 163 909 919 10.1016/j.neuroscience.2009.06.055 19560523 PMC2746868 · DOI
  66. [67]Bardoni R. Takazawa T. Tong C.K. Choudhury P. Scherrer G. Macdermott A.B. Pre- and postsynaptic inhibitory control in the spinal cord dorsal horn Ann. N. Y. Acad. Sci. 2013 1279 90 96 10.1111/nyas.12056 23531006 PMC7359868 · DOI
  67. [68]Basbaum A.I. Bautista D.M. Scherrer G. Julius D. Cellular and molecular mechanisms of pain Cell 2009 139 267 284 10.1016/j.cell.2009.09.028 19837031 PMC2852643 · DOI · Paper page
  68. [69]Cioffi C.L. Modulation of Glycine-Mediated Spinal Neurotransmission for the Treatment of Chronic Pain J. Med. Chem. 2018 61 2652 2679 10.1021/acs.jmedchem.7b00956 28876062 · DOI
  69. [71]Paul J. Zeilhofer H.U. Fritschy J.M. Selective distribution of GABA(A) receptor subtypes in mouse spinal dorsal horn neurons and primary afferents J. Comp. Neurol. 2012 520 3895 3911 10.1002/cne.23129 22522945 · DOI
  70. [72]Malosio M.L. Marqueze-Pouey B. Kuhse J. Betz H. Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain EMBO J. 1991 10 2401 2409 10.1002/j.1460-2075.1991.tb07779.x 1651228 PMC452935 · DOI
  71. [73]Todd A.J. Watt C. Spike R.C. Sieghart W. Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord J. Neurosci. 1996 16 974 982 10.1523/JNEUROSCI.16-03-00974.1996 8558266 PMC6578783 · DOI
  72. [74]Dorfman V.B. Vega M.C. Coirini H. Age-related changes of the GABA-B receptor in the lumbar spinal cord of male rats and penile erection Life Sci. 2006 78 1529 1534 10.1016/j.lfs.2005.06.045 16472824 · DOI
  73. [75]Sands S.A. Purisai M.G. Chronwall B.M. Enna S.J. Ontogeny of GABA(B) receptor subunit expression and function in the rat spinal cord Brain Res. 2003 972 197 206 10.1016/S0006-8993(03)02534-4 12711093 · DOI
  74. [76]Rozzo A. Armellin M. Franzot J. Chiaruttini C. Nistri A. Tongiorgi E. Expression and dendritic mRNA localization of GABAC receptor rho1 and rho2 subunits in developing rat brain and spinal cord Eur. J. Neurosci. 2002 15 1747 1758 10.1046/j.1460-9568.2002.02013.x 12081654 · DOI
  75. [77]Kim J. Kosaka Y. Shimizu-Okabe C. Niizaki A. Takayama C. Characteristic development of the GABA-removal system in the mouse spinal cord Neuroscience 2014 262 129 142 10.1016/j.neuroscience.2013.12.066 24412234 · DOI
  76. [78]Jursky F. Nelson N. Localization of glycine neurotransmitter transporter (GLYT2) reveals correlation with the distribution of glycine receptor J. Neurochem. 1995 64 1026 1033 10.1046/j.1471-4159.1995.64031026.x 7861131 · DOI
  77. [79]Owens D.F. Kriegstein A.R. Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 2002 3 715 727 10.1038/nrn919 12209120 · DOI
  78. [80]Ben-Ari Y. Excitatory actions of gaba during development: The nature of the nurture Nat. Rev. Neurosci. 2002 3 728 739 10.1038/nrn920 12209121 · DOI · Paper page
  79. [81]Payne J.A. Rivera C. Voipio J. Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma Trends Neurosci. 2003 26 199 206 10.1016/S0166-2236(03)00068-7 12689771 · DOI
  80. [82]Baccei M.L. Fitzgerald M. Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn J. Neurosci. 2004 24 4749 4757 10.1523/JNEUROSCI.5211-03.2004 15152035 PMC6729459 · DOI
  81. [83]Sagner A. Briscoe J. Establishing neuronal diversity in the spinal cord: A time and a place Development 2019 146 dev182154 10.1242/dev.182154 31767567 · DOI
