Emerging themes in GABAergic synapse development

Progress in Neurobiology

Volumn 95, Issue 1, 2011, Pages 68-87

  Kuzirian, Marissa S ^a   Paradis, Suzanne ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

GABAergic; Glutamatergic; Synapse development

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; COLLYBISTIN; DYSTROPHIN; EPIDERMAL GROWTH FACTOR RECEPTOR 4; GEPHYRIN; GLUTAMIC ACID; GUANINE NUCLEOTIDE EXCHANGE FACTOR; KERATINOCYTE GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; NEUREXIN; NEUROLIGIN; SEMAPHORIN; UNCLASSIFIED DRUG;

ASTROCYTE; AUTISM; CYTOLOGY; DEPOLARIZATION; GABAERGIC SYSTEM; HIPPOCAMPUS; HUMAN; MOLECULAR BIOLOGY; NERVE ENDING; NEUROLOGIC DISEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RETT SYNDROME; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; GAMMA-AMINOBUTYRIC ACID; HUMANS; NEURONAL PLASTICITY; NEURONS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 79961102105     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2011.07.002     Document Type: Review

References (300)

1. Abrahams B.S., Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 2008, 9:341-355.
2. - co-transporter KCC2. Development 2003, 130:1267-1280.
3. Ahmari S.E., Buchanan J., Smith S.J. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat. Neurosci. 2000, 3:445-451.
4. Akerman C.J., Cline H.T. Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J. Neurosci. 2006, 26:5117-5130.
5. Allene C., Cossart R. Early NMDA receptor-driven waves of activity in the developing neocortex: physiological or pathological network oscillations?. J. Physiol. 2010, 588:83-91.
6. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999, 23:185-188.
7. Andersen P., Eccles J.C., Loyning Y. Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature 1963, 198:540-542.
8. Andersen P., Eccles J.C., Loyning Y. Pathway of postsynaptic inhibition in the hippocampus. J. Neurophysiol. 1964, 27:608-619.
9. Anderson T.R., Shah P.A., Benson D.L. Maturation of glutamatergic and GABAergic synapse composition in hippocampal neurons. Neuropharmacology 2004, 47:694-705.
10. Ango F., di Cristo G., Higashiyama H., Bennett V., Wu P., Huang Z.J. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 2004, 119:257-272.
11. Araque A., Parpura V., Sanzgiri R.P., Haydon P.G. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 1999, 22:208-215.
12. Bailey A., Le Couteur A., Gottesman I., Bolton P., Simonoff E., Yuzda E., Rutter M. Autism as a strongly genetic disorder: evidence from a British twin study. Psychol. Med. 1995, 25:63-77.
13. Balasubramanian S., Fam S.R., Hall R.A. GABAB receptor association with the PDZ scaffold Mupp1 alters receptor stability and function. J. Biol. Chem. 2007, 282:4162-4171.
14. Baldelli P., Fassio A., Valtorta F., Benfenati F. Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J. Neurosci. 2007, 27:13520-13531.
15. Baldelli P., Hernandez-Guijo J.M., Carabelli V., Carbone E. Brain-derived neurotrophic factor enhances GABA release probability and nonuniform distribution of N- and P/Q-type channels on release sites of hippocampal inhibitory synapses. J. Neurosci. 2005, 25:3358-3368.
16. Bannai H., Levi S., Schweizer C., Inoue T., Launey T., Racine V., Sibarita J.B., Mikoshiba K., Triller A. Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron 2009, 62:670-682.
17. Barros C.S., Calabrese B., Chamero P., Roberts A.J., Korzus E., Lloyd K., Stowers L., Mayford M., Halpain S., Muller U. Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4507-4512.
18. Barrow S.L., Constable J.R., Clark E., El-Sabeawy F., McAllister A.K., Washbourne P. Neuroligin1: a cell adhesion molecule that recruits PSD-95 and NMDA receptors by distinct mechanisms during synaptogenesis. Neural Dev. 2009, 4:17.
19. Baumann S.W., Baur R., Sigel E. Subunit arrangement of gamma-aminobutyric acid type A receptors. J. Biol. Chem. 2001, 276:36275-36280.
20. Bear M.F., Huber K.M., Warren S.T. The mGluR theory of fragile X mental retardation. Trends Neurosci. 2004, 27:370-377.
21. Beattie E.C., Stellwagen D., Morishita W., Bresnahan J.C., Ha B.K., Von Zastrow M., Beattie M.S., Malenka R.C. Control of synaptic strength by glial TNFalpha. Science 2002, 295:2282-2285.
22. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 2002, 3:728-739.
23. Ben-Ari Y., Cherubini E., Corradetti R., Gaiarsa J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 1989, 416:303-325.
24. Ben-Ari Y., Gaiarsa J.L., Tyzio R., Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 2007, 87:1215-1284.
25. Ben-Ari Y., Khalilov I., Represa A., Gozlan H. Interneurons set the tune of developing networks. Trends Neurosci. 2004, 27:422-427.
26. 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.
27. Boehler M.D., Wheeler B.C., Brewer G.J. Added astroglia promote greater synapse density and higher activity in neuronal networks. Neuron Glia Biol. 2007, 3:127-140.
28. Bogdanov Y., Michels G., Armstrong-Gold C., Haydon P.G., Lindstrom J., Pangalos M., Moss S.J. Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J. 2006, 25:4381-4389.
29. Boucard A.A., Chubykin A.A., Comoletti D., Taylor P., Sudhof T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 2005, 48:229-236.
30. Boulland J.L., Qureshi T., Seal R.P., Rafiki A., Gundersen V., Bergersen L.H., Fremeau R.T., Edwards R.H., Storm-Mathisen J., Chaudhry F.A. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J. Comp. Neurol. 2004, 480:264-280.
31. Bouzioukh F., Daoudal G., Falk J., Debanne D., Rougon G., Castellani V. Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. Eur. J. Neurosci. 2006, 23:2247-2254.
32. Bowery N.G., Brown D.A. The cloning of GABA(B) receptors. Nature 1997, 386:223-224.
33. Bresler T., Ramati Y., Zamorano P.L., Zhai R., Garner C.C., Ziv N.E. The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Mol. Cell. Neurosci. 2001, 18:149-167.
34. Brunig I., Suter A., Knuesel I., Luscher B., Fritschy J.M. GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin. J. Neurosci. 2002, 22:4805-4813.
35. Buhl E.H., Halasy K., Somogyi P. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 1994, 368:823-828.
36. Burrone J., Li Z., Murthy V.N. Studying vesicle cycling in presynaptic terminals using the genetically encoded probe synaptopHluorin. Nat. Protoc. 2006, 1:2970-2978.
