Emerging neurotrophic role of GABAB receptors in neuronal circuit development

Frontiers in Cellular Neuroscience

Volumn 6, Issue NOV, 2013, Pages

  Gaiarsa, Jean Luc ^a,b,c   Porcher, Christophe ^a,b,c  

^a Institut National de la Santé el de la Recherche Médicale   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c Turing Center for Living Systems CENTURI Aix Marseille University   (France)

Author keywords

Cortical development; GABA; GABAB receptors; Migration; Synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; BACLOFEN; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM; CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROTRANSMITTER; TROPOMYOSIN; VOLTAGE GATED CALCIUM CHANNEL;

BINDING SITE; BRAIN; BRAIN DEVELOPMENT; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CHEMOKINESIS; CHEMOTAXIS; DEVELOPMENTAL STAGE; EXOCYTOSIS; HUMAN; HYPOTHALAMUS; IN VIVO STUDY; INTRACELLULAR SIGNALING; MAMMAL; MOLECULAR CLONING; NERVE CELL DIFFERENTIATION; NERVE CELL INHIBITION; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE FUNCTION; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NEUROTROPISM; NONHUMAN; OLFACTORY BULB; OLIGODENDROGLIA; ONTOGENY; PERINATAL PERIOD; PRESYNAPTIC POTENTIAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM; REVIEW; SYNAPTOGENESIS; XENOPUS;

EID: 84888155744     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00206     Document Type: Review

References (112)

1. Behar, T. N., Li, Y. X., Tran, H. T., Ma, W., Dunlap, V., Scott, C., et al. (1996). GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. J. Neurosci. 16, 1808-1818.
2. Behar, T. N., Schaffner, A. E., Colton, C. A., Somogyi, R., Olah, Z., Lehel, C., et al. (1994). GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons. J. Neurosci. 14,29-38.
3. Behar, T. N., Schaffner, A. E., Scott, C. A., Greene, C. L., and Barker, J. L. (2000). GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb. Cortex 10, 899-909.doi: 10.1093/cercor/10.9.899
4. Behar, T. N., Schaffner, A. E., Scott, C. A., O'Connell, C., and Barker, J. L. (1998). Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus. J. Neurosci. 18, 6378-6387.
5. Behar, T. N., Schaffner, A. E., Tran, H. T., and Barker, J. L. (1995). 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. 42, 97-108.doi: 10.1002/jnr.490420111
6. Behar, T. N., Smith, S. V., Kennedy, R. T., McKenzie, J. M., Maric, I., and Barker, J. L. (2001). GABA(B) receptors mediate motility signals for migrating embryonic cortical cells. Cereb. Cortex 11, 744-753.doi: 10.1093/cercor/11.8.744
7. Ben-Ari, Y., Cherubini, E., Corradetti, R., and Gaiarsa, J.-L. (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. (Lond.) 416, 303-325.
8. 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
9. Bianchi, M. S., Lux-Lantos, V. A., Bettler, B., and Libertun, C. (2005). Expression of gamma-aminobutyric acid B receptor subunits in hypothalamus of male and female developing rats. Brain Res. Dev. Brain Res. 160, 124-129.doi: 10.1016/j.devbrainres.2005.06.017
10. Biermann, B., Ivankova-Susankova, K., Bradaia, A., Abdel, A. S., Besseyrias, V., Kapfhammer, J. P., et al. (2010). The sushi domains of GABAb receptors function as axonal targeting signals. J. Neurosci. 30, 1385-1394.doi: 10.1523/JNEUR0SCI.3172-09.2010
11. Bird, M., and Owen, A. (1998). Neurite outgrowth-regulating properties of GABA and the effect ofserum on mouse spinal cord neurons in culture. J. Anat. 193(Pt 4), 503-508.doi: 10.1046/j.1469-7580.1998.19340503.x
12. Blackmer, T., Larsen, E. C., Bartleson, C., Kowalchyk, J. A., Yoon, E. J., Preininger, A. M., et al. (2005). G protein betagamma directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat. Neurosci. 8, 421-425.
