Neurexins and neuroligins: new partners for GABAA receptors at synapses
Received date: 15 Oct 2010
Accepted date: 10 Nov 2010
Published date: 01 Jun 2011
Copyright
Gamma-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in the brain. As one of several types of endogenous receptors, GABAA receptors have been shown to be essential in most, if not all, aspects of brain functioning, including neural development and information processing. Mutations in genes encoding GABAA receptors and alterations in the function of GABAA receptors are associated with many neurologic diseases, and GABAA receptors have been clinically targeted by many drugs, such as benzodiazepines and general anesthetics. Extensive studies have revealed a number of intracellular chaperons/interactions for GABAA receptors, providing a protein–protein network in regulating the trafficking and location of GABAA receptors in the brain. Recently, neurexins and neuroligins, two families of transmembrane proteins present at neurological synapses, are implicated as new partners to GABAA receptors. These works shed new light on the synaptic regulation of GABAA receptor activity. Here, we summarized the proteins that were implicated in the function of GABAA receptors, including neurexins and neuroligins.
Key words: GABAA receptors; synapses; neurexins; neuroligins
Bei WU , Chen ZHANG . Neurexins and neuroligins: new partners for GABAA receptors at synapses[J]. Frontiers in Biology, 2011 , 6(3) : 251 -260 . DOI: 10.1007/s11515-011-1020-2
1 |
Absalom N L, Schofield P R, Lewis T M (2009). Pore structure of the Cys-loop ligand-gated ion channels. Neurochem Res, 34(10): 1805–1815
|
2 |
Alldred M J, Mulder-Rosi J, Lingenfelter S E, Chen G, Lüscher B (2005). Distinct gamma2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin. J Neurosci, 25(3): 594–603
|
3 |
Allison D W, Chervin A S, Gelfand V I, Craig A M (2000). Postsynaptic scaffolds of excitatory and inhibitory synapses in hippocampal neurons: maintenance of core components independent of actin filaments and microtubules. J Neurosci, 20(12): 4545–4554
|
4 |
Araç D, Boucard A A, Ozkan E, Strop P, Newell E, Südhof T C, Brunger A T (2007). Structures of neuroligin-1 and the neuroligin-1/neurexin-1 beta complex reveal specific protein-protein and protein-Ca2+ interactions. Neuron, 56(6): 992–1003
|
5 |
Atasoy D, Ertunc M, Moulder K L, Blackwell J, Chung C, Su J, Kavalali E T (2008). Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap. J Neurosci, 28(40): 10151–10166
|
6 |
Baer K, Essrich C, Benson J A, Benke D, Bluethmann H, Fritschy J M, Lüscher B (1999). Postsynaptic clustering of gamma-aminobutyric acid type A receptors by the gamma3 subunit in vivo. Proc Natl Acad Sci USA, 96(22): 12860–12865
|
7 |
Baulac S, Huberfeld G, Gourfinkel-An I, Mitropoulou G, Beranger A, Prud’homme J F, Baulac M, Brice A, Bruzzone R, LeGuern E (2001). First genetic evidence of GABA(A) receptor dysfunction in epilepsy: a mutation in the gamma2-subunit gene. Nat Genet, 28(1): 46–48
|
8 |
Beck M, Brickley K, Wilkinson H L, Sharma S, Smith M, Chazot P L, Pollard S, Stephenson F A (2002). Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J Biol Chem, 277(33): 30079–30090
|
9 |
Bedford F K, Kittler J T, Muller E, Thomas P, Uren J M, Merlo D, Wisden W, Triller A, Smart T G, Moss S J (2001). GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat Neurosci, 4(9): 908–916
|
10 |
Blatt G J (2005). GABAergic cerebellar system in autism: a neuropathological and developmental perspective. Int Rev Neurobiol, 71: 167–178
|
11 |
