Glycine receptors and brain development

Frontiers in Cellular Neuroscience

Volumn , Issue OCT, 2013, Pages

  Avila, Ariel ^a,b   Nguyen, Laurent ^b   Rigo, Jean Michel ^a  

^a HASSELT UNIVERSITY   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Brain development; Cortex; Glycine; Glycine receptors; GlyRs; Hippocampus; Interneurons; Migration

Indexed keywords

4 AMINOBUTYRIC ACID; CHLORIDE CHANNEL; GLYCINE; GLYCINE RECEPTOR; MESSENGER RNA; METHYLENETETRAHYDROFOLIC ACID; TAURINE;

AUTISM; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN MALFORMATION; BRAIN REGION; BRAIN STEM; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CHANNEL GATING; CYTOLOGY; EMBRYO DEVELOPMENT; EPILEPSY; GABAERGIC TRANSMISSION; GENE MUTATION; HIPPOCAMPUS; HUMAN; MOLECULAR MECHANICS; MOTOR CONTROL; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PATHOPHYSIOLOGY; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REVIEW; SCHIZOPHRENIA; SPINAL CORD; SYNAPTIC TRANSMISSION; THALAMUS;

EID: 84886841965     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00184     Document Type: Review

References (136)

1. Agmon, A., and O'Dowd, D. K. (1992). NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition.J. Neurophysiol. 68, 345-349.
2. Aroeira, R. I., Ribeiro, J. A., Sebastiao, A. M., and Valente, C. A. (2011). Age-related changes of glycine receptor at the rat hippocampus: from the embryo to the adult. J. Neurochem. 118, 339-353. doi: 10.1111/j.1471-4159.2011.07197.x
3. Avila, A., Vidal, P. M., Dear, T. N., Harvey, R. J., Rigo, J. M., and Nguyen, L. (2013). Glycine receptor alpha2 subunit activation promotes cortical interneuron migration. Cell Rep. 4, 738-750. doi: 10.1016/j.celrep.2013.07.016
4. Backus, K. H., Deitmer, J. W., and Friauf, E. (1998). Glycine-activated currents are changed by coincident membrane depolarization in developing rat auditory brainstem neurones. J. Physiol. 507(Pt 3), 783-794. doi: 10.1111/j.1469-7793.1998.783bs.x
5. Ben-Ari, Y. (2002). Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739. doi: 10.1038/nrn920
6. Ben-Ari, Y., Cherubini, E., Corradetti, R., and Gaiarsa, J. L. (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 416, 303-325.
7. Ben-Ari, Y., Gaiarsa, J. L., Tyzio, R., and Khazipov, R. (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284. doi: 10.1152/physrev.00017.2006
8. Ben-Ari, Y., Khalilov, I., Represa, A., and Gozlan, H. (2004). Interneurons set the tune of developing networks. Trends Neurosci. 27, 422-427. doi: 10.1016/j.tins.2004.05.002
9. Benitez-Diaz, P., Miranda-Contreras, L., Mendoza-Briceno, R. V., Pena-Contreras, Z., and Palacios-Pru, E. (2003). Prenatal and postnatal contents of amino acid neurotransmitters in mouse parietal cortex. Dev. Neurosci. 25, 366-374. doi: 10.1159/000073514
10. Bortone, D., and Polleux, F. (2009). KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 62, 53-71. doi: 10.1016/j.neuron.2009.01.034
11. Brackmann, M., Zhao, C., Schmieden, V., and Braunewell, K. H. (2004). Cellular and subcellular localization of the inhibitory glycine receptor in hippocampal neurons. Biochem. Biophys. Res. Commun. 324, 1137-1142. doi: 10.1016/j.bbrc.2004.09.172
12. Breustedt, J., Schmitz, D., Heinemann, U., and Schmieden, V. (2004). Characterization of the inhibitory glycine receptor on entorhinal cortex neurons. Eur. J. Neurosci. 19, 1987-1991. doi: 10.1111/j.1460-9568.2004.03266.x
13. Brickley, S. G., Cull-Candy, S. G., and 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, 753-759.
14. Caronia-Brown, G., and Grove, E. A. (2011). Timing of cortical interneuron migration is influenced by the cortical hem. Cereb. Cortex 21, 748-755. doi: 10.1093/cercor/bhq142
15. Chattipakorn, S. C., and McMahon, L. L. (2002). Pharmacological characterization of glycine-gated chloride currents recorded in rat hippocampal slices. J. Neurophysiol.87, 1515-1525.