  82. [84]Hernandez-Miranda L.R. Muller T. Birchmeier C. The dorsal spinal cord and hindbrain: From developmental mechanisms to functional circuits Dev. Biol. 2017 432 34 42 10.1016/j.ydbio.2016.10.008 27742210 · DOI
  83. [85]Briscoe J. Ericson J. Specification of neuronal fates in the ventral neural tube Curr. Opin. Neurobiol. 2001 11 43 49 10.1016/S0959-4388(00)00172-0 11179871 · DOI
  84. [86]Jessell T.M. Neuronal specification in the spinal cord: Inductive signals and transcriptional codes Nat. Rev. Genet. 2000 1 20 29 10.1038/35049541 11262869 · DOI · Paper page
  85. [87]Lee K.J. Jessell T.M. The specification of dorsal cell fates in the vertebrate central nervous system Annu. Rev. Neurosci. 1999 22 261 294 10.1146/annurev.neuro.22.1.261 10202540 · DOI
  86. [88]Helms A.W. Johnson J.E. Specification of dorsal spinal cord interneurons Curr. Opin. Neurobiol. 2003 13 42 49 10.1016/S0959-4388(03)00010-2 12593981 · DOI
  87. [89]Hori K. Hoshino M. GABAergic neuron specification in the spinal cord, the cerebellum, and the cochlear nucleus Neural Plast. 2012 2012 921732 10.1155/2012/921732 22830054 PMC3395262 · DOI
  88. [90]Goulding M. Lamar E. Neuronal patterning: Making stripes in the spinal cord Curr. Biol. 2000 10 R565 R568 10.1016/S0960-9822(00)00615-1 10959831 · DOI
  89. [91]Tran T.S. Alijani A. Phelps P.E. Unique developmental patterns of GABAergic neurons in rat spinal cord J. Comp. Neurol. 2003 456 112 126 10.1002/cne.10511 12509869 · DOI
  90. [92]Allain A.E. Bairi A. Meyrand P. Branchereau P. Ontogenic changes of the GABAergic system in the embryonic mouse spinal cord Brain Res. 2004 1000 134 147 10.1016/j.brainres.2003.11.071 15053961 · DOI
  91. [93]Huang J. Chen J. Wang W. Wei Y.Y. Cai G.H. Tamamaki N. Li Y.Q. Wu S.X. Birthdate study of GABAergic neurons in the lumbar spinal cord of the glutamic acid decarboxylase 67-green fluorescent protein knock-in mouse Front. Neuroanat. 2013 7 42 10.3389/fnana.2013.00042 24367298 PMC3856430 · DOI
  92. [95]Borromeo M.D. Meredith D.M. Castro D.S. Chang J.C. Tung K.C. Guillemot F. Johnson J.E. A transcription factor network specifying inhibitory versus excitatory neurons in the dorsal spinal cord Development 2014 141 2803 2812 10.1242/dev.105866 24924197 PMC4197617 · DOI
  93. [96]Restrepo C.E. Lundfald L. Szabo G. Erdelyi F. Zeilhofer H.U. Glover J.C. Kiehn O. Transmitter-phenotypes of commissural interneurons in the lumbar spinal cord of newborn mice J. Comp. Neurol. 2009 517 177 192 10.1002/cne.22144 19731323 · DOI
  94. [97]Lee S.K. Pfaff S.L. Transcriptional networks regulating neuronal identity in the developing spinal cord Nat. Neurosci. 2001 4 1183 1191 10.1038/nn750 11687828 · DOI
  95. [98]Stachowski N.J. Dougherty K.J. Spinal Inhibitory Interneurons: Gatekeepers of Sensorimotor Pathways Int. J. Mol. Sci. 2021 22 2667 10.3390/ijms22052667 33800863 PMC7961554 · DOI
  96. [99]Tran T.S. Cohen-Cory S. Phelps P.E. Embryonic GABAergic spinal commissural neurons project rostrally to mesencephalic targets J. Comp. Neurol. 2004 475 327 339 10.1002/cne.20166 15221949 · DOI