Boileau A J, Pearce R A, Czajkowski C (2005). Tandem subunits effectively constrain GABAA receptor stoichiometry and recapitulate receptor kinetics but are insensitive to GABAA receptor-associated protein. J Neurosci, 25(49): 11219–11230
|
12 |
Boucard A A, Chubykin A A, Comoletti D, Taylor P, Südhof T C (2005). A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron, 48(2): 229–236
|
13 |
Brejc K, van Dijk W J, Klaassen R V, Schuurmans M, van Der Oost J, Smit A B, Sixma T K (2001). Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature, 411(6835): 269–276
|
14 |
Brünig I, Scotti E, Sidler C, Fritschy J M (2002). Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol, 443(1): 43–55
|
15 |
Bucan M, Abrahams B S, Wang K, Glessner J T, Herman E I, Sonnenblick L I, Alvarez Retuerto A I, Imielinski M, Hadley D, Bradfield J P, Kim C, Gidaya N B, Lindquist I, Hutman T, Sigman M, Kustanovich V, Lajonchere C M, Singleton A, Kim J, Wassink T H, McMahon W M, Owley T, Sweeney J A, Coon H, Nurnberger J I, Li M, Cantor R M, Minshew N J, Sutcliffe J S, Cook E H, Dawson G, Buxbaum J D, Grant S F, Schellenberg G D, Geschwind D H, Hakonarson H, Gibson G (2009). Genome-wide analyses of exonic copy number variants in a family-based study point to novel autism susceptibility genes. PLoS Genet, 5(6): e1000536
|
16 |
Buhr A, Bianchi M T, Baur R, Courtet P, Pignay V, Boulenger J P, Gallati S, Hinkle D J, Macdonald R L, Sigel E (2002). Functional characterization of the new human GABA(A) receptor mutation beta3(R192H). Hum Genet, 111(2): 154–160
|
17 |
Caraiscos V B, Elliott E M, You-Ten K E, Cheng V Y, Belelli D, Newell J G, Jackson M F, Lambert J J, Rosahl T W, Wafford K A, MacDonald J F, Orser B A (2004). Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci USA, 101(10): 3662–3667
|
18 |
Cederholm J M E, Schofield P R, Lewis T M (2009). Gating mechanisms in Cys-loop receptors. Eur Biophys J, 39(1): 37–49
|
19 |
Charych E I, Yu W, Miralles C P, Serwanski D R, Li X, Rubio M, De Blas A L (2004). The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the beta subunits of the GABA receptors. J Neurochem, 90(1): 173–189
|
20 |
Chen L, Wang H, Vicini S, Olsen R W (2000). The gamma-aminobutyric acid type A (GABAA) receptor-associated protein (GABARAP) promotes GABAA receptor clustering and modulates the channel kinetics. Proc Natl Acad Sci USA, 97(21): 11557–11562
|
21 |
Chen Z W, Chang C S, Leil T A, Olcese R, Olsen R W (2005). GABAA receptor-associated protein regulates GABAA receptor cell-surface number in Xenopus laevis oocytes. Mol Pharmacol, 68(1): 152–159
|
22 |
Cherlyn S Y T, Woon P S, Liu J J, Ong W Y, Tsai G C, Sim K (2010). Genetic association studies of glutamate, GABA and related genes in schizophrenia and bipolar disorder: a decade of advance. Neurosci Biobehav Rev, 34(6): 958–977
|
23 |
Cherubini E, Gaiarsa J L, Ben-Ari Y (1991). GABA: an excitatory transmitter in early postnatal life. Trends Neurosci, 14(12): 515–519
|
24 |
Christie S B, Li R W, Miralles C P, Riquelme R, Yang B Y, Charych E, WendouYu, Daniels S B, Cantino M E, De Blas A L (2002). Synaptic and extrasynaptic GABAA receptor and gephyrin clusters. Prog Brain Res, 136: 157–180
|
25 |
Chubykin A A, Atasoy D, Etherton M R, Brose N, Kavalali E T, Gibson J R, Südhof T C (2007). Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron, 54(6): 919–931
|
26 |
Chubykin A A, Liu X, Comoletti D, Tsigelny I, Taylor P, Südhof T C (2005). Dissection of synapse induction by neuroligins: effect of a neuroligin mutation associated with autism. J Biol Chem, 280(23): 22365–22374
|
27 |
Cockcroft V B, Osguthorpe D J, Barnard E A, Lunt G G (1990). Modeling of agonist binding to the ligand-gated ion channel superfamily of receptors. Proteins, 8(4): 386–397
|
28 |