16. Chattopadhyaya, B., and Cristo, G. D. (2012). GABAergic circuit dysfunctions in neurodevelopmental disorders. Front. Psychiatry 3:51. doi: 10.3389/fpsyt.2012.00051
17. Chen, R. Q., Wang, S. H., Yao, W., Wang, J. J., Ji, F., Yan, J. Z., et al. (2011). Role of glycine receptors in glycine-induced LTD in hippocampal CA1 pyramidal neurons. Neuropsychopharmacology 36, 1948-1958. doi: 10.1038/npp.2011.86
18. Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C., et al. (2005). Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 8, 1059-1068. doi: 10.1038/nn1499
19. Colin, I., Rostaing, P., Augustin, A., and Triller, A. (1998). Localization of components of glycinergic synapses during rat spinal cord development. J. Comp. Neurol. 398, 359-372. doi: 10.1002/(SICI)1096-9861(19980831)398:3<359::AID-CNE5>3.0.CO;2-Z
20. Cossart, R. (2011). The maturation of cortical interneuron diversity: how multiple developmental journeys shape the emergence of proper network function? Curr. Opin. Neurobiol. 21, 160-168. doi: 10.1016/j.conb.2010.10.003
21. Crook, J., Hendrickson, A., and Robinson, F. R. (2006). Co-localization of glycine and gaba immunoreactivity in interneurons in Macaca monkey cerebellar cortex. Neuroscience 141, 1951-1959. doi: 10.1016/j.neuroscience.2006.05.012
22. Cubelos, B., Gimenez, C., and Zafra, F. (2005). Localization of the GLYT1 glycine transporter at glutamatergic synapses in the rat brain. Cereb. Cortex 15, 448-459. doi: 10.1093/cercor/bhh147
23. Danglot, L., Rostaing, P., Triller, A., and Bessis, A. (2004). Morphologically identified glycinergic synapses in the hippocampus. Mol. Cell. Neurosci. 27, 394-403. doi: 10.1016/j.mcn.2004.05.007
24. De Saint Jan, D., David-Watine, B., Korn, H., and Bregestovski, P. (2001). Activation of human alpha1 and alpha2 homomeric glycine receptors by taurine and GABA. J. Physiol. 535, 741-755. doi: 10.1111/j.1469-7793.2001.t01-1-00741.x
25. Denter, D. G., Heck, N., Riedemann, T., White, R., Kilb, W., and Luhmann, H. J. (2010). GABAC receptors are functionally expressed in the intermediate zone and regulate radial migration in the embryonic mouse neocortex. Neuroscience 167, 124-134. doi: 10.1016/j.neuroscience.2010.01.049
26. Dieudonne, S. (1995). Glycinergic synaptic currents in Golgi cells of the rat cerebellum. Proc. Natl. Acad. Sci. U.S.A. 92, 1441-1445. doi: 10.1073/pnas.92.5.1441
27. Dougherty, J. D., Maloney, S. E., Wozniak, D. F., Rieger, M. A., Sonnenblick, L., Coppola, G., et al. (2013). The disruption of Celf6, a gene identified by translational profiling of serotonergic neurons, results in autism-related behaviors. J. Neurosci. 33, 2732-2753. doi: 10.1523/JNEUROSCI.4762-12.2013
28. Dugue, G. P., Dumoulin, A., Triller, A., and Dieudonne, S. (2005). Target-dependent use of co-released inhibitory transmitters at central synapses. J. Neurosci. 25, 6490-6498. doi: 10.1523/JNEUROSCI.1500-05.2005
29. Dumoulin, A., Triller, A., and Dieudonne, S. (2001). IPSC kinetics at identified GABAergic and mixed GABAergic and glycinergic synapses onto cerebellar Golgi cells.J. Neurosci. 21, 6045-6057.
30. Dunning, D. D., Hoover, C. L., Soltesz, I., Smith, M. A., and O'Dowd, D. K. (1999). GABA(A) receptor-mediated miniature postsynaptic currents and alpha-subunit expression in developing cortical neurons. J. Neurophysiol. 82, 3286-3297.