37. Cabelli R.J., Allendoerfer K.L., Radeke M.J., Welcher A.A., Feinstein S.C., Shatz C.J. Changing patterns of expression and subcellular localization of TrkB in the developing visual system. J. Neurosci. 1996, 16:7965-7980.
38. Ceccaldi P.E., Benfenati F., Chieregatti E., Greengard P., Valtorta F. Rapid binding of synapsin I to F- and G-actin. A study using fluorescence resonance energy transfer. FEBS Lett. 1993, 329:301-305.
39. Cellerino A., Maffei L., Domenici L. The distribution of brain-derived neurotrophic factor and its receptor trkB in parvalbumin-containing neurons of the rat visual cortex. Eur. J. Neurosci. 1996, 8:1190-1197.
40. Cesca F., Baldelli P., Valtorta F., Benfenati F. The synapsins: key actors of synapse function and plasticity. Prog. Neurobiol. 2010, 91:313-348.
41. Chadman K.K., Gong S., Scattoni M.L., Boltuck S.E., Gandhy S.U., Heintz N., Crawley J.N. Minimal aberrant behavioral phenotypes of neuroligin-3 R451C knockin mice. Autism Res. 2008, 1:147-158.
42. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
43. Chalifoux J.R., Carter A.G. GABAB receptors modulate NMDA receptor calcium signals in dendritic spines. Neuron 2010, 66:101-113.
44. Chalifoux J.R., Carter A.G. GABA(B) receptor modulation of synaptic function. Curr. Opin. Neurobiol. 2011, 21:339-344.
45. Chang Y., Wang R., Barot S., Weiss D.S. Stoichiometry of a recombinant GABAA receptor. J. Neurosci. 1996, 16:5415-5424.
46. Chao H.T., Chen H., Samaco R.C., Xue M., Chahrour M., Yoo J., Neul J.L., Gong S., Lu H.C., Heintz N., et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 2010, 468:263-269.
47. Chao H.T., Zoghbi H.Y., Rosenmund C. MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 2007, 56:58-65.
48. Chattopadhyaya B., Di Cristo G., Higashiyama H., Knott G.W., Kuhlman S.J., Welker E., Huang Z.J. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 2004, 24:9598-9611.
49. Chattopadhyaya B., Di Cristo G., Wu C.Z., Knott G., Kuhlman S., Fu Y., Palmiter R.D., Huang Z.J. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 2007, 54:889-903.
50. Cheetham J.J., Murray J., Ruhkalova M., Cuccia L., McAloney R., Ingold K.U., Johnston L.J. Interaction of synapsin I with membranes. Biochem. Biophys. Res. Commun. 2003, 309:823-829.
51. Chen A.I., Nguyen C.N., Copenhagen D.R., Badurek S., Minichiello L., Ranscht B., Reichardt L.F. TrkB (tropomyosin-related kinase B) controls the assembly and maintenance of GABAergic synapses in the cerebellar cortex. J. Neurosci. 2011, 31:2769-2780.
52. Chen G., Trombley P.Q., van den Pol A.N. GABA receptors precede glutamate receptors in hypothalamic development; differential regulation by astrocytes. J. Neurophysiol. 1995, 74:1473-1484.
53. Chen R.Z., Akbarian S., Tudor M., Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 2001, 27:327-331.
54. Chen X., Ye H., Kuruvilla R., Ramanan N., Scangos K.W., Zhang C., Johnson N.M., England P.M., Shokat K.M., Ginty D.D. A chemical-genetic approach to studying neurotrophin signaling. Neuron 2005, 46:13-21.
55. Chiappalone M., Casagrande S., Tedesco M., Valtorta F., Baldelli P., Martinoia S., Benfenati F. Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks. Cereb. Cortex 2009, 19:1422-1439.
56. Chih B., Engelman H., Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005, 307:1324-1328.
57. Chih B., Gollan L., Scheiffele P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 2006, 51:171-178.
58. Chiou T.T., Bonhomme B., Jin H., Miralles C.P., Xiao H., Fu Z., Harvey R.J., Harvey K., Vicini S., De Blas A.L. Differential regulation of the postsynaptic clustering of {gamma}-aminobutyric acid type A (GABAA) receptors by collybistin isoforms. J. Biol. Chem. 2011, 286:22456-22468.
59. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005, 120:421-433.
60. Chubykin A.A., Atasoy D., Etherton M.R., Brose N., Kavalali E.T., Gibson J.R., Sudhof T.C. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007, 54:919-931.
61. Chudotvorova I., Ivanov A., Rama S., Hubner C.A., Pellegrino C., Ben-Ari Y., Medina I. Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses. J. Physiol. 2005, 566:671-679.
62. Cobb S., Guy J., Bird A. Reversibility of functional deficits in experimental models of Rett syndrome. Biochem. Soc. Trans. 2010, 38:498-506.
63. Cobb S.R., Buhl E.H., Halasy K., Paulsen O., Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 1995, 378:75-78.
64. Cohen S., Greenberg M.E. Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu. Rev. Cell Dev. Biol. 2008, 24:183-209.
65. Coles J.A., Abbott N.J. Signalling from neurones to glial cells in invertebrates. Trends Neurosci. 1996, 19:358-362.
66. Colonnier M. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 1968, 9:268-287.
67. Correia S.S., Bassani S., Brown T.C., Lise M.F., Backos D.S., El-Husseini A., Passafaro M., Esteban J.A. Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat. Neurosci. 2008, 11:457-466.
68. Cossart R., Petanjek Z., Dumitriu D., Hirsch J.C., Ben-Ari Y., Esclapez M., Bernard C. Interneurons targeting similar layers receive synaptic inputs with similar kinetics. Hippocampus 2006, 16:408-420.
69. Craig A.M., Blackstone C.D., Huganir R.L., Banker G. Selective clustering of glutamate and gamma-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:12373-12377.
70. Craig A.M., Graf E.R., Linhoff M.W. How to build a central synapse: clues from cell culture. Trends Neurosci. 2006, 29:8-20.
71. Craig A.M., Kang Y. Neurexin-neuroligin signaling in synapse development. Curr. Opin. Neurobiol. 2007, 17:43-52.
72. Dai Z., Peng H.B. Dynamics of synaptic vesicles in cultured spinal cord neurons in relationship to synaptogenesis. Mol. Cell. Neurosci. 1996, 7:443-452.
73. Dalva M.B., McClelland A.C., Kayser M.S. Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci. 2007, 8:206-220.
74. Danglot L., Triller A., Marty S. The development of hippocampal interneurons in rodents. Hippocampus 2006, 16:1032-1060.
75. Dani V.S., Chang Q., Maffei A., Turrigiano G.G., Jaenisch R., Nelson S.B. Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:12560-12565.