Collins A L, Ma D, Whitehead P L, Martin E R, Wright H H, Abramson R K, Hussman J P, Haines J L, Cuccaro M L, Gilbert J R, Pericak-Vance M A (2006). Investigation of autism and GABA receptor subunit genes in multiple ethnic groups. Neurogenetics, 7(3): 167–174
|
29 |
Connolly C N, Wafford K A (2004). The Cys-loop superfamily of ligand-gated ion channels: the impact of receptor structure on function. Biochem Soc Trans, 32(Pt3): 529–534
|
30 |
Cossette P, Liu L, Brisebois K, Dong H, Lortie A, Vanasse M, Saint-Hilaire J M, Carmant L, Verner A, Lu W Y, Wang Y T, Rouleau G A (2002). Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat Genet, 31(2): 184–189
|
31 |
Craig A M, Kang Y (2007). Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol, 17(1): 43–52
|
32 |
Dan B, Boyd S G (2003). Angelman syndrome reviewed from a neurophysiological perspective. The UBE3A-GABRB3 hypothesis. Neuropediatrics, 34(4): 169–176
|
33 |
Dean C, Dresbach T (2006). Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci, 29(1): 21–29
|
34 |
Dean C, Scholl F G, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P (2003). Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci, 6(7): 708–716
|
35 |
Dudanova I, Tabuchi K, Rohlmann A, Südhof T C, Missler M (2007). Deletion of alpha-neurexins does not cause a major impairment of axonal pathfinding or synapse formation. J Comp Neurol, 502(2): 261–274
|
36 |
Dykens E M, Sutcliffe J S, Levitt P (2004). Autism and 15q11-q13 disorders: behavioral, genetic, and pathophysiological issues. Ment Retard Dev Disabil Res Rev, 10(4): 284–291
|
37 |
Ernst M, Brauchart D, Boresch S, Sieghart W (2003). Comparative modeling of GABA(A) receptors: limits, insights, future developments. Neuroscience, 119(4): 933–943
|
38 |
Ernst M, Bruckner S, Boresch S, Sieghart W (2005). Comparative models of GABAA receptor extracellular and transmembrane domains: important insights in pharmacology and function. Mol Pharmacol, 68(5): 1291–1300
|
39 |
Essrich C, Lorez M, Benson J A, Fritschy J M, Lüscher B (1998). Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci, 1(7): 563–571
|
40 |
Fischer F, Kneussel M, Tintrup H, Haverkamp S, Rauen T, Betz H, Wässle H (2000). Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. J Comp Neurol, 427(4): 634–648
|
41 |
Fredj N B, Burrone J (2009). A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci, 12(6): 751–758
|
42 |
Fritschy J M, Johnson D K, Mohler H, Rudolph U (1998). Independent assembly and subcellular targeting of GABA(A)-receptor subtypes demonstrated in mouse hippocampal and olfactory neurons in vivo. Neurosci Lett, 249(2-3): 99–102
|
43 |
Fuhrmann J C, Kins S, Rostaing P, El Far O, Kirsch J, Sheng M, Triller A, Betz H, Kneussel M (2002). Gephyrin interacts with Dynein light chains 1 and 2, components of motor protein complexes. J Neurosci, 22(13): 5393–5402
|
44 |
Gibson J R, Huber K M, Südhof T C (2009). Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking but not from somatostatin-positive interneurons. J Neurosci, 29(44): 13883–13897
|
45 |
Giesemann T, Schwarz G, Nawrotzki R, Berhörster K, Rothkegel M, Schlüter K, Schrader N, Schindelin H, Mendel R R, Kirsch J, Jockusch B M (2003). Complex formation between the postsynaptic scaffolding protein gephyrin, profilin, and Mena: a possible link to the microfilament system. J Neurosci, 23(23): 8330–8339
|
46 |
Giustetto M, Kirsch J, Fritschy J M, Cantino D, Sassoè-Pognetto M (1998). Localization of the clustering protein gephyrin at GABAergic synapses in the main olfactory bulb of the rat. J Comp Neurol, 395(2): 231–244
|
47 |
Goldstein P A, Elsen F P, Ying S W, Ferguson C, Homanics G E, Harrison N L (2002). Prolongation of hippocampal miniature inhibitory postsynaptic currents in mice lacking the GABA(A) receptor alpha1 subunit. J Neurophysiol, 88(6): 3208–3217