13. Bony, G., Szczurkowska, J., Tamagno, I., Shelly, M., Contestabile, A., and Cancedda, L. (2013). Non-hyperpolarizing GABAb receptor activation regulates neuronal migration and neurite growth and specification by cAMP/LKB1. Nat. Commun. 4, 1800.doi: 10.1038/ncomms2820
14. Bowery, N. G. (1993). GABAb receptor pharmacology. Annu. Rev. Pharmacol. Toxicol. 33, 109-147.doi: 10.1146/annurev.pa.33.040193.000545
15. Bowery, N. G., Bettler, B., Froestl, W., Gallagher, J. P., Marshall, F., Raiteri, M., et al. (2002). International union of pharmacology. XXXIII. Mammalian gamma-aminobutyric acid (B) receptors: structure and function. Pharmacol. Rev. 54, 247-264.doi: 10.1124/pr.54.2.247
16. Caillard, O., McLean, H. A., Ben-Ari, Y., and Gai'arsa, J.-L. (1998). Ontogenesis of presynaptic GABAB receptor-mediated inhibition in the CA3 region of the rat hippocampus. J. Neurophysiol. 79,1341-1348.
17. Cancedda, L., Fiumelli, H., Chen, K., and Poo, M. M. (2007). Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J. Neurosci. 27, 5224-5235.doi: 10.1523/JNEUR0SCI.5169-06.2007
18. Catsicas, S., and Mobbs, P. (2001). GABAb receptors regulate chick retinal calcium waves. J. Neurosci. 21, 897-910.
19. Chang, E.H., Kotak, V. C., and Sanes, D.H. (2003). Long-termdepression ofsynaptic inhibition is expressed postsynaptically in the developing auditory system. J. Neurophysiol. 90,1479-1488.doi: 10.1152/jn.00386.2003
20. Chattopadhyaya, B., Di Cristo, G., Wu, C. Z., Knott, G., Kuhlman, S., Fu, Y., et al. (2007). GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54, 889-903.doi: 10.1016/j.neuron.2007.05.015
21. Chudotvorova, I., Ivanov, A., Rama, S., Hubner, C. A., Pellegrino, C., Ben-Ari, Y., et al. (2005). Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses. J. Physiol. 566, 671-679.doi: 10.1113/jphysiol.2005.089821
22. Colin-Le Brun, I., Ferrand, N., Caillard, O., Tosetti, P., Ben-Ari, Y., and Gaiarsa, J. L. (2004). Spontaneous synaptic activity is required for the formation of functional GABAergic synapses in the developing rat hippocampus. J. Physiol. 559, 129-139.doi: 10.1113/jphysiol.2004.065060
23. Correa, S. A., Munton, R., Nishimune, A., Fitzjohn, S., and Henley, J. M. (2004). Development of GABAB subunits and functional GABAB receptors in rat cultured hippocampal neurons. Neuropharmacology 47, 475-484.doi: 10.1016/j.neuropharm.2004.04.021
24. Davis, A. M., Henion, T. R., and Tobet, S. A. (2002). Gamma-aminobutyric acid B receptors and the development of the ventromedial nucleus of the hypothalamus. J. Comp. Neurol. 449, 270-280.doi: 10.1002/cne.10293
25. Demarque, M., Represa, A., Becq, H., Khalilov, I., Ben-Ari, Y., and Aniksztejn, L. (2002). Paracrine intercellular communication by a Ca(2+)- and SNARE- independent release of GABA and glutamate prior to synapse formation. Neuron 36,1051-1061.doi: 10.1016/S0896-6273(02)01053-X
26. Dutar, P., and Nicoll, R. A. (1988). A physiological role for GABAb receptors in the central nervous system. Nature 332, 156-158.doi: 10.1038/332156a0
27. Ehrengruber, M. U., Doupnik, C. A., Xu, Y., Garvey, J., Jasek, M. C., Lester, H. A., et al. (1997). Activation of heteromeric G protein-gated inward rectifier K+ channels overexpressed by adenovirus gene transfer inhibits the excitability of hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 94, 7070-7075.doi: 10.1073/pnas.94.13.7070
28. Ferguson, S. C., and McFarlane, S. (2002). GABA and development of the Xenopus optic projection. J. Neurobiol. 51, 272-284.doi: 10.1002/neu.10061
29. Fiorentino, H., Kuczewski, N., Diabira, D., Ferrand, N., Pangalos, M. N., Porcher, C., et al. (2009). GABA(B) receptor activation triggers BDNF release and promotes the maturation of GABAergic synapses. J. Neurosci. 29, 11650-11661.doi: 10.1523/JNEUROSCI.3587-09.2009
30. Fritschy, J. M., Meskenaite, V., Weinmann, O., Honer, M., Benke, D., and Mohler, H. (1999). GABAB-receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization. Eur. J. Neurosci. 11, 761-768.doi: 10.1046/j.1460-9568.1999. 00481.x
31. Fritschy, J. M., Sidler, C., Parpan, F., Gassmann, M., Kaupmann, K., Bettler, B., et al. (2004). Independent maturation of the GABA(B) receptor subunits GABA(B1) and GABA(B2) during postnatal development in rodent brain. J. Comp. Neurol. 477,235-252.doi: 10.1002/cne.20188
32. Fukuda, A., Mody, I., and Prince, D. A. (1993). Differential ontogenesis of presy- naptic and postsynaptic GABAB inhibition in the rat somatosensory cortex. J. Neurophysiol. 70, 448-452.