76. Dani V.S., Nelson S.B. Intact long-term potentiation but reduced connectivity between neocortical layer 5 pyramidal neurons in a mouse model of Rett syndrome. J. Neurosci. 2009, 29:11263-11270.
77. Davies C.H., Starkey S.J., Pozza M.F., Collingridge G.L. GABA autoreceptors regulate the induction of LTP. Nature 1991, 349:609-611.
78. Dean C., Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci. 2006, 29:21-29.
79. Dean C., Scholl F.G., Choih J., DeMaria S., Berger J., Isacoff E., Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 2003, 6:708-716.
80. Dowell J.A., Johnson J.A., Li L. Identification of astrocyte secreted proteins with a combination of shotgun proteomics and bioinformatics. J. Proteome Res. 2009, 8:4135-4143.
81. Dumitriu D., Cossart R., Huang J., Yuste R. Correlation between axonal morphologies and synaptic input kinetics of interneurons from mouse visual cortex. Cereb. Cortex 2007, 17:81-91.
82. Durand C.M., Betancur C., Boeckers T.M., Bockmann J., Chaste P., Fauchereau F., Nygren G., Rastam M., Gillberg I.C., Anckarsater H., et al. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet. 2007, 39:25-27.
83. Durand G.M., Konnerth A. Long-term potentiation as a mechanism of functional synapse induction in the developing hippocampus. J. Physiol. Paris 1996, 90:313-315.
84. Durand G.M., Kovalchuk Y., Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 1996, 381:71-75.
85. Dutar P., Nicoll R.A. A physiological role for GABAB receptors in the central nervous system. Nature 1988, 332:156-158.
86. Dzhala V.I., Talos D.M., Sdrulla D.A., Brumback A.C., Mathews G.C., Benke T.A., Delpire E., Jensen F.E., Staley K.J. NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 2005, 11:1205-1213.
87. Elmariah S.B., Crumling M.A., Parsons T.D., Balice-Gordon R.J. Postsynaptic TrkB-mediated signaling modulates excitatory and inhibitory neurotransmitter receptor clustering at hippocampal synapses. J. Neurosci. 2004, 24:2380-2393.
88. Elmariah S.B., Oh E.J., Hughes E.G., Balice-Gordon R.J. Astrocytes regulate inhibitory synapse formation via Trk-mediated modulation of postsynaptic GABAA receptors. J. Neurosci. 2005, 25:3638-3650.
89. Ernfors P., Lee K.F., Jaenisch R. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 1994, 368:147-150.
90. Essrich C., Lorez M., Benson J.A., Fritschy J.M., Luscher B. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat. Neurosci. 1998, 1:563-571.
91. Faissner A., Pyka M., Geissler M., Sobik T., Frischknecht R., Gundelfinger E.D., Seidenbecher C. Contributions of astrocytes to synapse formation and maturation - potential functions of the perisynaptic extracellular matrix. Brain Res. Rev. 2010, 63:26-38.
92. Farrar S.J., Whiting P.J., Bonnert T.P., McKernan R.M. Stoichiometry of a ligand-gated ion channel determined by fluorescence energy transfer. J. Biol. Chem. 1999, 274:10100-10104.
93. Fazzari P., Paternain A.V., Valiente M., Pla R., Lujan R., Lloyd K., Lerma J., Marin O., Rico B. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010, 464:1376-1380.
94. Feng G., Tintrup H., Kirsch J., Nichol M.C., Kuhse J., Betz H., Sanes J.R. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 1998, 282:1321-1324.
95. Fernandez F., Garner C.C. Over-inhibition: a model for developmental intellectual disability. Trends Neurosci. 2007, 30:497-503.
96. Fischer F., Kneussel M., Tintrup H., Haverkamp S., Rauen T., Betz H., Wassle H. Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. J. Comp. Neurol. 2000, 427:634-648.
97. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
98. Friedman H.V., Bresler T., Garner C.C., Ziv N.E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 2000, 27:57-69.
99. Fritschy J.M., Brunig I. Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol. Ther. 2003, 98:299-323.
100. Fritschy J.M., Harvey R.J., Schwarz G. Gephyrin: where do we stand, where do we go?. Trends Neurosci. 2008, 31:257-264.
101. Fritschy J.M., Panzanelli P., Kralic J.E., Vogt K.E., Sassoe-Pognetto M. Differential dependence of axo-dendritic and axo-somatic GABAergic synapses on GABAA receptors containing the alpha1 subunit in Purkinje cells. J. Neurosci. 2006, 26:3245-3255.
102. Frotscher M., Zhao S., Graber W., Drakew A., Studer D. New ways of looking at synapses. Histochem. Cell Biol. 2007, 128:91-96.
103. + current in voltage-clamped CA3 pyramidal cells in hippocampal cultures. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:1558-1562.
104. Galvan A., Charara A., Pare J.F., Levey A.I., Smith Y. Differential subcellular and subsynaptic distribution of GABA(A) and GABA(B) receptors in the monkey subthalamic nucleus. Neuroscience 2004, 127:709-721.
105. Ganguly K., Schinder A.F., Wong S.T., Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 2001, 105:521-532.
106. Garcia R.A., Vasudevan K., Buonanno A. The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:3596-3601.
107. Gerrow K., Romorini S., Nabi S.M., Colicos M.A., Sala C., El-Husseini A. A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 2006, 49:547-562.
108. Ghiretti A.E., Paradis S. The GTPase Rem2 regulates synapse development and dendritic morphology. Dev. Neurobiol. 2011, 71:374-389.
109. Gilman S.R., Iossifov I., Levy D., Ronemus M., Wigler M., Vitkup D. Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Neuron 2011, 70:898-907.
110. Godenschwege T.A., Hu H., Shan-Crofts X., Goodman C.S., Murphey R.K. Bi-directional signaling by Semaphorin 1a during central synapse formation in Drosophila. Nat. Neurosci. 2002, 5:1294-1301.
111. Gottmann K., Mittmann T., Lessmann V. BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp. Brain Res. 2009, 199:203-234.
112. Gozlan H., Ben-Ari Y. Interneurons are the source and the targets of the first synapses formed in the rat developing hippocampal circuit. Cereb. Cortex 2003, 13:684-692.
113. Graf E.R., Kang Y., Hauner A.M., Craig A.M. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J. Neurosci. 2006, 26:4256-4265.
114. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 2004, 119:1013-1026.
115. Gray E.G. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J. Anat. 1959, 93:420-433.
116. Greenberg M.E., Xu B., Lu B., Hempstead B.L. New insights in the biology of BDNF synthesis and release: implications in CNS function. J. Neurosci. 2009, 29:12764-12767.