31. Dupont, E., Hanganu, I. L., Kilb, W., Hirsch, S., and Luhmann, H. J. (2006). Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 439, 79-83. doi: 10.1038/nature04264
32. - regulation. J. Physiol. 520, 121-137. doi: 10.1111/j.1469-7793.1999.00121.x
33. Eichler, S. A., Forstera, B., Smolinsky, B., Juttner, R., Lehmann, T. N., Fahling, M., et al. (2009). Splice-specific roles of glycine receptor alpha3 in the hippocampus. Eur. J. Neurosci. 30, 1077-1091. doi: 10.1111/j.1460-9568.2009.06903.x
34. Eichler, S. A., Kirischuk, S., Juttner, R., Schaefermeier, P. K., Legendre, P., Lehmann, T. N., et al. (2008). Glycinergic tonic inhibition of hippocampal neurons with depolarizing GABAergic transmission elicits histopathological signs of temporal lobe epilepsy. J. Cell Mol. Med. 12, 2848-2866. doi: 10.1111/j.1582-4934.2008.00357.x
35. Eulenburg, V., Retiounskaia, M., Papadopoulos, T., Gomeza, J., and Betz, H. (2010). Glial glycine transporter 1 function is essential for early postnatal survival but dispensable in adult mice. Glia 58, 1066-1073. doi: 10.1002/glia.20987
36. Flint, A. C., Liu, X., and Kriegstein, A. R. (1998). Nonsynaptic glycine receptor activation during early neocortical development. Neuron 20, 43-53. doi: 10.1016/S0896-6273(00)80433-X
37. Frostholm, A., and Rotter, A. (1985). Glycine receptor distribution in mouse CNS: autoradiographic localization of [3H]strychnine binding sites. Brain Res. Bull. 15, 473-486. doi: 10.1016/0361-9230(85)90038-3
38. Gao, B. X., Stricker, C., and Ziskind-Conhaim, L. (2001). Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J. Neurophysiol.86, 492-502.
39. Ghavanini, A. A., Mathers, D. A., and Puil, E. (2005). Glycinergic inhibition in thalamus revealed by synaptic receptor blockade. Neuropharmacology 49, 338-349. doi: 10.1016/j.neuropharm.2005.03.013
40. Gogolla, N., Leblanc, J. J., Quast, K. B., Sudhof, T. C., Fagiolini, M., and Hensch, T. K. (2009). Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J. Neurodev. Disord. 1, 172-181. doi: 10.1007/s11689-009-9023-x
41. Gomeza, J., Ohno, K., Hulsmann, S., Armsen, W., Eulenburg, V., Richter, D. W., et al. (2003). Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality. Neuron 40, 797-806. doi: 10.1016/S0896-6273(03)00673-1
42. Gozlan, H., and Ben-Ari, Y. (2003). Interneurons are the source and the targets of the first synapses formed in the rat developing hippocampal circuit. Cereb. Cortex 13, 684-692. doi: 10.1093/cercor/13.6.684
43. Gutierrez, R. (2003). The GABAergic phenotype of the "glutamatergic" granule cells of the dentate gyrus. Prog. Neurobiol. 71, 337-358. doi: 10.1016/j.pneurobio.2003.11.004
44. Harvey, R. J., Depner, U. B., Wassle, H., Ahmadi, S., Heindl, C., Reinold, H., et al. (2004). GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science 304, 884-887. doi: 10.1126/science.1094925
45. Heng, J. I., Moonen, G., and Nguyen, L. (2007). Neurotransmitters regulate cell migration in the telencephalon. Eur. J. Neurosci. 26, 537-546. doi: 10.1111/j.1460-9568.2007.05694.x
46. Hennou, S., Khalilov, I., Diabira, D., Ben-Ari, Y., and Gozlan, H. (2002). Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur. J. Neurosci. 16, 197-208. doi: 10.1046/j.1460-9568.2002.02073.x
47. Hussy, N., Deleuze, C., Pantaloni, A., Desarmenien, M. G., and Moos, F. (1997). Agonist action of taurine on glycine receptors in rat supraoptic magnocellular neurones: possible role in osmoregulation. J. Physiol. 502, 609-621. doi: 10.1111/j.1469-7793.1997.609bj.x
48. Ichinohe, A., Kure, S., Mikawa, S., Ueki, T., Kojima, K., Fujiwara, K., et al. (2004). Glycine cleavage system in neurogenic regions. Eur. J. Neurosci. 19, 2365-2370. doi: 10.1111/j.0953-816X.2004.03345.x
49. - homeostasis via with-no-lysine (WNK) protein kinase signaling pathway. J. Biol. Chem. 287, 20839-20850. doi: 10.1074/jbc.M111.319418
50. Ito, S., and Cherubini, E. (1991). Strychnine-sensitive glycine responses of neonatal rat hippocampal neurones. J. Physiol. 440, 67-83.