  97. [100]Moran-Rivard L. Kagawa T. Saueressig H. Gross M.K. Burrill J. Goulding M. Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord Neuron 2001 29 385 399 10.1016/S0896-6273(01)00213-6 11239430 · DOI
  98. [101]Joshi K. Lee S. Lee B. Lee J.W. Lee S.K. LMO4 controls the balance between excitatory and inhibitory spinal V2 interneurons Neuron 2009 61 839 851 10.1016/j.neuron.2009.02.011 19323994 PMC2848494 · DOI
  99. [102]Lundfald L. Restrepo C.E. Butt S.J. Peng C.Y. Droho S. Endo T. Zeilhofer H.U. Sharma K. Kiehn O. Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord Eur. J. Neurosci. 2007 26 2989 3002 10.1111/j.1460-9568.2007.05906.x 18028107 · DOI
  100. [103]Alvarez F.J. Jonas P.C. Sapir T. Hartley R. Berrocal M.C. Geiman E.J. Todd A.J. Goulding M. Postnatal phenotype and localization of spinal cord V1 derived interneurons J. Comp. Neurol. 2005 493 177 192 10.1002/cne.20711 16255029 PMC2997483 · DOI · Paper page
  101. [105]Condie B.G. Bain G. Gottlieb D.I. Capecchi M.R. Cleft palate in mice with a targeted mutation in the gamma-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67 Proc. Natl. Acad. Sci. USA 1997 94 11451 11455 10.1073/pnas.94.21.11451 9326630 PMC23502 · DOI
  102. [106]Ding R. Tsunekawa N. Obata K. Cleft palate by picrotoxin or 3-MP and palatal shelf elevation in GABA-deficient mice Neurotoxicol. Teratol. 2004 26 587 592 10.1016/j.ntt.2004.04.002 15203181 · DOI
  103. [107]Ji F. Kanbara N. Obata K. GABA and histogenesis in fetal and neonatal mouse brain lacking both the isoforms of glutamic acid decarboxylase Neurosci. Res. 1999 33 187 194 10.1016/S0168-0102(99)00011-5 10211762 · DOI
  104. [108]Gao B.X. Stricker C. Ziskind-Conhaim L. Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks J. Neurophysiol. 2001 86 492 502 10.1152/jn.2001.86.1.492 11431527 · DOI
  105. [109]Singer J.H. Berger A.J. Development of inhibitory synaptic transmission to motoneurons Brain Res. Bull. 2000 53 553 560 10.1016/S0361-9230(00)00389-0 11165791 · DOI
  106. [110]Kotak V.C. Korada S. Schwartz I.R. Sanes D.H. A developmental shift from GABAergic to glycinergic transmission in the central auditory system J. Neurosci. 1998 18 4646 4655 10.1523/JNEUROSCI.18-12-04646.1998 9614239 PMC6792682 · DOI
  107. [112]Nerlich J. Rubsamen R. Milenkovic I. Developmental Shift of Inhibitory Transmitter Content at a Central Auditory Synapse Front. Cell. Neurosci. 2017 11 211 10.3389/fncel.2017.00211 28769768 PMC5516124 · DOI
  108. [113]McMenamin C.A. Anselmi L. Travagli R.A. Browning K.N. Developmental regulation of inhibitory synaptic currents in the dorsal motor nucleus of the vagus in the rat J. Neurophysiol. 2016 116 1705 1714 10.1152/jn.00249.2016 27440241 PMC5144697 · DOI
  109. [114]Ma W. Saunders P.A. Somogyi R. Poulter M.O. Barker J.L. Ontogeny of GABAA receptor subunit mRNAs in rat spinal cord and dorsal root ganglia J. Comp. Neurol. 1993 338 337 359 10.1002/cne.903380303 7509352 · DOI
  110. [115]Laurie D.J. Wisden W. Seeburg P.H. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development J. Neurosci. 1992 12 4151 4172 10.1523/JNEUROSCI.12-11-04151.1992 1331359 PMC6576006 · DOI
  111. [116]LoTurco J.J. Owens D.F. Heath M.J. Davis M.B. Kriegstein A.R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis Neuron 1995 15 1287 1298 10.1016/0896-6273(95)90008-X 8845153 · DOI · Paper page