117. Gulyas A.I., Hajos N., Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci. 1996, 16:3397-3411.
118. Gunther U., Benson J., Benke D., Fritschy J.M., Reyes G., Knoflach F., Crestani F., Aguzzi A., Arigoni M., Lang Y., et al. Benzodiazepine-insensitive mice generated by targeted disruption of the gamma 2 subunit gene of gamma-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:7749-7753.
119. Guy J., Hendrich B., Holmes M., Martin J.E., Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 2001, 27:322-326.
120. Harms K.J., Craig A.M. Synapse composition and organization following chronic activity blockade in cultured hippocampal neurons. J. Comp. Neurol. 2005, 490:72-84.
121. Harvey K., Duguid I.C., Alldred M.J., Beatty S.E., Ward H., Keep N.H., Lingenfelter S.E., Pearce B.R., Lundgren J., Owen M.J., et al. The GDP-GTP exchange factor collybistin: an essential determinant of neuronal gephyrin clustering. J. Neurosci. 2004, 24:5816-5826.
122. Hayashi M.K., Tang C., Verpelli C., Narayanan R., Stearns M.H., Xu R.M., Li H., Sala C., Hayashi Y. The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 2009, 137:159-171.
123. Haydon P.G., Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol. Rev. 2006, 86:1009-1031.
124. Hennou S., Khalilov I., Diabira D., Ben-Ari Y., Gozlan H. Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur. J. Neurosci. 2002, 16:197-208.
125. Hoffman E.P., Brown R.H., Kunkel L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987, 51:919-928.
126. Holmgren C.D., Mukhtarov M., Malkov A.E., Popova I.Y., Bregestovski P., Zilberter Y. Energy substrate availability as a determinant of neuronal resting potential, GABA signaling and spontaneous network activity in the neonatal cortex in vitro. J. Neurochem. 2010, 112:900-912.
127. Hong E.J., McCord A.E., Greenberg M.E. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 2008, 60:610-624.
128. Hong E.J., West A.E., Greenberg M.E. Transcriptional control of cognitive development. Curr. Opin. Neurobiol. 2005, 15:21-28.
129. Hong Q., Zhang M., Pan X.Q., Guo M., Li F., Tong M.L., Chen R.H., Guo X.R., Chi X. Prefrontal cortex Homer expression in an animal model of attention-deficit/hyperactivity disorder. J. Neurol. Sci. 2009, 287:205-211.
130. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 2001, 24:677-736.
131. Huang Y.Z., Won S., Ali D.W., Wang Q., Tanowitz M., Du Q.S., Pelkey K.A., Yang D.J., Xiong W.C., Salter M.W., et al. Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 2000, 26:443-455.
132. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
133. Huang Z.J., Scheiffele P. GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development. Curr. Opin. Neurobiol. 2008, 18:77-83.
134. 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.
135. Hughes E.G., Elmariah S.B., Balice-Gordon R.J. Astrocyte secreted proteins selectively increase hippocampal GABAergic axon length, branching, and synaptogenesis. Mol. Cell. Neurosci. 2010, 43:136-145.
136. Hutsler J.J., Zhang H. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res. 2010, 1309:83-94.
137. - concentrations in rat hippocampal neurons. Neurosci. Lett. 1991, 134:75-78.
138. Isomoto S., Kaibara M., Sakurai-Yamashita Y., Nagayama Y., Uezono Y., Yano K., Taniyama K. Cloning and tissue distribution of novel splice variants of the rat GABAB receptor. Biochem. Biophys. Res. Commun. 1998, 253:10-15.
139. Jacob T.C., Bogdanov Y.D., Magnus C., Saliba R.S., Kittler J.T., Haydon P.G., Moss S.J. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J. Neurosci. 2005, 25:10469-10478.
140. Jacob T.C., Moss S.J., Jurd R. GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 2008, 9:331-343.
141. Jacob T.C., Wan Q., Vithlani M., Saliba R.S., Succol F., Pangalos M.N., Moss S.J. GABA(A) receptor membrane trafficking regulates spine maturity. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:12500-12505.
142. Jamain S., Quach H., Betancur C., Rastam M., Colineaux C., Gillberg I.C., Soderstrom H., Giros B., Leboyer M., Gillberg C., et al. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 2003, 34:27-29.
143. Jeon H., Lee S., Lee W.H., Suk K. Analysis of glial secretome: the long pentraxin PTX3 modulates phagocytic activity of microglia. J. Neuroimmunol. 2010, 229:63-72.
144. Jones K.R., Farinas I., Backus C., Reichardt L.F. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 1994, 76:989-999.
145. Kalscheuer V.M., Musante L., Fang C., Hoffmann K., Fuchs C., Carta E., Deas E., Venkateswarlu K., Menzel C., Ullmann R., et al. A balanced chromosomal translocation disrupting ARHGEF9 is associated with epilepsy, anxiety, aggression, and mental retardation. Hum. Mutat. 2009, 30:61-68.
146. Kandel E.R., Spencer W.A., Brinley J.R. Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J. Neurophysiol. 1961, 24:225-242.
147. Kantamneni S., Correa S.A., Hodgkinson G.K., Meyer G., Vinh N.N., Henley J.M., Nishimune A. GISP: a novel brain-specific protein that promotes surface expression and function of GABA(B) receptors. J. Neurochem. 2007, 100:1003-1017.
148. Kasai H., Matsuzaki M., Noguchi J., Yasumatsu N., Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 2003, 26:360-368.
149. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
150. Kaupmann K., Huggel K., Heid J., Flor P.J., Bischoff S., Mickel S.J., McMaster G., Angst C., Bittiger H., Froestl W., et al. Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature 1997, 386:239-246.
151. Khakhalin A.S. Questioning the depolarizing effects of GABA during early brain development. J. Neurophysiol. 2011, (May, 18) doi:10.1152/jn.00293.2011.
152. Khazipov R., Khalilov I., Tyzio R., Morozova E., Ben-Ari Y., Holmes G.L. Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur. J. Neurosci. 2004, 19:590-600.
153. Kim E., Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 2004, 5:771-781.
154. Kins S., Betz H., Kirsch J. Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nat. Neurosci. 2000, 3:22-29.
155. Kishi N., Macklis J.D. MECP2 is progressively expressed in post-migratory neurons and is involved in neuronal maturation rather than cell fate decisions. Mol. Cell. Neurosci. 2004, 27:306-321.
156. Kneussel M., Brandstatter J.H., Gasnier B., Feng G., Sanes J.R., Betz H. Gephyrin-independent clustering of postsynaptic GABA(A) receptor subtypes. Mol. Cell. Neurosci. 2001, 17:973-982.