33. Gahwiler, B. H., and Brown, D.A. (1985). GABAB-receptor-activatedK+ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures. Proc. Natl. Acad. Sci. U.S.A. 82, 1558-1562.doi: 10.1073/pnas.82.5.1558
34. Gaiarsa, J.-L., Tseeb, V., and Ben-Ari, Y. (1995). Postnatal development of pre- and postsynaptic GABAB-mediated inhibitions in the CA3 hippocampal region of the rat. J. Neurophysiol. 73, 246-255.
35. Gambardella, A., Manna, I., Labate, A., Chifari, R., La, R. A., Serra, P., et al. (2003). GABA(B) receptor 1 polymorphism (G1465A) is associated with temporal lobe epilepsy. Neurology 60, 560-563.doi: 10.1212/01.WNL.0000046520. 79877.D8
36. Gao, X. B., and Van den Pol, A. N. (2000). GABA release from mouse axonal growth cones. J. Physiol. 523(Pt 3), 629-637.doi: 10.1111/j.1469-7793.2000.t01- 1-00629.x
37. Gascon, E., Dayer, A. G., Sauvain, M. O., Potter, G., Jenny, B., De, R. M., et al. (2006). GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J. Neurosci. 26, 12956-12966.doi: 10.1523/JNEUROSCI.4508-06.2006
38. Gassmann, M., Shaban, H., Vigot, R., Sansig, G., Haller, C., Barbieri, S., et al. (2004). Redistribution of GABAb(1) protein and atypical GABAb responses in GABAB(2)-deficient mice. J. Neurosci. 24, 6086-6097.doi: 10.1523/JNEUROSCI.5635-03.2004
39. Ge, S., Goh, E. L., Sailor, K. A., Kitabatake, Y., Ming, G. L., and Song, H. (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589-593.doi: 10.1038/nature04404
40. Gottmann, K., Mittmann, T., and Lessmann, V. (2009). BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp. BrainRes. 199,203-234.doi: 10.1007/s00221-009-1994-z
41. Guetg, N., Seddik, R., Vigot, R., Turecek, R., Gassmann, M., Vogt, K. E., et al. (2009). The GABAB1a isoform mediates heterosynaptic depression at hippocampal mossy fiber synapses. J. Neurosci. 29, 1414-1423.doi: 10.1523/JNEUROSCI.3697-08.2009
42. Haller, C., Casanova, E., Muller, M., Vacher, C. M., Vigot, R., Doll, T., et al. (2004). Floxed allele for conditional inactivation of the GABAb(1) gene. Genesis 40, 125-130.doi: 10.1002/gene.20073
43. Hassfurth, B., Grothe, B., and Koch, U. (2010). The mammalian interaural time difference detection circuit is differentially controlled by GABAB receptors during development. J. Neurosci. 30,9715-9727.doi: 10.1523/JNEUROSCI.1552-10.2010
44. Hirono, M., Yoshioka, T., and Konishi, S. (2001). GABA(B) receptor activation enhances mGluR-mediated responses at cerebellar excitatorysynapses. Nat. Neurosci. 4, 1207-1216.doi: 10.1038/nn764
45. Inagaki, T., Begum, T., Reza, F., Horibe, S., Inaba, M., Yoshimura, Y., et al. (2008). Brain-derived neurotrophic factor-mediated retrograde signaling required for the induction of long-term potentiation at inhibitory synapses of visual cortical pyramidal neurons. Neurosci. Res. 61, 192-200.doi: 10.1016/j.neures.2008. 02.006
46. Isaacson, J. S., and Nicoll, R. A. (1993). Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10, 165-175.doi: 10.1016/0896-6273(93)90308-E
47. Ji, F., Kanbara, N., and Obata, K. (1999). GABA and histogenesis in fet al and neonatal mouse brain lacking both the isoforms of glutamic acid decarboxylase. Neurosci. Res. 33, 187-194.doi: 10.1016/S0168-0102(99)00011-5