  112. [117]Kim M.O. Li S. Park M.S. Hornung J.P. Early fetal expression of GABA(B1) and GABA(B2) receptor mRNAs on the development of the rat central nervous system Brain Res. Dev. Brain Res. 2003 143 47 55 10.1016/S0165-3806(03)00099-3 12763580 · DOI
  113. [118]Watanabe E. Akagi H. Distribution patterns of mRNAs encoding glycine receptor channels in the developing rat spinal cord Neurosci. Res. 1995 23 377 382 10.1016/0168-0102(95)00972-V 8602277 · DOI
  114. [119]Takahashi T. Momiyama A. Hirai K. Hishinuma F. Akagi H. Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels Neuron 1992 9 1155 1161 10.1016/0896-6273(92)90073-M 1281418 · DOI
  115. [120]Withers M.D. St John P.A. Embryonic rat spinal cord neurons change expression of glycine receptor subtypes during development in vitro J. Neurobiol. 1997 32 579 592 10.1002/(SICI)1097-4695(19970605)32:6<579::AID-NEU4>3.0.CO;2-X 9183739 · DOI
  116. [121]Aguayo L.G. van Zundert B. Tapia J.C. Carrasco M.A. Alvarez F.J. Changes on the properties of glycine receptors during neuronal development Brain Res. Brain Res. Rev. 2004 47 33 45 10.1016/j.brainresrev.2004.06.007 15572161 · DOI
  117. [122]Jonsson S. Morud J. Pickering C. Adermark L. Ericson M. Soderpalm B. Changes in glycine receptor subunit expression in forebrain regions of the Wistar rat over development Brain Res. 2012 1446 12 21 10.1016/j.brainres.2012.01.050 22330726 · DOI
  118. [123]Aroeira R.I. Ribeiro J.A. Sebastiao A.M. Valente C.A. Age-related changes of glycine receptor at the rat hippocampus: From the embryo to the adult J. Neurochem. 2011 118 339 353 10.1111/j.1471-4159.2011.07197.x 21272003 · DOI
  119. [124]Borden L.A. GABA transporter heterogeneity: Pharmacology and cellular localization Neurochem. Int. 1996 29 335 356 10.1016/0197-0186(95)00158-1 8939442 · DOI
  120. [125]Jursky F. Nelson N. Developmental expression of GABA transporters GAT1 and GAT4 suggests involvement in brain maturation J. Neurochem. 1996 67 857 867 10.1046/j.1471-4159.1996.67020857.x 8764616 · DOI
  121. [126]Takayama C. Inoue Y. GABAergic signaling in the developing cerebellum Anat. Sci. Int. 2004 79 124 136 10.1111/j.1447-073x.2004.00081.x 15453613 · DOI
  122. [128]Hubner C.A. Stein V. Hermans-Borgmeyer I. Meyer T. Ballanyi K. Jentsch T.J. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition Neuron 2001 30 515 524 10.1016/S0896-6273(01)00297-5 11395011 · DOI
  123. [129]Lee H. Chen C.X. Liu Y.J. Aizenman E. Kandler K. KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses Eur. J. Neurosci. 2005 21 2593 2599 10.1111/j.1460-9568.2005.04084.x 15932617 PMC2945502 · DOI
  124. [130]Rivera C. Voipio J. Kaila K. Two developmental switches in GABAergic signalling: The K+-Cl− cotransporter KCC2 and carbonic anhydrase CAVII J. Physiol. 2005 562 27 36 10.1113/jphysiol.2004.077495 15528236 PMC1665491 · DOI · Paper page
  125. [131]Mahadevan V. Woodin M.A. Regulation of neuronal chloride homeostasis by neuromodulators J. Physiol. 2016 594 2593 2605 10.1113/JP271593 26876607 PMC4865579 · DOI
  126. [132]Delpy A. Allain A.E. Meyrand P. Branchereau P. NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron J. Physiol. 2008 586 1059 1075 10.1113/jphysiol.2007.146993 18096599 PMC2375629 · DOI