157. Kneussel M., Brandstatter J.H., Laube B., Stahl S., Muller U., Betz H. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J. Neurosci. 1999, 19:9289-9297.
158. Knuesel I., Mastrocola M., Zuellig R.A., Bornhauser B., Schaub M.C., Fritschy J.M. Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur. J. Neurosci. 1999, 11:4457-4462.
159. Kohara K., Yasuda H., Huang Y., Adachi N., Sohya K., Tsumoto T. A local reduction in cortical GABAergic synapses after a loss of endogenous brain-derived neurotrophic factor, as revealed by single-cell gene knock-out method. J. Neurosci. 2007, 27:7234-7244.
160. Kokaia Z., Bengzon J., Metsis M., Kokaia M., Persson H., Lindvall O. Coexpression of neurotrophins and their receptors in neurons of the central nervous system. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:6711-6715.
161. Koller H., Siebler M., Schmalenbach C., Muller H.W. GABA and glutamate receptor development of cultured neurons from rat hippocampus, septal region, and neocortex. Synapse 1990, 5:59-64.
162. Kralic J.E., Sidler C., Parpan F., Homanics G.E., Morrow A.L., Fritschy J.M. Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J. Comp. Neurol. 2006, 495:408-421.
163. Kruger R.P., Aurandt J., Guan K.L. Semaphorins command cells to move. Nat. Rev. Mol. Cell Biol. 2005, 6:789-800.
164. Kulik A., Vida I., Lujan R., Haas C.A., Lopez-Bendito G., Shigemoto R., Frotscher M. Subcellular localization of metabotropic GABA(B) receptor subunits GABA(B1a/b) and GABA(B2) in the rat hippocampus. J. Neurosci. 2003, 23:11026-11035.
165. Lardi-Studler B., Fritschy J.M. Matching of pre- and postsynaptic specializations during synaptogenesis. Neuroscientist 2007, 13:115-126.
166. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
167. Levi S., Logan S.M., Tovar K.R., Craig A.M. Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J. Neurosci. 2004, 24:207-217.
168. Levy D., Ronemus M., Yamrom B., Lee Y.H., Leotta A., Kendall J., Marks S., Lakshmi B., Pai D., Ye K., et al. Rare de novo and transmitted copy-number variation in autistic spectrum disorders. Neuron 2011, 70:886-897.
169. Li B., Woo R.S., Mei L., Malinow R. The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 2007, 54:583-597.
170. Lin X., Ogiya M., Takahara M., Yamaguchi W., Furuyama T., Tanaka H., Tohyama M., Inagaki S. Sema4D-plexin-B1 implicated in regulation of dendritic spine density through RhoA/ROCK pathway. Neurosci. Lett. 2007, 428:1-6.
171. Lin Y., Bloodgood B.L., Hauser J.L., Lapan A.D., Koon A.C., Kim T.K., Hu L.S., Malik A.N., Greenberg M.E. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 2008, 455:1198-1204.
172. Liu Q.Y., Schaffner A.E., Chang Y.H., Vaszil K., Barker J.L. Astrocytes regulate amino acid receptor current densities in embryonic rat hippocampal neurons. J. Neurobiol. 1997, 33:848-864.
173. Liu Q.Y., Schaffner A.E., Li Y.X., Dunlap V., Barker J.L. Upregulation of GABAA current by astrocytes in cultured embryonic rat hippocampal neurons. J. Neurosci. 1996, 16:2912-2923.
174. Lohmann C., Bonhoeffer T. A role for local calcium signaling in rapid synaptic partner selection by dendritic filopodia. Neuron 2008, 59:253-260.
175. Lord C., Cook E.H., Leventhal B.L., Amaral D.G. Autism spectrum disorders. Neuron 2000, 28:355-363.
176. Luscher B., Fuchs T., Kilpatrick C.L. GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 2011, 70:385-409.
177. Magdaleno S., Jensen P., Brumwell C.L., Seal A., Lehman K., Asbury A., Cheung T., Cornelius T., Batten D.M., Eden C., et al. BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol. 2006, 4:e86.
178. Marshall C.R., Noor A., Vincent J.B., Lionel A.C., Feuk L., Skaug J., Shago M., Moessner R., Pinto D., Ren Y., et al. Structural variation of chromosomes in autism spectrum disorder. Am. J. Hum. Genet. 2008, 82:477-488.
179. Marty S., Wehrle R., Sotelo C. Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J. Neurosci. 2000, 20:8087-8095.
180. McAllister A.K. Dynamic aspects of CNS synapse formation. Annu. Rev. Neurosci. 2007, 30:425-450.
181. McGraw C.M., Samaco R.C., Zoghbi H.Y. Adult Neural Function Requires MeCP2 2011, Science.
182. McNair K., Spike R., Guilding C., Prendergast G.C., Stone T.W., Cobb S.R., Morris B.J. A role for RhoB in synaptic plasticity and the regulation of neuronal morphology. J. Neurosci. 2010, 30:3508-3517.
183. Mei L., Xiong W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 2008, 9:437-452.
184. Melin M., Carlsson B., Anckarsater H., Rastam M., Betancur C., Isaksson A., Gillberg C., Dahl N. Constitutional downregulation of SEMA5A expression in autism. Neuropsychobiology 2006, 54:64-69.
185. Meyer G., Kirsch J., Betz H., Langosch D. Identification of a gephyrin binding motif on the glycine receptor beta subunit. Neuron 1995, 15:563-572.
186. Micheva K.D., Beaulieu C. An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:11834-11838.
187. Micheva K.D., Busse B., Weiler N.C., O'Rourke N., Smith S.J. Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 2010, 68:639-653.
188. Miles R., Wong R.K. Unitary inhibitory synaptic potentials in the guinea-pig hippocampus in vitro. J. Physiol. 1984, 356:97-113.
189. Miles R., Wong R.K. Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J. Physiol. 1987, 388:611-629.
190. Miranda R.C., Sohrabji F., Toran-Allerand C.D. Neuronal colocalization of mRNAs for neurotrophins and their receptors in the developing central nervous system suggests a potential for autocrine interactions. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:6439-6443.
191. 2+ channels to synaptic vesicle exocytosis. Nature 2003, 423:939-948.
192. Moessner R., Marshall C.R., Sutcliffe J.S., Skaug J., Pinto D., Vincent J., Zwaigenbaum L., Fernandez B., Roberts W., Szatmari P., et al. Contribution of SHANK3 mutations to autism spectrum disorder. Am. J. Hum. Genet. 2007, 81:1289-1297.
193. Morita A., Yamashita N., Sasaki Y., Uchida Y., Nakajima O., Nakamura F., Yagi T., Taniguchi M., Usui H., Katoh-Semba R., et al. Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J. Neurosci. 2006, 26:2971-2980.