|
48 |
Gonzalez-Burgos G, Hashimoto T, Lewis D A (2010). Alterations of cortical GABA neurons and network oscillations in schizophrenia. Curr Psychiatry Rep, 12(4): 335–344
|
49 |
Goto H, Terunuma M, Kanematsu T, Misumi Y, Moss S J, Hirata M (2005). Direct interaction of N-ethylmaleimide-sensitive factor with GABA(A) receptor beta subunits. Mol Cell Neurosci, 30(2): 197–206
|
50 |
Graf E R, Zhang X, Jin S X, Linhoff M W, Craig A M (2004). Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell, 119(7): 1013–1026
|
51 |
Guidotti A, Auta J, Davis J M, Dong E, Grayson D R, Veldic M, Zhang X, Costa E (2005). GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon. Psychopharmacology (Berl), 180(2): 191–205
|
52 |
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, Smart T G, Lüscher B, Rees M I, Harvey R J (2004). The GDP-GTP exchange factor collybistin: an essential determinant of neuronal gephyrin clustering. J Neurosci, 24(25): 5816–5826
|
53 |
Herd M B, Haythornthwaite A R, Rosahl T W, Wafford K A, Homanics G E, Lambert J J, Belelli D (2008). The expression of GABAA beta subunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells. J Physiol, 586(4): 989–1004
|
54 |
Hoon M, Bauer G, Fritschy J M, Moser T, Falkenburger B H, Varoqueaux F (2009). Neuroligin 2 controls the maturation of GABAergic synapses and information processing in the retina. J Neurosci, 29(25): 8039–8050
|
55 |
Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Südhof T C (1995). Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell, 81(3): 435–443
|
56 |
Ichtchenko K, Nguyen T, Südhof T C (1996). Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem, 271(5): 2676–2682
|
57 |
Jacob T C, Bogdanov Y D, Magnus C, Saliba R S, Kittler J T, Haydon P G, Moss S J (2005). Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci, 25(45): 10469–10478
|
58 |
Kananura C, Haug K, Sander T, Runge U, Gu W, Hallmann K, Rebstock J, Heils A, Steinlein O K (2002). A splice-site mutation in GABRG2 associated with childhood absence epilepsy and febrile convulsions. Arch Neurol, 59(7): 1137–1141
|
59 |
Kim H G, Kishikawa S, Higgins A W, Seong I S, Donovan D J, Shen Y, Lally E, Weiss L A, Najm J, Kutsche K, Descartes M, Holt L, Braddock S, Troxell R, Kaplan L, Volkmar F, Klin A, Tsatsanis K, Harris D J, Noens I, Pauls D L, Daly M J, MacDonald M E, Morton C C, Quade B J, Gusella J F (2008). Disruption of neurexin 1 associated with autism spectrum disorder. Am J Hum Genet, 82(1): 199–207
|
60 |
Kins S, Betz H, Kirsch J (2000). Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nat Neurosci, 3(1): 22–29
|
61 |
Kirov G, Gumus D, Chen W, Norton N, Georgieva L, Sari M, O’Donovan M C, Erdogan F, Owen M J, Ropers H H, Ullmann R (2008). Comparative genome hybridization suggests a role for NRXN1 and APBA2 in schizophrenia. Hum Mol Genet, 17(3): 458–465
|
62 |
Kirsch J, Betz H (1995). The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton. J Neurosci, 15(6): 4148–4156
|
63 |
Kirsch J, Langosch D, Prior P, Littauer U Z, Schmitt B, Betz H (1991). The 93-kDa glycine receptor-associated protein binds to tubulin. J Biol Chem, 266(33): 22242–22245
|
64 |
Kittler J T, Delmas P, Jovanovic J N, Brown D A, Smart T G, Moss S J (2000). Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci, 20(21): 7972–7977
|
65 |
Kittler J T, Thomas P, Tretter V, Bogdanov Y D, Haucke V, Smart T G, Moss S J (2004). Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc Natl Acad Sci USA, 101(34): 12736–12741
|
66 |