48. Jones, K. A., Borowsky, B., Tamm, J. A., Craig, D. A., Durkin, M. M., Dai, M., et al. (1998). GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature 396, 674-679.doi: 10.1038/25348
49. Kaeser, G. E., Rabe, B. A., and Saha, M. S. (2011). Cloning and characterization of GABAa alpha subunits and GABAb subunits in Xenopus laevis during development. Dev. Dyn. 240, 862-873.doi: 10.1002/dvdy.22580
50. Katz, L. C., and Shatz, C. J. (1996). Synaptic activityand the construction of cortical circuits. Science 274, 1133-1138.doi: 10.1126/science.274.5290.1133
51. Kaupmann, K., Huggel, K., Heid, J., Flor, P. J., Bischoff, S., Mickel, S. J., et al. (1997). Expression cloning of GABAB receptors uncovers similarity to metabotropic glutamate receptors. Nature 386, 239-246.doi: 10.1038/386239a0
52. Kaupmann, K., Malitschek, B., Schuler, V., Heid, J., Froestl, W., Beck, P., et al. (1998). GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature 396, 683-687.doi: 10.1038/25360
53. Khazipov, R., Leinekugel, X., Khalilov, I., Gaiarsa, J.-L., and Ben-Ari, Y. (1997). Synchronization of GABAergic interneuronal network in CA3 subfield of neonatal rat hippocampal slices. J. Physiol. (Lond.) 498, 763-772.
54. Khazipov, R., and Luhmann, H. J. (2006). Early patterns of electrical activity in the developing cerebral cortex ofhumans and rodents. Trends Neurosci. 29,414-418.doi: 10.1016/j.tins.2006.05.007
55. Kim, M. O., Li, S., Park, M. S., and Hornung, J. P. (2003). Early fet al expression of GABA(B1) and GABA(B2) receptor mRNAs on the development of the rat centralnervoussystem. Brain Res. Dev. BrainRes. 143,47-55.doi: 10.1016/S0165- 3806(03)00099-3
56. Kirmse, K., and 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.doi: 10.1523/JNEUR0SCI.0589-06.2006
57. Kolarow, R., Brigadski, T., and Lessmann, V. (2007). Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium calmodulin kinase II signaling and proceeds via delayed fusion pore opening. J. Neurosci. 27, 10350-10364.doi: 10.1523/JNEUROSCI.0692-07.2007
58. Komatsu, Y., and Iwakiri, M. (1993). Long-term modification of inhibitory synaptic transmission in developing visual cortex. Neuroreport 4, 907-910.doi: 10.1097/00001756-199307000-00017
59. Kotak, V. C., and Sanes, D. H. (2000). Long-lasting inhibitory synaptic depression is age- and calcium-dependent. J. Neurosci. 20, 5820-5826.
60. Kotak, V. C., and Sanes, D. H. (2002). Postsynaptic kinase signaling underlies inhibitorysynaptic plasticityin the lateral superior olive. J. Neurobiol. 53, 36-43.doi: 10.1002/neu.10107
61. Kuczewski, N., Fuchs, C., Ferrand, N., Jovanovic, J. N., Gaiarsa, J. L., and Porcher, C. (2011). Mechanism of GABA(B) receptor-induced BDNF secretion and promotion of GABA(A) receptor membrane expression. J. Neurochem. 118, 533-545.doi: 10.1111/j.1471-4159.2011.07192.x
62. Kulik, A., Vida, I., Lujan, R., Haas, C. A., Lopez-Bendito, G., Shigemoto, R., et al. (2003). Subcellular localization of metabotropic GABA(B) receptor subunits GABA(B1a/b) and GABA(B2) in the rat hippocampus. J. Neurosci. 23, 11026-11035.