51. Jonsson, S., Morud, J., Pickering, C., Adermark, L., Ericson, M., and Soderpalm, B. (2012). Changes in glycine receptor subunit expression in forebrain regions of the Wistar rat over development. Brain Res. 1446, 12-21. doi: 10.1016/j.brainres.2012.01.050
52. Jursky, F., and Nelson, N. (1996). Developmental expression of the glycine transporters GLYT1 and GLYT2 in mouse brain. J. Neurochem. 67, 336-344. doi: 10.1046/j.1471-4159.1996.67010336.x
53. Jursky, F., Tamura, S., Tamura, A., Mandiyan, S., Nelson, H., and Nelson, N. (1994). Structure, function and brain localization of neurotransmitter transporters. J. Exp. Biol. 196, 283-295.
54. Kaneda, M., Farrant, M., and Cull-Candy, S. G. (1995). Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J. Physiol. 485(Pt 2), 419-435.
55. Kawa, K. (2003a). Glycine facilitates transmitter release at developing synapses: a patch clamp study from Purkinje neurons of the newborn rat. Brain Res. Dev. Brain Res. 144, 57-71. doi: 10.1016/S0165-3806(03)00159-7
56. Kawa, K. (2003b). Glycine receptors and glycinergic synaptic transmission in the deep cerebellar nuclei of the rat: a patch-clamp study. J. Neurophysiol. 90, 3490-3500. doi: 10.1152/jn.00447.2003
57. Keck, T., Lillis, K. P., Zhou, Y. D., and White, J. A. (2008). Frequency-dependent glycinergic inhibition modulates plasticity in hippocampus. J. Neurosci. 28, 7359-7369. doi: 10.1523/JNEUROSCI.5618-07.2008
58. Kilb, W., Hanganu, I. L., Okabe, A., Sava, B. A., Shimizu-Okabe, C., Fukuda, A., et al. (2008). Glycine receptors mediate excitation of subplate neurons in neonatal rat cerebral cortex. J. Neurophysiol. 100, 698-707. doi: 10.1152/jn.00657.2007
59. Kilb, W., Ikeda, M., Uchida, K., Okabe, A., Fukuda, A., and Luhmann, H. J. (2002). Depolarizing glycine responses in Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 112, 299-307. doi: 10.1016/S0306-4522(02)00071-4
60. Kirsch, J., Kuhse, J., and Betz, H. (1995). Targeting of glycine receptor subunits to gephyrin-rich domains in transfected human embryonic kidney cells. Mol. Cell. Neurosci. 6, 450-461. doi: 10.1006/mcne.1995.1033
61. Konur, S., and Ghosh, A. (2005). Calcium signaling and the control of dendritic development. Neuron 46, 401-405. doi: 10.1016/j.neuron.2005.04.022
62. Kotak, V. C., Korada, S., Schwartz, I. R., and Sanes, D. H. (1998). A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J. Neurosci. 18, 4646-4655.