Kneussel M, Brandstätter J H, Laube B, Stahl S, Müller U, Betz H (1999). Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J Neurosci, 19(21): 9289–9297
|
67 |
Kneussel M, Haverkamp S, Fuhrmann J C, Wang H, Wässle H, Olsen R W, Betz H (2000). The gamma-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc Natl Acad Sci USA, 97(15): 8594–8599
|
68 |
Lalande M, Calciano M A (2007). Molecular epigenetics of Angelman syndrome. Cell Mol Life Sci, 64(7-8): 947–960
|
69 |
Leil T A, Chen Z W, Chang C S, Olsen R W (2004). GABAA receptor-associated protein traffics GABAA receptors to the plasma membrane in neurons. J Neurosci, 24(50): 11429–11438
|
70 |
Lester H A, Dibas M I, Dahan D S, Leite J F, Dougherty D A (2004). Cys-loop receptors: new twists and turns. Trends Neurosci, 27(6): 329–336
|
71 |
Lisé M F, El-Husseini A (2006). The neuroligin and neurexin families: from structure to function at the synapse. Cell Mol Life Sci, 63(16): 1833–1849
|
72 |
Lüscher B, Keller C A (2004). Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther, 102(3): 195–221
|
73 |
Mammoto A, Sasaki T, Asakura T, Hotta I, Imamura H, Takahashi K, Matsuura Y, Shirao T, Takai Y (1998). Interactions of drebrin and gephyrin with profilin. Biochem Biophys Res Commun, 243(1): 86–89
|
74 |
Marshall C R, Noor A, Vincent J B, Lionel A C, Feuk L, Skaug J, Shago M, Moessner R, Pinto D, Ren Y, Thiruvahindrapduram B, Fiebig A, Schreiber S, Friedman J, Ketelaars C E, Vos Y J, Ficicioglu C, Kirkpatrick S, Nicolson R, Sloman L, Summers A, Gibbons C A, Teebi A, Chitayat D, Weksberg R, Thompson A, Vardy C, Crosbie V, Luscombe S, Baatjes R, Zwaigenbaum L, Roberts W, Fernandez B, Szatmari P, Scherer S W (2008). Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet, 82(2): 477–488
|
75 |
Maximov A, Tang J, Yang X, Pang Z P, Südhof T C (2009). Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science, 323(5913): 516–521
|
76 |
Meyer G, Kirsch J, Betz H, Langosch D (1995). Identification of a gephyrin binding motif on the glycine receptor beta subunit. Neuron, 15(3): 563–572
|
77 |
Missler M, Fernandez-Chacon R, Südhof T C (1998). The making of neurexins. J Neurochem, 71(4): 1339–1347
|
78 |
Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer R E, Gottmann K, Südhof T C (2003). Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature, 423(6943): 939–948
|
79 |
Miyazawa A, Fujiyoshi Y, Unwin N (2003). Structure and gating mechanism of the acetylcholine receptor pore. Nature, 423(6943): 949–955
|
80 |
Need A C, Ge D, Weale M E, Maia J, Feng S, Heinzen E L, Shianna K V, Yoon W, Kasperaviciūte D, Gennarelli M, Strittmatter W J, Bonvicini C, Rossi G, Jayathilake K, Cola P A, McEvoy J P, Keefe R S, Fisher E M, St Jean P L, Giegling I, Hartmann A M, Möller H J, Ruppert A, Fraser G, Crombie C, Middleton L T, St Clair D, Roses A D, Muglia P, Francks C, Rujescu D, Meltzer H Y, Goldstein D B (2009). A genome-wide investigation of SNPs and CNVs in schizophrenia. PLoS Genet, 5(2): e1000373
|
81 |
Nguyen T, Südhof T C (1997). Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J Biol Chem, 272(41): 26032–26039
|
82 |
Nusser Z, Roberts J D, Baude A, Richards J G, Sieghart W, Somogyi P (1995). Immunocytochemical localization of the alpha 1 and beta 2/3 subunits of the GABAA receptor in relation to specific GABAergic synapses in the dentate gyrus. Eur J Neurosci, 7(4): 630–646
|
83 |
Nusser Z, Sieghart W, Somogyi P (1998). Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci, 18(5): 1693–1703
|
84 |
Nutt D J, Malizia A L (2001). New insights into the role of the GABA(A)-benzodiazepine receptor in psychiatric disorder. Br J Psychiatry, 179(5): 390–396
|
85 |