63. Lancaster, E., Lai, M., Peng, X., Hughes, E., Constantinescu, R., Raizer, J., et al. (2010). Antibodies to the GABA(B) receptor in limbic encephalitis with seizures: case series and characterisation of the antigen. Lancet Neurol. 9, 67-76.doi: 10.1016/S1474-4422(09)70324-2
64. Lopez-Bendito, G., Lujan, R., Shigemoto, R., Ganter, P., Paulsen, O., and Molnar, Z. (2003). Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. Cereb. Cortex 13, 932-942.doi: 10.1093/cercor/13.9.932
65. Lopez-Bendito, G., Shigemoto, R., Kulik, A., Paulsen, O., Fairen, A., and Lujan, R. (2002). Expression and distribution of metabotropic GABA receptor subtypes GABAbr1 and GABAbr2 during rat neocortical development. Eur. J. Neurosci. 15, 1766-1778.doi: 10.1046/j.1460-9568.2002.02032.x
66. Lopez-Bendito, G., Shigemoto, R., Kulik, A., Vida, I., Fairen, A., and Lujan, R. (2004). Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 14, 836-848.doi: 10.1002/hipo.10221
67. Luhmann, H. J., and Prince, D. A. (1991). Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 247-263.
68. Lujan, R., and Shigemoto, R. (2006). Localization of metabotropic GABA receptor subunits GABAB1 and GABAB2 relative to synaptic sites in the rat developing cerebellum. Eur. J. Neurosci. 23, 1479-1490.doi: 10.1111/j.1460-9568.2006. 04669.x
69. Luyt, K., Slade, T. P., Dorward, J. J., Durant, C. F., Wu, Y., Shigemoto, R., et al. (2007). Developing oligodendrocytes express functional GABA(B) receptors that stimulate cell proliferation and migration. J. Neurochem. 100, 822-840.doi: 10.1111/j.1471-4159.2006.04255.x
70. Manent, J. B., Beguin, S., Ganay, T., and Represa, A. (2011). Cell-autonomous and cell-to-cell signalling events in normal and altered neuronal migration. Eur. J. Neurosci. 34, 1595-1608.doi: 10.1111/j.1460-9568.2011.07867.x
71. 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
72. Maric, D., Liu, Q. Y., Maric, I., Chaudry, S., Chang, Y. H., Smith, S. V., et al. (2001). GABA expression dominates neuronal lineage progression in the embryonic rat neocortex and facilitates neurite outgrowth via GABA(A) autoreceptor/Cl-channels. J. Neurosci. 21, 2343-2360.
73. Martin, S. C., Steiger, J. L., Gravielle, M. C., Lyons, H. R., Russek, S. J., and Farb, D. H. (2004). Differential expression of gamma-aminobutyric acid type B receptor subunit mRNAs in the developing nervous system and receptor coupling to adenylyl cyclase in embryonic neurons. J. Comp. Neurol. 473, 16-29.doi: 10.1002/cne.20094
74. McClellan, K. M., Calver, A. R., and Tobet, S.A. (2008). GABAb receptorsrole in cell migration and positioningwithin the ventromedial nucleus of the hypothalamus. Neuroscience 151, 1119-1131.doi: 10.1016/j.neuroscience.2007.11.048
75. McLean, H. A., Caillard, O., Khazipov, R., Ben-Ari, Y., and Gaiarsa, J.-L. (1996). Spontaneous release of GABA activates GABAB receptors and controls network activityin the neonatal rat hippocampus. J. Neurophysiol. 76, 1036-1046.