63. Kubota, H., Alle, H., Betz, H., and Geiger, J. R. (2010). Presynaptic glycine receptors on hippocampal mossy fibers. Biochem. Biophys. Res. Commun. 393, 587-591. doi: 10.1016/j.bbrc.2010.02.019
64. Kuhse, J., Kuryatov, A., Maulet, Y., Malosio, M. L., Schmieden, V., and Betz, H. (1991). Alternative splicing generates two isoforms of the alpha 2 subunit of the inhibitory glycine receptor. FEBS Lett. 283, 73-77. doi: 10.1016/0014-5793(91)80557-J
65. Kunz, P. A., Burette, A. C., Weinberg, R. J., and Philpot, B. D. (2012). Glycine receptors support excitatory neurotransmitter release in developing mouse visual cortex. J. Physiol. 590, 5749-5764. doi: 10.1113/jphysiol.2012.241299
66. Lall, D., Armbruster, A., Ruffert, K., Betz, H., and Eulenburg, V. (2012). Transport activities and expression patterns of glycine transporters 1 and 2 in the developing murine brain stem and spinal cord. Biochem. Biophys. Res. Commun. 423, 661-666. doi: 10.1016/j.bbrc.2012.06.007
67. Le-Corronc, H., Rigo, J. M., Branchereau, P., and Legendre, P. (2011). GABA(A) receptor and glycine receptor activation by paracrine/autocrine release of endogenous agonists: more than a simple communication pathway. Mol. Neurobiol.44, 28-52. doi: 10.1007/s12035-011-8185-1
68. Lee, E. A., Cho, J. H., Choi, I. S., Nakamura, M., Park, H. M., Lee, J. J., et al. (2009). Presynaptic glycine receptors facilitate spontaneous glutamate release onto hilar neurons in the rat hippocampus. J. Neurochem. 109, 275-286. doi: 10.1111/j.1471-4159.2009.05960.x
69. Lee, H., Chen, C. X., Liu, Y. J., Aizenman, E., and Kandler, K. (2005). KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur. J. Neurosci. 21, 2593-2599. doi: 10.1111/j.1460-9568.2005.04084.x
70. Legendre, P., Forstera, B., Juttner, R., and Meier, J. C. (2009). Glycine receptors caught between genome and proteome-functional implications of RNA editing and splicing. Front. Mol. Neurosci. 2:23. doi: 10.3389/neuro.02.023.2009
71. Li, Y., and Xu, T. L. (2002). State-dependent cross-inhibition between anionic GABA(A) and glycine ionotropic receptors in rat hippocampal CA1 neurons. Neuroreport 13, 223-226. doi: 10.1097/00001756-200202110-00010
72. LoTurco, J. J., Owens, D. F., Heath, M. J., Davis, M. B., and Kriegstein, A. R. (1995). GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287-1298. doi: 10.1016/0896-6273(95)90008-X
73. Lu, T., Rubio, M. E., and Trussell, L. O. (2008). Glycinergic transmission shaped by the corelease of GABA in a mammalian auditory synapse. Neuron 57, 524-535. doi: 10.1016/j.neuron.2007.12.010
74. Lynch, J. W. (2009). Native glycine receptor subtypes and their physiological roles. Neuropharmacology 56, 303-309. doi: 10.1016/j.neuropharm.2008.07.034
75. Lynch, J. W., and Callister, R. J. (2006). Glycine receptors: a new therapeutic target in pain pathways. Curr. Opin. Invest. Drugs 7, 48-53.
76. Malosio, M. L., Grenningloh, G., Kuhse, J., Schmieden, V., Schmitt, B., Prior, P., et al. (1991a). Alternative splicing generates two variants of the alpha 1 subunit of the inhibitory glycine receptor. J. Biol. Chem. 266, 2048-2053.
77. Malosio, M. L., Marqueze-Pouey, B., Kuhse, J., and Betz, H. (1991b). Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J. 10, 2401-2409.
78. Manent, J. B., Demarque, M., Jorquera, I., Pellegrino, C., Ben-Ari, Y., Aniksztejn, L., et al. (2005). A noncanonical release of GABA and glutamate modulates neuronal migration. J. Neurosci. 25, 4755-4765. doi: 10.1523/JNEUROSCI.0553-05.2005
79. Manent, J. B., and Represa, A. (2007). Neurotransmitters and brain maturation: early paracrine actions of GABA and glutamate modulate neuronal migration. Neuroscientist 13, 268-279. doi: 10.1177/1073858406298918
80. Marin, O. (2012). Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120.
81. Martina, M., Gorfinkel, Y., Halman, S., Lowe, J. A., Periyalwar, P., Schmidt, C. J., 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. doi: 10.1113/jphysiol.2004.063321
82. Marty, S., Berninger, B., Carroll, P., and Thoenen, H. (1996). GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16, 565-570. doi: 10.1016/S0896-6273(00)80075-6
83. Matzenbach, B., Maulet, Y., Sefton, L., Courtier, B., Avner, P., Guenet, J. L., et al. (1994). Structural analysis of mouse glycine receptor alpha subunit genes. Identification and chromosomal localization of a novel variant. J. Biol. Chem. 269, 2607-2612.