Nymann-Andersen J, Wang H, Chen L, Kittler J T, Moss S J, Olsen R W (2002b). Subunit specificity and interaction domain between GABA(A) receptor-associated protein (GABARAP) and GABA(A) receptors. J Neurochem, 80(5): 815–823
|
86 |
Nymann-Andersen J, Wang H, Olsen R W (2002a). Biochemical identification of the binding domain in the GABA(A) receptor-associated protein (GABARAP) mediating dimer formation. Neuropharmacology, 43(4): 476–481
|
87 |
O’Sullivan G A, Kneussel M, Elazar Z, Betz H (2005). GABARAP is not essential for GABA receptor targeting to the synapse. Eur J Neurosci, 22(10): 2644–2648
|
88 |
Ortinski P I, Lu C, Takagaki K, Fu Z, Vicini S (2004). Expression of distinct alpha subunits of GABAA receptor regulates inhibitory synaptic strength. J Neurophysiol, 92(3): 1718–1727
|
89 |
Paarmann I, Schmitt B, Meyer B, Karas M, Betz H (2006). Mass spectrometric analysis of glycine receptor-associated gephyrin splice variants. J Biol Chem, 281(46): 34918–34925
|
90 |
Papadopoulos T, Korte M, Eulenburg V, Kubota H, Retiounskaia M, Harvey R J, Harvey K, O’Sullivan G A, Laube B, Hülsmann S, Geiger J R P, Betz H (2007). Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin-deficient mice. EMBO J, 26(17): 3888–3899
|
91 |
Petryshen T L, Middleton F A, Tahl A R, Rockwell G N, Purcell S, Aldinger K A, Kirby A, Morley C P, McGann L, Gentile K L, Waggoner S G, Medeiros H M, Carvalho C, Macedo A, Albus M, Maier W, Trixler M, Eichhammer P, Schwab S G, Wildenauer D B, Azevedo M H, Pato M T, Pato C N, Daly M J, Sklar P (2005). Genetic investigation of chromosome 5q GABAA receptor subunit genes in schizophrenia. Mol Psychiatry, 10(12): 1074–1088, 1057
|
92 |
Pfeiffer F, Graham D, Betz H (1982). Purification by affinity chromatography of the glycine receptor of rat spinal cord. J Biol Chem, 257(16): 9389–9393
|
93 |
Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000). GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience, 101(4): 815–850
|
94 |
Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Zhang M, Paarmann I, Fuchs C, Harvey K, Jedlicka P, Schwarzacher S W, Betz H, Harvey R J, Brose N, Zhang W, Varoqueaux F (2009). Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron, 63(5): 628–642
|
95 |
Prior P, Schmitt B, Grenningloh G, Pribilla I, Multhaup G, Beyreuther K, Maulet Y, Werner P, Langosch D, Kirsch J,
|
96 |
Rivera C, Voipio J, Payne J A, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999). The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature, 397(6716): 251–255
|
97 |
Roberts E, Frankel S (1950). gamma-Aminobutyric acid in brain: its formation from glutamic acid. J Biol Chem, 187(1): 55–63
|
98 |
Rujescu D, Ingason A, Cichon S, Pietiläinen O P, Barnes M R, Toulopoulou T, Picchioni M, Vassos E, Ettinger U, Bramon E, Murray R, Ruggeri M, Tosato S, Bonetto C, Steinberg S, Sigurdsson E, Sigmundsson T, Petursson H, Gylfason A, Olason P I, Hardarsson G, Jonsdottir G A, Gustafsson O, Fossdal R, Giegling I, Möller H J, Hartmann A M, Hoffmann P, Crombie C, Fraser G, Walker N, Lonnqvist J, Suvisaari J, Tuulio-Henriksson A, Djurovic S, Melle I, Andreassen O A, Hansen T, Werge T, Kiemeney L A, Franke B, Veltman J, Buizer-Voskamp J E, GROUP Investigators, Sabatti C, Ophoff R A, Rietschel M, Nöthen M M, Stefansson K, Peltonen L, St Clair D, Stefansson H, Collier D A, (2009). Disruption of the neurexin 1 gene is associated with schizophrenia. Hum Mol Genet, 18(5): 988–996
|
99 |
Rupprecht R, Eser D, Zwanzger P, Möller H J (2006). GABAA receptors as targets for novel anxiolytic drugs. World J Biol Psychiatry, 7(4): 231–237
|
100 |
Sassoè-Pognetto M, Panzanelli P, Sieghart W, Fritschy J M (2000). Colocalization of multiple GABA(A) receptor subtypes with gephyrin at postsynaptic sites. J Comp Neurol, 420(4): 481–498