76. Meier, S. D., Kafitz, K. W., and Rose, C. R. (2008). Developmental profile and mechanisms of GABA-induced calcium signaling in hippocampal astrocytes. Glia 56, 1127-1137.doi: 10.1002/glia.20684
77. 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.doi: 10.1016/0736-5748(90)90078-G
78. Mintz, I. M., and Bean, B. P. (1993). GABAB receptor inhibition of P-type Ca2 + channels in central neurons. Neuron 10, 889-898.doi: 10.1016/0896- 6273(93)90204-5
79. New, D. C., An, H., Ip, N. Y., and Wong, Y. H. (2006). GABAb heterodimeric receptorspromote Ca2+ influxviastore-operatedchannels inratcortical neurons and transfected Chinese hamster ovary cells. Neuroscience 137, 1347-1358. doi: 10.1016/j.neuroscience.2005.10.033
80. Nurse, S., and Lacaille, J. C. (1999). Late maturation of GABA(B) synaptic transmission in area CA1 of the rat hippocampus. Neuropharmacology 38,1733-1742. doi: 10.1016/S0028-3908(99)00122-7
81. Obrietan, K., and Van den Pol, A. N. (1998). GABAB receptor-mediated inhibition of GABAA receptor calcium elevations in developing hypothalamic neurons. J. Neurophysiol. 79,1360-1370.
82. Obrietan, K., andVan den Pol, A. N. (1999). GABAb receptor-mediated regulation of glutamate-activated calcium transients in hypothalamic and cortial neuron development. J. Neurophysiol. 81, 94-102.
83. Owens, D. F., and Kriegstein, A. R. (2002). Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715-727. doi: 10.1038/nrn919
84. Perez-Garci, E., Gassmann, M., Bettler, B., and Larkum, M. E. (2006). The GABAB1b isoform mediates long-lasting inhibition of dendritic Ca2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 50, 603-616. doi: 10.1016/j.neuron.2006.04.019
85. Priest, C. A., and Puche, A. C. (2004). GABAB receptor expression and function in olfactory receptor neuron axon growth. J. Neurobiol. 60, 154-165. doi: 10.1002/neu.20011
86. Prosser, H. M., Gill, C. H., Hirst, W.D., Grau, E., Robbins, M., Calver, A., et al. (2001). Epileptogenesis and enhanced prepulse inhibition in GABA(B1)-deficient mice. Mol. Cell. Neurosci. 17,1059-1070. doi: 10.1006/mcne.2001.0995
87. Queva, C., Bremner-Danielsen, M., Edlund, A., Ekstrand, A. J., Elg, S., Erickson, S., et al. (2003). Effects of GABA agonists on body temperature regulation in GABA(B(1))-/-mice. Br. J. Pharmacol. 140,315-322. doi: 10.1038/sj.bjp.0705447
88. Reynolds, A., Brustein, E., Liao, M., Mercado, A., Babilonia, E., Mount, D. B., 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. doi: 10.1523/JNEUROSCI.3791-07.2008
89. Rivera, C., Voipio, J., Payne, J. A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., et al. (1999). TheK+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255. doi: 10.1038/16697
90. Robbins, M. J., Calver, A. R., Filippov, A. K., Hirst, W. D., Russell, R. B., Wood, M. D., et al. (2001). GABA(B2) is essential for G-protein coupling of the GABA(B) receptor heterodimer. J. Neurosci. 21, 8043-8052.
91. Root, C. M., Velazquez-Ulloa, N. A., Monsalve, G. C., Minakova, E., and Spitzer, N. C. (2008). Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J. Neurosci. 28, 4777-4784. doi: 10.1523/JNEUROSCI.4873-07.2008
92. Sakaba, T., and Neher, E. (2003). Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424, 775-778. doi: 10.1038/nature01859
93. Scanziani, M. (2000). GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25, 673-681. doi: 10.1016/S0896- 6273(00)81069-7
94. Schuler, V., Luscher, C., Blanchet, C., Klix, N., Sansig, G., Klebs, K., et al. (2001). Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron 31, 47-58. doi: 10.1016/S0896-6273(01)00345-2
95. Sernagor, E., Chabrol, F., Bony, G., and Cancedda, L. (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. doi: 10.3389/fncel.2010.00011
96. Taylor, J., and Gordon-Weeks, P. R. (1991). Calcium-indenpendent g-aminobutyric acid release from growth cones: role of g-aminobutyric acid transport. J. Neurochem. 56,273-280. doi: 10.1111/j.1471-4159.1991.tb02592.x
97. Thompson, S. M., and Gahwiler, B. H. (1992a). Comparison of the actions of baclofen at pre- and postsynaptic receptors in the rat hippocampus in vitro. J. Physiol. 451, 329-345.