84. McDearmid, J. R., Liao, M., and Drapeau, P. (2006). Glycine receptors regulate interneuron differentiation during spinal network development. Proc. Natl. Acad. Sci. U.S.A. 103, 9679-9684. doi: 10.1073/pnas.0504871103
85. Moss, S. J., and Smart, T. G. (2001). Constructing inhibitory synapses. Nat. Rev. Neurosci. 2, 240-250. doi: 10.1038/35067500
86. Muller, E., Le Corronc, H., Scain, A. L., Triller, A., and Legendre, P. (2008). Despite GABAergic neurotransmission, GABAergic innervation does not compensate for the defect in glycine receptor postsynaptic aggregation in spastic mice. Eur. J. Neurosci.27, 2529-2541. doi: 10.1111/j.1460-9568.2008.06217.x
87. Muller, E., Le Corronc, H., Triller, A., and Legendre, P. (2006). Developmental dissociation of presynaptic inhibitory neurotransmitter and postsynaptic receptor clustering in the hypoglossal nucleus. Mol. Cell. Neurosci. 32, 254-273. doi: 10.1016/j.mcn.2006.04.007
88. Nabekura, J., Katsurabayashi, S., Kakazu, Y., Shibata, S., Matsubara, A., Jinno, S., et al. (2004). Developmental switch from GABA to glycine release in single central synaptic terminals. Nat. Neurosci. 7, 17-23. doi: 10.1038/nn1170
89. Nguyen, L., Malgrange, B., Belachew, S., Rogister, B., Rocher, V., Moonen, G., et al. (2002). Functional glycine receptors are expressed by postnatal nestin-positive neural stem/progenitor cells. Eur. J. Neurosci. 15, 1299-1305. doi: 10.1046/j.1460-9568.2002.01966.x
90. Nguyen, L., Rigo, J. M., Rocher, V., Belachew, S., Malgrange, B., Rogister, B., et al. (2001). Neurotransmitters as early signals for central nervous system development. Cell Tissue Res. 305, 187-202. doi: 10.1007/s004410000343
91. Nikolic, Z., Laube, B., Weber, R. G., Lichter, P., Kioschis, P., Poustka, A., et al. (1998). The human glycine receptor subunit alpha3. Glra3 gene structure, chromosomal localization, and functional characterization of alternative transcripts. J. Biol. Chem.273, 19708-19714. doi: 10.1074/jbc.273.31.19708
92. Nimmervoll, B., Denter, D. G., Sava, I., Kilb, W., and Luhmann, H. J. (2011). Glycine receptors influence radial migration in the embryonic mouse neocortex. Neuroreport22, 509-513. doi: 10.1097/WNR.0b013e328348aafe
93. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L., and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144. doi: 10.1038/nn1172
94. Oertel, J., Villmann, C., Kettenmann, H., Kirchhoff, F., and Becker, C. M. (2007). A novel glycine receptor beta subunit splice variant predicts an unorthodox transmembrane topology. Assembly into heteromeric receptor complexes. J. Biol. Chem. 282, 2798-2807. doi: 10.1074/jbc.M608941200
95. Okabe, A., Kilb, W., Shimizu-Okabe, C., Hanganu, I. L., Fukuda, A., and Luhmann, H. J. (2004). Homogenous glycine receptor expression in cortical plate neurons and Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 123, 715-724. doi: 10.1016/j.neuroscience.2003.10.014
96. Owens, D. F., Boyce, L. H., Davis, M. B., and Kriegstein, A. R. (1996). Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16, 6414-6423.
97. Pedroarena, C. M., and Kamphausen, S. (2008). Glycinergic synaptic currents in the deep cerebellar nuclei. Neuropharmacology 54, 784-795. doi: 10.1016/j.neuropharm.2007.12.005
98. Piton, A., Gauthier, J., Hamdan, F. F., Lafreniere, R. G., Yang, Y., Henrion, E., et al. (2011). Systematic resequencing of X-chromosome synaptic genes in autism spectrum disorder and schizophrenia. Mol. Psychiatry 16, 867-880. doi: 10.1038/mp.2010.54
99. Pla, R., Borrell, V., Flames, N., and Marin, O. (2006). Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J. Neurosci. 26, 6924-6934. doi: 10.1523/JNEUROSCI.0245-06.2006
100. 2+ entry leads to glutamate secretion in mouse neocortical preplate. Proc. Natl. Acad. Sci. U.S.A. 102, 19174-19179. doi: 10.1073/pnas.0504540102
101. Pribilla, I., Takagi, T., Langosch, D., Bormann, J., and Betz, H. (1992). The atypical M2 segment of the beta subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. EMBO J. 11, 4305-4311.