194. Moulder K.L., Jiang X., Taylor A.A., Shin W., Gillis K.D., Mennerick S. Vesicle pool heterogeneity at hippocampal glutamate and GABA synapses. J. Neurosci. 2007, 27:9846-9854.
195. Murphey R.K., Froggett S.J., Caruccio P., Shan-Crofts X., Kitamoto T., Godenschwege T.A. Targeted expression of shibire ts and semaphorin 1a reveals critical periods for synapse formation in the giant fiber of Drosophila. Development 2003, 130:3671-3682.
196. Nagler K., Mauch D.H., Pfrieger F.W. Glia-derived signals induce synapse formation in neurones of the rat central nervous system. J. Physiol. 2001, 533:665-679.
197. Nicoll R.A., Malenka R.C., Kauer J.A. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev. 1990, 70:513-565.
198. Noh J., Seal R.P., Garver J.A., Edwards R.H., Kandler K. Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map. Nat. Neurosci. 2010, 13:232-238.
199. Noutel J., Hong Y.K., Leu B., Kang E., Chen C. Experience-dependent retinogeniculate synapse remodeling is abnormal in MeCP2-deficient mice. Neuron 2011, 70:35-42.
200. Nusser Z., Sieghart W., Benke D., Fritschy J.M., Somogyi P. Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:11939-11944.
201. Nusser Z., Sieghart W., Somogyi P. Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 1998, 18:1693-1703.
202. O'Connor T.P., Cockburn K., Wang W., Tapia L., Currie E., Bamji S.X. Semaphorin 5B mediates synapse elimination in hippocampal neurons. Neural. Dev. 2009, 4:18.
203. O'Sullivan G.A., Hofer W., Betz H. Inhibitory postsynaptic membrane specializations are formed in gephyrin-deficient mice. Neurosci. Lett. 2009, 458:106-110.
204. Papadopoulos T., Eulenburg V., Reddy-Alla S., Mansuy I.M., Li Y., Betz H. Collybistin is required for both the formation and maintenance of GABAergic postsynapses in the hippocampus. Mol. Cell. Neurosci. 2008, 39:161-169.
205. Papadopoulos T., Korte M., Eulenburg V., Kubota H., Retiounskaia M., Harvey R.J., Harvey K., O'Sullivan G.A., Laube B., Hulsmann S., et al. Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin-deficient mice. EMBO J. 2007, 26:3888-3899.
206. Paradis S., Harrar D.B., Lin Y., Koon A.C., Hauser J.L., Griffith E.C., Zhu L., Brass L.F., Chen C., Greenberg M.E. An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 2007, 53:217-232.
207. Parra P., Gulyas A.I., Miles R. How many subtypes of inhibitory cells in the hippocampus?. Neuron 1998, 20:983-993.
208. Pecho-Vrieseling E., Sigrist M., Yoshida Y., Jessell T.M., Arber S. Specificity of sensory-motor connections encoded by Sema3e-Plxnd1 recognition. Nature 2009, 459:842-846.
209. Percy A.K., Lane J.B. Rett syndrome: model of neurodevelopmental disorders. J. Child Neurol. 2005, 20:718-721.
210. Peters A., Harriman K.M. Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. I. Morphometric analysis. J. Neurocytol. 1990, 19:154-174.
211. Peters A., Palay S.L. The morphology of synapses. J. Neurocytol. 1996, 25:687-700.
212. Pfaff T., Malitschek B., Kaupmann K., Prezeau L., Pin J.P., Bettler B., Karschin A. Alternative splicing generates a novel isoform of the rat metabotropic GABA(B)R1 receptor. Eur. J. Neurosci. 1999, 11:2874-2882.
213. Pfeiffer F., Graham D., Betz H. Purification by affinity chromatography of the glycine receptor of rat spinal cord. J. Biol. Chem. 1982, 257:9389-9393.
214. Pfrieger F.W., Barres B.A. Synaptic efficacy enhanced by glial cells in vitro. Science 1997, 277:1684-1687.
215. Pilgram G.S., Potikanond S., Baines R.A., Fradkin L.G., Noordermeer J.N. The roles of the dystrophin-associated glycoprotein complex at the synapse. Mol. Neurobiol. 2010, 41:1-21.
216. Pinto D., Pagnamenta A.T., Klei L., Anney R., Merico D., Regan R., Conroy J., Magalhaes T.R., Correia C., Abrahams B.S., et al. Functional impact of global rare copy number variation in autism spectrum disorders. Nature 2010, 466:368-372.
217. Poulopoulos A., Aramuni G., Meyer G., Soykan T., Hoon M., Papadopoulos T., Zhang M., Paarmann I., Fuchs C., Harvey K., et al. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 2009, 63:628-642.
218. Prange O., Murphy T.H. Modular transport of postsynaptic density-95 clusters and association with stable spine precursors during early development of cortical neurons. J. Neurosci. 2001, 21:9325-9333.
219. 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.
220. Rao A., Cha E.M., Craig A.M. Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J. Neurosci. 2000, 20:8344-8353.
221. Rheims S., Holmgren C.D., Chazal G., Mulder J., Harkany T., Zilberter T., Zilberter Y. GABA action in immature neocortical neurons directly depends on the availability of ketone bodies. J. Neurochem. 2009, 110:1330-1338.
222. Richter K., Langnaese K., Kreutz M.R., Olias G., Zhai R., Scheich H., Garner C.C., Gundelfinger E.D. Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. J. Comp. Neurol. 1999, 408:437-448.
223. Rico B., Xu B., Reichardt L.F. TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat. Neurosci. 2002, 5:225-233.
224. Riddle D.R., McAllister A.K., Lo D.C., Katz L.C. Neurotrophins in cortical development. Cold Spring Harb. Symp. Quant. Biol. 1996, 61:85-93.
225. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999, 397:251-255.
226. Robinson T.E., Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 2004, 47(Suppl. 1):33-46.
227. Rostaing P., Real E., Siksou L., Lechaire J.P., Boudier T., Boeckers T.M., Gertler F., Gundelfinger E.D., Triller A., Marty S. Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography. Eur. J. Neurosci. 2006, 24:3463-3474.
228. Rubenstein J.L., Merzenich M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003, 2:255-267.
229. Russo S.J., Mazei-Robison M.S., Ables J.L., Nestler E.J. Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 2009, 56:73-82.
230. Sabo S.L., Gomes R.A., McAllister A.K. Formation of presynaptic terminals at predefined sites along axons. J. Neurosci. 2006, 26:10813-10825.
231. Saiepour L., Fuchs C., Patrizi A., Sassoe-Pognetto M., Harvey R.J., Harvey K. Complex role of collybistin and gephyrin in GABAA receptor clustering. J. Biol. Chem. 2010, 285:29623-29631.