  127. [133]Tatetsu M. Kim J. Kina S. Sunakawa H. Takayama C. GABA/glycine signaling during degeneration and regeneration of mouse hypoglossal nerves Brain Res. 2012 1446 22 33 10.1016/j.brainres.2012.01.048 22325090 · DOI
  128. [134]Kim J. Kobayashi S. Shimizu-Okabe C. Okabe A. Moon C. Shin T. Takayama C. Changes in the expression and localization of signaling molecules in mouse facial motor neurons during regeneration of facial nerves J. Chem. Neuroanat. 2018 88 13 21 10.1016/j.jchemneu.2017.11.002 29113945 · DOI
  129. [135]Nabekura J. Ueno T. Okabe A. Furuta A. Iwaki T. Shimizu-Okabe C. Fukuda A. Akaike N. Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury J. Neurosci. 2002 22 4412 4417 10.1523/JNEUROSCI.22-11-04412.2002 12040048 PMC6758784 · DOI
  130. [136]Toyoda H. Ohno K. Yamada J. Ikeda M. Okabe A. Sato K. Hashimoto K. Fukuda A. Induction of NMDA and GABAA receptor-mediated Ca2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons J. Neurophysiol. 2003 89 1353 1362 10.1152/jn.00721.2002 12612004 · DOI
  131. [137]Stein V. Hermans-Borgmeyer I. Jentsch T.J. Hubner C.A. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride J. Comp. Neurol. 2004 468 57 64 10.1002/cne.10983 14648690 · DOI
  132. [138]Stil A. Liabeuf S. Jean-Xavier C. Brocard C. Viemari J.C. Vinay L. Developmental up-regulation of the potassium-chloride cotransporter type 2 in the rat lumbar spinal cord Neuroscience 2009 164 809 821 10.1016/j.neuroscience.2009.08.035 19699273 · DOI
  133. [139]Vinay L. Jean-Xavier C. Plasticity of spinal cord locomotor networks and contribution of cation-chloride cotransporters Brain Res. Rev. 2008 57 103 110 10.1016/j.brainresrev.2007.09.003 17949820 · DOI
  134. [140]Nishimaru H. Kakizaki M. The role of inhibitory neurotransmission in locomotor circuits of the developing mammalian spinal cord Acta Physiol. 2009 197 83 97 10.1111/j.1748-1716.2009.02020.x 19673737 · DOI
  135. [141]Vinay L. Brocard F. Pflieger J.F. Simeoni-Alias J. Clarac F. Perinatal development of lumbar motoneurons and their inputs in the rat Brain Res. Bull. 2000 53 635 647 10.1016/S0361-9230(00)00397-X 11165799 · DOI
  136. [142]Kahle K.T. Deeb T.Z. Puskarjov M. Silayeva L. Liang B. Kaila K. Moss S.J. Modulation of neuronal activity by phosphorylation of the K-Cl cotransporter KCC2 Trends Neurosci. 2013 36 726 737 10.1016/j.tins.2013.08.006 24139641 PMC4381966 · DOI
  137. [143]Kahle K.T. Delpire E. Kinase-KCC2 coupling: Cl− rheostasis, disease susceptibility, therapeutic target J. Neurophysiol. 2016 115 8 18 10.1152/jn.00865.2015 26510764 PMC4760510 · DOI
  138. [144]Fukuda A. Watanabe M. Pathogenic potential of human SLC12A5 variants causing KCC2 dysfunction Brain Res. 2019 1710 1 7 10.1016/j.brainres.2018.12.025 30576625 · DOI
  139. [145]Come E. Heubl M. Schwartz E.J. Poncer J.C. Levi S. Reciprocal Regulation of KCC2 Trafficking and Synaptic Activity Front. Cell. Neurosci. 2019 13 48 10.3389/fncel.2019.00048 30842727 PMC6391895 · DOI
  140. [146]Tang B.L. K(+)-Cl(−) co-transporter 2 (KCC2)—A membrane trafficking perspective Mol. Membr. Biol. 2016 33 100 110 10.1080/09687688.2017.1393566 29143559 · DOI