98. Thompson, S. M., and Gahwiler, B. H. (1992b). Effects of the GABA uptake inhibitor tiagabine on inhibitory synaptic potentials in rat hippocampal slice cultures. J. Neurophysiol. 67, 1698-1701.
99. Tosetti, P., Bakels, R., Colin-Le Brun, I., Ferrand, N., Gaiarsa, J. L., and Caillard, O. (2004).Acute desensitization of presynaptic GABAB-mediated inhibition and induction of epileptiform discharges in the neonatal rat hippocampus. Eur. J. Neurosci. 19, 3227-3234. doi: 10.1111/j.0953-816X.2004.03413.x
100. Tosetti, P., Ferrand, N., Brun, I. C., and Gaiarsa, J. L. (2005). Epileptiform activity triggers long-term plasticity of GABAB receptor signalling in the developing rat hippocampus. J. Physiol. 568, 951-966. doi: 10.1113/jphysiol.2005. 094631
101. Tremblay, E., Ben-Ari, Y., and Roisin, M. P. (1995). Different GABAB-mediated effects on protein kinase C activity and immunoreactivity in neonatal and adult rat hippocampal slices. J. Neurochem. 65, 863-870. doi: 10.1046/j.1471- 4159.1995.65020863.x
102. Turgeon, S. M., and Albin, R. L. (1994). Postnatal ontogeny of GABAB binding in rat brain. Neuroscience 62, 601-613. doi: 10.1016/0306-4522(94)90392-1
103. 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.
104. Vernon, E., Meyer, G., Pickard, L., Dev, K., Molnar, E., Collingridge, G. L., et al. (2001). GABA(B) receptors couple directly to the transcription factorATF4. Mol. Cell. Neurosci. 17, 637-645. doi: 10.1006/mcne.2000.0960
105. Vigot, R., Barbieri, S., Brauner-Osborne, H., Turecek, R., Shigemoto, R., Zhang, Y. P., et al. (2006). Differential compartmentalization and distinct functions of GABAb receptor variants. Neuron 50, 589-601. doi: 10.1016/j.neuron.2006. 04.014
106. Wang, D. D., and Kriegstein, A. R. (2008). GABA regulatesexcitatorysynapse formation in the neocortex via NMDA receptor activation. J. Neurosci. 28, 5547-5558.doi: 10.1523/JNEUROSCI.5599-07.2008
107. Wang, X., Sun, W., Zhu, X., Li, L., Wu, X., Lin, H., et al. (2008).Association between the gamma-aminobutyric acid type B receptor 1 and 2 gene polymorphisms and mesial temporal lobe epilepsy in a Han Chinese population. Epilepsy Res. 81, 198-203.doi: 10.1016/j.eplepsyres.2008.06.001
108. White, J. H., McIllhinney, R. A., Wise, A., Ciruela, F., Chan, W. Y., Emson, P. C., et al. (2000). The GABAB receptor interacts directly with the related transcription factors CREB2 and ATFx. Proc. Natl. Acad. Sci. U.S.A. 97, 13967-13972.doi: 10.1073/pnas.240452197
109. White, J. H., Wise, A., Main, M. J., Green, A., Fraser, N. J., Disney, G. H., et al. (1998). Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature396, 679-682.doi: 10.1038/25354
110. Wu, Y., Chan, K. F., Eubanks, J. H., Guin Ting, W. C., Cortez, M. A., Shen, L., et al. (2007). Transgenic mice over-expressing GABA(B)R1a receptors acquire an atypical absence epilepsy-like phenotype. Neurobiol. Dis. 26, 439-451. doi: 10.1016/j.nbd.2007.01.013
111. Xiang, Y., Li, Y., Zhang, Z., Cui, K., Wang, S., Yuan, X. B., et al. (2002). Nerve growth cone guidance mediated by G protein-coupled receptors. Nat. Neurosci. 5, 843-848. doi: 10.1038/nn899
112. Xu, C., Zhao, M.X., Poo, M. M., and Zhang, X. H. (2008). GABA(B) receptor activation mediates frequency-dependent plasticity of developing GABAergic synapses. Nat. Neurosci. 11, 1410-1418. doi: 10.1038/nn.2215