232. Sala C., Piech V., Wilson N.R., Passafaro M., Liu G., Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 2001, 31:115-130.
233. Sanders S.J., Ercan-Sencicek A.G., Hus V., Luo R., Murtha M.T., Moreno-De-Luca D., Chu S.H., Moreau M.P., Gupta A.R., Thomson S.A., et al. Multiple recurrent de novo CNVs, including duplications of the 7q11.23 williams syndrome region, are strongly associated with autism. Neuron 2011, 70:863-885.
234. Sanmarti-Vila L., tom Dieck S., Richter K., Altrock W., Zhang L., Volknandt W., Zimmermann H., Garner C.C., Gundelfinger E.D., Dresbach T. Membrane association of presynaptic cytomatrix protein bassoon. Biochem. Biophys. Res. Commun. 2000, 275:43-46.
235. Sassoe-Pognetto M., Kirsch J., Grunert U., Greferath U., Fritschy J.M., Mohler H., Betz H., Wassle H. Colocalization of gephyrin and GABAA-receptor subunits in the rat retina. J. Comp. Neurol. 1995, 357:1-14.
236. Scanziani M. GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 2000, 25:673-681.
237. Scheiffele P. Cell-cell signaling during synapse formation in the CNS. Annu. Rev. Neurosci. 2003, 26:485-508.
238. Scheiffele P., Fan J., Choih J., Fetter R., Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 2000, 101:657-669.
239. Schumann C.M., Hamstra J., Goodlin-Jones B.L., Lotspeich L.J., Kwon H., Buonocore M.H., Lammers C.R., Reiss A.L., Amaral D.G. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J. Neurosci. 2004, 24:6392-6401.
240. Schwarz D.A., Barry G., Eliasof S.D., Petroski R.E., Conlon P.J., Maki R.A. Characterization of gamma-aminobutyric acid receptor GABAB(1e), a GABAB(1) splice variant encoding a truncated receptor. J. Biol. Chem. 2000, 275:32174-32181.
241. Sekiguchi M., Zushida K., Yoshida M., Maekawa M., Kamichi S., Sahara Y., Yuasa S., Takeda S., Wada K. A deficit of brain dystrophin impairs specific amygdala GABAergic transmission and enhances defensive behaviour in mice. Brain 2009, 132:124-135.
242. Shapira M., Zhai R.G., Dresbach T., Bresler T., Torres V.I., Gundelfinger E.D., Ziv N.E., Garner C.C. Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 2003, 38:237-252.
243. Siksou L., Rostaing P., Lechaire J.P., Boudier T., Ohtsuka T., Fejtova A., Kao H.T., Greengard P., Gundelfinger E.D., Triller A., et al. Three-dimensional architecture of presynaptic terminal cytomatrix. J. Neurosci. 2007, 27:6868-6877.
244. Siksou L., Triller A., Marty S. An emerging view of presynaptic structure from electron microscopic studies. J. Neurochem. 2009, 108:1336-1342.
245. Slezak M., Pfrieger F.W. New roles for astrocytes: regulation of CNS synaptogenesis. Trends Neurosci. 2003, 26:531-535.
246. Soghomonian J.J., Martin D.L. Two isoforms of glutamate decarboxylase: why?. Trends Pharmacol. Sci. 1998, 19:500-505.
247. Somogyi J., Baude A., Omori Y., Shimizu H., El Mestikawy S., Fukaya M., Shigemoto R., Watanabe M., Somogyi P. GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat. Eur. J. Neurosci. 2004, 19:552-569.
248. Song J.Y., Ichtchenko K., Sudhof T.C., Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:1100-1105.
249. Studer R., von Boehmer L., Haenggi T., Schweizer C., Benke D., Rudolph U., Fritschy J.M. Alteration of GABAergic synapses and gephyrin clusters in the thalamic reticular nucleus of GABAA receptor alpha3 subunit-null mice. Eur. J. Neurosci. 2006, 24:1307-1315.
250. Studler B., Fritschy J.M., Brunig I. GABAergic and glutamatergic terminals differentially influence the organization of GABAergic synapses in rat cerebellar granule cells in vitro. Neuroscience 2002, 114:123-133.
251. Swiercz J.M., Kuner R., Behrens J., Offermanns S. Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 2002, 35:51-63.
252. Szatmari P., Paterson A.D., Zwaigenbaum L., Roberts W., Brian J., Liu X.Q., Vincent J.B., Skaug J.L., Thompson A.P., Senman L., et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat. Genet. 2007, 39:319-328.
253. Tabuchi K., Blundell J., Etherton M.R., Hammer R.E., Liu X., Powell C.M., Sudhof T.C. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 2007, 318:71-76.
254. - transport. Eur. J. Pharmacol. 1996, 297:137-143.
255. Tamagnone L., Artigiani S., Chen H., He Z., Ming G.I., Song H., Chedotal A., Winberg M.L., Goodman C.S., Poo M., et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 1999, 99:71-80.
256. Tashiro A., Minden A., Yuste R. Regulation of dendritic spine morphology by the rho family of small GTPases: antagonistic roles of Rac and Rho. Cereb. Cortex 2000, 10:927-938.
257. Tate P., Skarnes W., Bird A. The methyl-CpG binding protein MeCP2 is essential for embryonic development in the mouse. Nat. Genet. 1996, 12:205-208.
258. Terauchi A., Johnson-Venkatesh E.M., Toth A.B., Javed D., Sutton M.A., Umemori H. Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 2010, 465:783-787.
259. Thompson S.M., Gahwiler B.H. Comparison of the actions of baclofen at pre- and postsynaptic receptors in the rat hippocampus in vitro. J. Physiol. 1992, 451:329-345.
260. Tran T.S., Rubio M.E., Clem R.L., Johnson D., Case L., Tessier-Lavigne M., Huganir R.L., Ginty D.D., Kolodkin A.L. Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature 2009, 462:1065-1069.
261. Tretter V., Jacob T.C., Mukherjee J., Fritschy J.M., Pangalos M.N., Moss S.J. The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha 2 subunits to gephyrin. J. Neurosci. 2008, 28:1356-1365.
262. Tretter V., Moss S.J. GABA(A) receptor dynamics and constructing GABAergic synapses. Front. Mol. Neurosci. 2008, 1:7.
263. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. 1996, 16:877-885.
264. Tsay D., Yuste R. On the electrical function of dendritic spines. Trends Neurosci. 2004, 27:77-83.
265. Turner N., Grose R. Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 2010, 10:116-129.
266. Twelvetrees A.E., Yuen E.Y., Arancibia-Carcamo I.L., MacAskill A.F., Rostaing P., Lumb M.J., Humbert S., Triller A., Saudou F., Yan Z., et al. Delivery of GABAARs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin. Neuron 2010, 65:53-65.