102. Probst, A., Cortes, R., and Palacios, J. M. (1986). The distribution of glycine receptors in the human brain. A light microscopic autoradiographic study using [3H]strychnine. Neuroscience 17, 11-35. doi: 10.1016/0306-4522(86)90222-8
103. Rahman, J., Latal, A. T., Besser, S., Hirrlinger, J., and Hulsmann, S. (2013). Mixed miniature postsynaptic currents resulting from co-release of glycine and GABA recorded from glycinergic neurons in the neonatal respiratory network. Eur. J. Neurosci. 37, 1229-1241. doi: 10.1111/ejn.12136
104. Rees, M. I., Harvey, K., Ward, H., White, J. H., Evans, L., Duguid, I. C., et al. (2003). Isoform heterogeneity of the human gephyrin gene (GPHN), binding domains to the glycine receptor, and mutation analysis in hyperekplexia. J. Biol. Chem. 278, 24688-24696. doi: 10.1074/jbc.M301070200
105. Represa, A., and Ben-Ari, Y. (2005). Trophic actions of GABA on neuronal development. Trends Neurosci. 28, 278-283. doi: 10.1016/j.tins.2005.03.010
106. Ripps, H., and Shen, W. (2012). Review: taurine: a "very essential" amino acid. Mol. Vis. 18, 2673-2686.
107. Sahara, S., Yanagawa, Y., O'Leary, D. D., and Stevens, C. F. (2012). The fraction of cortical GABAergic neurons is constant from near the start of cortical neurogenesis to adulthood. J. Neurosci. 32, 4755-4761. doi: 10.1523/JNEUROSCI.6412-11.2012
108. Sauer, J. F., and Bartos, M. (2011). Postnatal differentiation of cortical interneuron signalling. Eur. J. Neurosci. 34, 1687-1696. doi: 10.1111/j.1460-9568.2011.07872.x
109. Scain, A. L., Le Corronc, H., Allain, A. E., Muller, E., Rigo, J. M., Meyrand, P., 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. doi: 10.1523/JNEUROSCI.2115-09.2010
110. Schmieden, V., Kuhse, J., and Betz, H. (1992). Agonist pharmacology of neonatal and adult glycine receptor alpha subunits: identification of amino acid residues involved in taurine activation. EMBO J. 11, 2025-2032.
111. Seybold, B. A., Stanco, A., Cho, K. K., Potter, G. B., Kim, C., Sohal, V. S., et al. (2012). Chronic reduction in inhibition reduces receptive field size in mouse auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 109, 13829-13834. doi: 10.1073/pnas.1205909109
112. Singer, J. H. (2008). GABA is an endogenous ligand for synaptic glycine receptors. Neuron 57, 475-477. doi: 10.1016/j.neuron.2008.02.007
113. Singer, J. H., Talley, E. M., Bayliss, D. A., and Berger, A. J. (1998). Development of glycinergic synaptic transmission to rat brain stem motoneurons. J. Neurophysiol.80, 2608-2620.
114. Song, W., Chattipakorn, S. C., and McMahon, L. L. (2006). Glycine-gated chloride channels depress synaptic transmission in rat hippocampus. J. Neurophysiol. 95, 2366-2379. doi: 10.1152/jn.00386.2005
115. Sorensen, S. A., Bernard, A., Menon, V., Royall, J. J., Glattfelder, K. J., Hirokawa, K., et al. (2013). Correlated gene expression and target specificity demonstrate excitatory projection neuron diversity. Cereb. Cortex doi: 10.1093/cercor/bht243 [Epub ahead of print].