  141. [147]Lee H.H. Jurd R. Moss S.J. Tyrosine phosphorylation regulates the membrane trafficking of the potassium chloride co-transporter KCC2 Mol. Cell. Neurosci. 2010 45 173 179 10.1016/j.mcn.2010.06.008 20600929 PMC3529177 · DOI
  142. [148]Friedel P. Kahle K.T. Zhang J. Hertz N. Pisella L.I. Buhler E. Schaller F. Duan J. Khanna A.R. Bishop P.N. WNK1-regulated inhibitory phosphorylation of the KCC2 cotransporter maintains the depolarizing action of GABA in immature neurons Sci. Signal. 2015 8 ra65 10.1126/scisignal.aaa0354 26126716 · DOI
  143. [149]Watanabe M. Zhang J. Mansuri M.S. Duan J. Karimy J.K. Delpire E. Alper S.L. Lifton R.P. Fukuda A. Kahle K.T. Developmentally regulated KCC2 phosphorylation is essential for dynamic GABA-mediated inhibition and survival Sci. Signal. 2019 12 eaaw9315 10.1126/scisignal.aaw9315 31615901 PMC7219477 · DOI
  144. [150]Connor J.A. Tseng H.Y. Hockberger P.E. Depolarization- and transmitter-induced changes in intracellular Ca2+ of rat cerebellar granule cells in explant cultures J. Neurosci. 1987 7 1384 1400 10.1523/JNEUROSCI.07-05-01384.1987 2883269 PMC6568833 · DOI
  145. [152]Reichling D.B. Kyrozis A. Wang J. MacDermott A.B. Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons J. Physiol. 1994 476 411 421 10.1113/jphysiol.1994.sp020142 8057250 PMC1160455 · DOI
  146. [153]Leinekugel X. Tseeb V. Ben-Ari Y. Bregestovski P. Synaptic GABAA activation induces Ca2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices J. Physiol. 1995 487 Pt 2 319 329 10.1113/jphysiol.1995.sp020882 8558466 PMC1156575 · DOI
  147. [154]Obrietan K. van den Pol A.N. Growth cone calcium elevation by GABA J. Comp. Neurol. 1996 372 167 175 10.1002/(SICI)1096-9861(19960819)372:2<167::AID-CNE1>3.0.CO;2-1 8863123 · DOI
  148. [155]Ben-Ari Y. Khazipov R. Leinekugel X. Caillard O. Gaiarsa J.L. GABAA, NMDA and AMPA receptors: A developmentally regulated ‘menage a trois’ Trends Neurosci. 1997 20 523 529 10.1016/S0166-2236(97)01147-8 9364667 · DOI
  149. [156]Serafini R. Ma W. Maric D. Maric I. Lahjouji F. Sieghart W. Barker J.L. Initially expressed early rat embryonic GABA(A) receptor Cl- ion channels exhibit heterogeneous channel properties Eur. J. Neurosci. 1998 10 1771 1783 10.1046/j.1460-9568.1998.00187.x 9751149 · DOI
  150. [157]Eilers J. Plant T.D. Marandi N. Konnerth A. GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones J. Physiol. 2001 536 429 437 10.1111/j.1469-7793.2001.0429c.xd 11600678 PMC2278887 · DOI
  151. [158]McCarthy M.M. Auger A.P. Perrot-Sinal T.S. Getting excited about GABA and sex differences in the brain Trends Neurosci. 2002 25 307 312 10.1016/S0166-2236(02)02182-3 12086749 · DOI
  152. [159]Belhage B. Hansen G.H. Elster L. Schousboe A. Effects of gamma-aminobutyric acid (GABA) on synaptogenesis and synaptic function Perspect. Dev. Neurobiol. 1998 5 235 246 9777639
  153. [160]Kardos J. Recent advances in GABA research Neurochem. Int. 1999 34 353 358 10.1016/S0197-0186(99)00036-4 10397362 · DOI
  154. [161]Haydar T.F. Wang F. Schwartz M.L. Rakic P. Differential modulation of proliferation in the neocortical ventricular and subventricular zones J. Neurosci. 2000 20 5764 5774 10.1523/JNEUROSCI.20-15-05764.2000 10908617 PMC3823557 · DOI