267. Tyzio R., Allene C., Nardou R., Picardo M.A., Yamamoto S., Sivakumaran S., Caiati M.D., Rheims S., Minlebaev M., Milh M., et al. Depolarizing actions of GABA in immature neurons depend neither on ketone bodies nor on pyruvate. J. Neurosci. 2011, 31:34-45.
268. Tyzio R., Minlebaev M., Rheims S., Ivanov A., Jorquera I., Holmes G.L., Zilberter Y., Ben-Ari Y., Khazipov R. Postnatal changes in somatic gamma-aminobutyric acid signalling in the rat hippocampus. Eur. J. Neurosci. 2008, 27:2515-2528.
269. Tyzio R., Represa A., Jorquera I., Ben-Ari Y., Gozlan H., Aniksztejn L. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci. 1999, 19:10372-10382.
270. Ullian E.M., Christopherson K.S., Barres B.A. Role for glia in synaptogenesis. Glia 2004, 47:209-216.
271. Ullian E.M., Sapperstein S.K., Christopherson K.S., Barres B.A. Control of synapse number by glia. Science 2001, 291:657-661.
272. Umemori H., Linhoff M.W., Ornitz D.M., Sanes J.R. FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 2004, 118:257-270.
273. van Spronsen M., Hoogenraad C.C. Synapse pathology in psychiatric and neurologic disease. Curr. Neurol. Neurosci. Rep. 2010, 10:207-214.
274. Varoqueaux F., Aramuni G., Rawson R.L., Mohrmann R., Missler M., Gottmann K., Zhang W., Sudhof T.C., Brose N. Neuroligins determine synapse maturation and function. Neuron 2006, 51:741-754.
275. Varoqueaux F., Jamain S., Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 2004, 83:449-456.
276. Varaqueaux R., Sigler A., Rhee J.S., Brose N., Enk C., Reim K., Rosenmund C. Total arrest of spontaneous and evoked synaptic transmission by normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. U.S.A. 2002, 99:9037-9042.
277. Vashlishan A.B., Madison J.M., Dybbs M., Bai J., Sieburth D., Ch'ng Q., Tavazoie M., Kaplan J.M. An RNAi screen identifies genes that regulate GABA synapses. Neuron 2008, 58:346-361.
278. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000, 287:864-869.
279. Vigot R., Barbieri S., Brauner-Osborne H., Turecek R., Shigemoto R., Zhang Y.P., Lujan R., Jacobson L.H., Biermann B., Fritschy J.M., et al. Differential compartmentalization and distinct functions of GABAB receptor variants. Neuron 2006, 50:589-601.
280. Vullhorst D., Neddens J., Karavanova I., Tricoire L., Petralia R.S., McBain C.J., Buonanno A. Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J. Neurosci. 2009, 29:12255-12264.
281. Walton M.K., Schaffner A.E., Barker J.L. Sodium channels, GABAA receptors, and glutamate receptors develop sequentially on embryonic rat spinal cord cells. J. Neurosci. 1993, 13:2068-2084.
282. Wang C., Shimizu-Okabe C., Watanabe K., Okabe A., Matsuzaki H., Ogawa T., Mori N., Fukuda A., Sato K. Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res. Develop. Brain Res. 2002, 139:59-66.
283. Wang D.D., Kriegstein A.R. GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J. Neurosci. 2008, 28:5547-5558.
284. Washbourne P., Bennett J.E., McAllister A.K. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat. Neurosci. 2002, 5:751-759.
285. Washbourne P., Liu X.B., Jones E.G., McAllister A.K. Cycling of NMDA receptors during trafficking in neurons before synapse formation. J. Neurosci. 2004, 24:8253-8264.
286. Weiss L.A., Arking D.E., Daly M.J., Chakravarti A. A genome-wide linkage and association scan reveals novel loci for autism. Nature 2009, 461:802-808.
287. Wen L., Lu Y.S., Zhu X.H., Li X.M., Woo R.S., Chen Y.J., Yin D.M., Lai C., Terry A.V., Vazdarjanova A., et al. Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1211-1216.
288. Wierenga C.J., Becker N., Bonhoeffer T. GABAergic synapses are formed without the involvement of dendritic protrusions. Nat. Neurosci. 2008, 11:1044-1052.
289. Woo R.S., Li X.M., Tao Y., Carpenter-Hyland E., Huang Y.Z., Weber J., Neiswender H., Dong X.P., Wu J., Gassmann M., et al. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 2007, 54:599-610.
290. Wu G., Malinow R., Cline H.T. Maturation of a central glutamatergic synapse. Science 1996, 274:972-976.
291. Xu J., Wojcik W.J. Gamma aminobutyric acid B receptor-mediated inhibition of adenylate cyclase in cultured cerebellar granule cells: blockade by islet-activating protein. J. Pharmacol. Exp. Ther. 1986, 239:568-573.
292. Yazdani U., Terman J.R. The semaphorins. Genome Biol. 2006, 7:211.
293. Yoshii A., Constantine-Paton M. Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev. Neurobiol. 2010, 70:304-322.
294. Zakharenko S., Chang S., O'Donoghue M., Popov S.V. Neurotransmitter secretion along growing nerve processes: comparison with synaptic vesicle exocytosis. J. Cell Biol. 1999, 144:507-518.
295. Zander J.F., Munster-Wandowski A., Brunk I., Pahner I., Gomez-Lira G., Heinemann U., Gutierrez R., Laube G., Ahnert-Hilger G. Synaptic and vesicular coexistence of VGLUT and VGAT in selected excitatory and inhibitory synapses. J. Neurosci. 2010, 30:7634-7645.
296. Zhai R.G., Vardinon-Friedman H., Cases-Langhoff C., Becker B., Gundelfinger E.D., Ziv N.E., Garner C.C. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 2001, 29:131-143.
297. Zhang C., Atasoy D., Arac D., Yang X., Fucillo M.V., Robison A.J., Ko J., Brunger A.T., Sudhof T.C. Neurexins physically and functionally interact with GABA(A) receptors. Neuron 2010, 66:403-416.
298. Zhang Z.W., Zak J.D., Liu H. MeCP2 is required for normal development of GABAergic circuits in the thalamus. J. Neurophysiol. 2010, 103:2470-2481.
299. Zilberter Y., Zilberter T., Bregestovski P. Neuronal activity in vitro and the in vivo reality: the role of energy homeostasis. Trends Pharmacol. Sci. 2010, 31:394-401.
300. Zoghbi H.Y. Postnatal neurodevelopmental disorders: meeting at the synapse?. Science 2003, 302:826-830.