116. Soria, J. M., and Valdeolmillos, M. (2002). Receptor-activated calcium signals in tangentially migrating cortical cells. Cereb. Cortex 12, 831-839. doi: 10.1093/cercor/12.8.831
117. Sturman, J. A. (1988). Taurine in development. J. Nutr. 118, 1169-1176.
118. Sturman, J. A. (1991). Dietary taurine and feline reproduction and development. J. Nutr. 121, S166-S170.
119. Thio, L. L., Shanmugam, A., Isenberg, K., and Yamada, K. (2003). Benzodiazepines block alpha2-containing inhibitory glycine receptors in embryonic mouse hippocampal neurons. J. Neurophysiol. 90, 89-99. doi: 10.1152/jn.00612.2002
120. Turecek, R., and Trussell, L. O. (2001). Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature 411, 587-590. doi: 10.1038/35079084
121. Tyzio, R., Holmes, G. L., Ben-Ari, Y., and Khazipov, R. (2007). Timing of the developmental switch in GABA(A) mediated signaling from excitation to inhibition in CA3 rat hippocampus using gramicidin perforated patch and extracellular recordings. Epilepsia 48(Suppl. 5), 96-105. doi: 10.1111/j.1528-1167.2007.01295.x
122. van den Pol, A. N. (2004). Developing neurons make the switch. Nat. Neurosci. 7, 7-8. doi: 10.1038/nn0104-7
123. van den Pol, A. N., and Gorcs, T. (1988). Glycine and glycine receptor immunoreactivity in brain and spinal cord. J. Neurosci. 8, 472-492.
124. Verheugen, J. A., Fricker, D., and Miles, R. (1999). Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J. Neurosci.19, 2546-2555.
125. Waseem, T. V., and Fedorovich, S. V. (2010). Presynaptic glycine receptors influence plasma membrane potential and glutamate release. Neurochem. Res. 35, 1188-1195. doi: 10.1007/s11064-010-0174-7
126. Watanabe, E., and Akagi, H. (1995). Distribution patterns of mRNAs encoding glycine receptor channels in the developing rat spinal cord. Neurosci. Res. 23, 377-382. doi: 10.1016/0168-0102(95)00972-V
127. Wegner, F., Kraft, R., Busse, K., Hartig, W., Ahrens, J., Leffler, A., et al. (2012). Differentiated human midbrain-derived neural progenitor cells express excitatory strychnine-sensitive glycine receptors containing alpha2beta subunits. PLoS ONE7:e36946. doi: 10.1371/journal.pone.0036946
128. Wu, W. L., Ziskind-Conhaim, L., and Sweet, M. A. (1992). Early development of glycine-and GABA-mediated synapses in rat spinal cord. J. Neurosci. 12, 3935-3945.
129. Xu, T. L., and Gong, N. (2010). Glycine and glycine receptor signaling in hippocampal neurons: diversity, function and regulation. Prog. Neurobiol. 91, 349-361. doi: 10.1016/j.pneurobio.2010.04.008
130. Yee, B. K., Balic, E., Singer, P., Schwerdel, C., Grampp, T., Gabernet, L., et al. (2006). Disruption of glycine transporter 1 restricted to forebrain neurons is associated with a procognitive and antipsychotic phenotypic profile. J. Neurosci. 26, 3169-3181. doi: 10.1523/JNEUROSCI.5120-05.2006
131. Yoshida, M., Fukuda, S., Tozuka, Y., Miyamoto, Y., and 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. doi: 10.1002/neu.20003
132. Young-Pearse, T. L., Ivic, L., Kriegstein, A. R., and Cepko, C. L. (2006). Characterization of mice with targeted deletion of glycine receptor alpha 2. Mol. Cell. Biol. 26, 5728-5734. doi: 10.1128/MCB.00237-06
133. Yu, T. W., Chahrour, M. H., Coulter, M. E., Jiralerspong, S., Okamura-Ikeda, K., Ataman, B., et al. (2013). Using whole-exome sequencing to identify inherited causes of autism. Neuron 77, 259-273. doi: 10.1016/j.neuron.2012.11.002
134. Zeilhofer, H. U. (2005). The glycinergic control of spinal pain processing. Cell. Mol. Life Sci. 62, 2027-2035. doi: 10.1007/s00018-005-5107-2
135. Zhang, L. H., Gong, N., Fei, D., Xu, L., and Xu, T. L. (2008). Glycine uptake regulates hippocampal network activity via glycine receptor-mediated tonic inhibition. Neuropsychopharmacology 33, 701-711. doi: 10.1038/sj.npp.1301449
136. Zhu, L., Lovinger, D., and Delpire, E. (2005). Cortical neurons lacking KCC2 expression show impaired regulation of intracellular chloride. J. Neurophysiol. 93, 1557-1568. doi: 10.1152/jn.00616.2004