  155. [162]Behar T.N. Schaffner A.E. Colton C.A. Somogyi R. Olah Z. Lehel C. Barker J.L. GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons J. Neurosci. 1994 14 29 38 10.1523/JNEUROSCI.14-01-00029.1994 8283236 PMC6576849 · DOI
  156. [163]Behar T.N. Li Y.X. Tran H.T. Ma W. Dunlap V. Scott C. Barker J.L. GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms J. Neurosci. 1996 16 1808 1818 10.1523/JNEUROSCI.16-05-01808.1996 8774448 PMC6578698 · DOI
  157. [164]Behar T.N. Schaffner A.E. Tran H.T. Barker J.L. GABA-induced motility of spinal neuroblasts develops along a ventrodorsal gradient and can be mimicked by agonists of GABAA and GABAB receptors J. Neurosci. Res. 1995 42 97 108 10.1002/jnr.490420111 8531231 · DOI
  158. [165]Abraham J.H. Schousboe A. Effects of taurine on cell morphology and expression of low-affinity GABA receptors in cultured cerebellar granule cells Neurochem. Res. 1989 14 1031 1038 10.1007/BF00965939 2558322 · DOI
  159. [166]Elster L. Hansen G.H. Belhage B. Fritschy J.M. Mohler H. Schousboe A. Differential distribution of GABAA receptor subunits in soma and processes of cerebellar granule cells: Effects of maturation and a GABA agonist Int. J. Dev. Neurosci. 1995 13 417 428 10.1016/0736-5748(95)00024-B 7484212 · DOI
  160. [167]Gao X.B. van den Pol A.N. GABA release from mouse axonal growth cones J. Physiol. 2000 523 Pt 3 629 637 10.1111/j.1469-7793.2000.t01-1-00629.x 10718743 PMC2269824 · DOI
  161. [168]Carlson B.X. Belhage B. Hansen G.H. Elster L. Olsen R.W. Schousboe A. Expression of the GABA(A) receptor alpha6 subunit in cultured cerebellar granule cells is developmentally regulated by activation of GABA(A) receptors J. Neurosci. Res. 1997 50 1053 1062 10.1002/(SICI)1097-4547(19971215)50:6<1053::AID-JNR17>3.0.CO;2-5 9452021 · DOI
  162. [169]Carlson B.X. Elster L. Schousboe A. Pharmacological and functional implications of developmentally-regulated changes in GABA(A) receptor subunit expression in the cerebellum Eur. J. Pharmacol. 1998 352 1 14 10.1016/S0014-2999(98)00355-0 9718261 · DOI
  163. [170]Mellor J.R. Merlo D. Jones A. Wisden W. Randall A.D. Mouse cerebellar granule cell differentiation: Electrical activity regulates the GABAA receptor alpha 6 subunit gene J. Neurosci. 1998 18 2822 2833 10.1523/JNEUROSCI.18-08-02822.1998 9525999 PMC6792580 · DOI
  164. [171]Moss S.J. Smart T.G. Constructing inhibitory synapses Nat. Rev. Neurosci. 2001 2 240 250 10.1038/35067500 11283747 · DOI
  165. [172]Meier E. Jorgensen O.S. Gamma-aminobutyric acid affects the developmental expression of neuron-associated proteins in cerebellar granule cell cultures J. Neurochem. 1986 46 1256 1262 10.1111/j.1471-4159.1986.tb00647.x 3950628 · DOI
  166. [173]Meier E. Jorgensen O.S. Schousboe A. Effect of repeated treatment with a gamma-aminobutyric acid receptor agonist on postnatal neural development in rats J. Neurochem. 1987 49 1462 1470 10.1111/j.1471-4159.1987.tb01015.x 3668533 · DOI
  167. [174]Wolff J.R. Joo F. Dames W. Plasticity in dendrites shown by continuous GABA administration in superior cervical ganglion of adult rat Nature 1978 274 72 74 10.1038/274072a0 661998 · DOI
  168. [175]Spoerri P.E. Neurotrophic effects of GABA in cultures of embryonic chick brain and retina Synapse 1988 2 11 22 10.1002/syn.890020104 3420527 · DOI
  169. [176]Barbin G. Pollard H. Gaiarsa J.L. Ben-Ari Y. Involvement of GABAA receptors in the outgrowth of cultured hippocampal neurons Neurosci. Lett. 1993 152 150 154 10.1016/0304-3940(93)90505-F 8390627 · DOI
  170. [177]Mitchell C.K. Redburn D.A. GABA and GABA-A receptors are maximally expressed in association with cone synaptogenesis in neonatal rabbit retina Brain Res. Dev. Brain Res. 1996 95 63 71 10.1016/0165-3806(96)00064-8 8873977 · DOI
  171. [178]Kim H.Y. Sapp D.W. Olsen R.W. Tobin A.J. GABA alters GABAA receptor mRNAs and increases ligand binding J. Neurochem. 1993 61 2334 2337 10.1111/j.1471-4159.1993.tb07481.x 8245988 · DOI
  172. [179]Saito K. Kakizaki T. Hayashi R. Nishimaru H. Furukawa T. Nakazato Y. Takamori S. Ebihara S. Uematsu M. Mishina M. The physiological roles of vesicular GABA transporter during embryonic development: A study using knockout mice Mol. Brain 2010 3 40 10.1186/1756-6606-3-40 21190592 PMC3023674 · DOI
  173. [180]Fujii M. Arata A. Kanbara-Kume N. Saito K. Yanagawa Y. Obata K. Respiratory activity in brainstem of fetal mice lacking glutamate decarboxylase 65/67 and vesicular GABA transporter Neuroscience 2007 146 1044 1052 10.1016/j.neuroscience.2007.02.050 17418495 · DOI
  174. [181]Yamada M.H. Nishikawa K. Kubo K. Yanagawa Y. Saito S. Impaired glycinergic synaptic transmission and enhanced inflammatory pain in mice with reduced expression of vesicular GABA transporter (VGAT) Mol. Pharmacol. 2012 81 610 619 10.1124/mol.111.076083 22275517 · DOI
  175. [182]Kakizaki T. Oriuchi N. Yanagawa Y. GAD65/GAD67 double knockout mice exhibit intermediate severity in both cleft palate and omphalocele compared with GAD67 knockout and VGAT knockout mice Neuroscience 2015 288 86 93 10.1016/j.neuroscience.2014.12.030 25545713 · DOI

Cited by

Sorted by citations

Authors
Shimizu-Okabe, C., Kobayashi, S., Kim, J., Kosaka, Y., Sunagawa, M., Okabe, A., & Takayama, C.
Affiliations
  • Department of Molecular Anatomy, Graduate School of Medicine, University of the Ryukyus, 207 Uehara, Nishihara 903-0215, Japan
  • University of the Ryukyus (JP)
  • Kosin University (KR)
  • Seinan Jo Gakuin University (JP)
Corresponding author
Takayama, Chitoshi
ORCID
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2022-01-13
Volume
23
Issue
2
Pages
834
ISSN
1422-0067 (ISSN-L)
DOI
10.3390/ijms23020834
PMC
PMC8776010
OpenAlex
W4225341257
Cited by
22
References
6
Citations by year
2026: 4 · 2025: 5 · 2024: 6 · 2023: 5 · 2022: 2
FWCI
0.64
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Molecular Sciences (publishedVersion, cc-by)
  • Preprints.org (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Japan Society for the Promotion of Science (JP18K07823, 21K0639, 20K16111, 19K19871)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Keywords
GABAergic neurons, glycinergic neurons, spinal cord development, inhibitory neurotransmission, ventricular zone, synaptogenesis, GABA receptor subunits, dorsal horn, ventral horn
MeSH terms
Animals, Anterior Horn Cells, Astrocytes, Axons, gamma-Aminobutyric Acid, Ganglia, Spinal, Glycine, Synaptic Transmission, Spinal Cord, Synapses, Signal Transduction, Biomarkers, Receptors, Glycine, Mice, GABAergic Neurons

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