|
101 |
Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000). Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell, 101(6): 657–669
|
102 |
Schmitz C, van Kooten I A J, Hof P R, van Engeland H, Patterson P H, Steinbusch H W M (2005). Autism: neuropathology, alterations of the GABAergic system, and animal models. Int Rev Neurobiol, 71: 1–26
|
103 |
Shah A K, Tioleco N M, Nolan K, Locker J, Groh K, Villa C, Stopkova P, Pedrosa E, Lachman H M (2010). Rare NRXN1 promoter variants in patients with schizophrenia. Neurosci Lett, 475(2): 80–84
|
104 |
Sieghart W, Fuchs K, Tretter V, Ebert V, Jechlinger M, Höger H, Adamiker D (1999). Structure and subunit composition of GABA(A) receptors. Neurochem Int, 34(5): 379–385
|
105 |
Sieghart W, Sperk G (2002). Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem, 2(8): 795–816
|
106 |
Smith G B, Olsen R W (1995). Functional domains of GABAA receptors. Trends Pharmacol Sci, 16(5): 162–168
|
107 |
Smith M J, Pozo K, Brickley K, Stephenson F A (2006). Mapping the GRIF-1 binding domain of the kinesin, KIF5C, substantiates a role for GRIF-1 as an adaptor protein in the anterograde trafficking of cargoes. J Biol Chem, 281(37): 27216–27228
|
108 |
Solís-Añez E, Delgado-Luengo W, Hernández M L (2007). Autism, chromosome 15 and the GAbaergic dysfunction hypothesis. Invest Clin, 48(4): 529–541 (in Spanish) PMID:18271397
|
109 |
Song J Y, Ichtchenko K, Südhof T C, Brose N (1999). Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci USA, 96(3): 1100–1105
|
110 |
Südhof T C (2008). Neuroligins and neurexins link synaptic function to cognitive disease. Nature, 455(7215): 903–911
|
111 |
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, Feuk L, Qian C, Bryson S E, Jones M B, Marshall C R, Scherer S W, Vieland V J, Bartlett C, Mangin L V, Goedken R, Segre A, Pericak-Vance M A, Cuccaro M L, Gilbert J R, Wright H H, Abramson R K, Betancur C, Bourgeron T, Gillberg C, Leboyer M, Buxbaum J D, Davis K L, Hollander E, Silverman J M, Hallmayer J, Lotspeich L, Sutcliffe J S, Haines J L, Folstein S E, Piven J, Wassink T H, Sheffield V, Geschwind D H, Bucan M, Brown W T, Cantor R M, Constantino J N, Gilliam T C, Herbert M, Lajonchere C, Ledbetter D H, Lese-Martin C, Miller J, Nelson S, Samango-Sprouse C A, Spence S, State M, Tanzi R E, Coon H, Dawson G, Devlin B, Estes A, Flodman P, Klei L, McMahon W M, Minshew N, Munson J, Korvatska E, Rodier P M, Schellenberg G D, Smith M, Spence M A, Stodgell C, Tepper P G, Wijsman E M, Yu C E, Rogé B, Mantoulan C, Wittemeyer K, Poustka A, Felder B, Klauck S M, Schuster C, Poustka F, Bölte S, Feineis-Matthews S, Herbrecht E, Schmötzer G, Tsiantis J, Papanikolaou K, Maestrini E, Bacchelli E, Blasi F, Carone S, Toma C, Van Engeland H, de Jonge M, Kemner C, Koop F, Koop F, Langemeijer M, Langemeijer M, Hijmans C, Hijimans C, Staal W G, Baird G, Bolton P F, Rutter M L, Weisblatt E, Green J, Aldred C, Wilkinson J A, Pickles A, Le Couteur A, Berney T, McConachie H, Bailey A J, Francis K, Honeyman G, Hutchinson A, Parr J R, Wallace S, Monaco A P, Barnby G, Kobayashi K, Lamb J A, Sousa I, Sykes N, Cook E H, Guter S J, Leventhal B L, Salt J, Lord C, Corsello C, Hus V, Weeks D E, Volkmar F, Tauber M, Fombonne E, Shih A, Meyer K J, and the Autism Genome Project Consortium (2007). Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet, 39(3): 319–328
|
112 |
Tabuchi K, Südhof T C (2002). Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics, 79(6): 849–859
|
113 |
Tanida I, Ueno T, Kominami E (2004). LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol, 36(12): 2503–2518
|
114 |
Taniguchi H, Gollan L, Scholl F G, Mahadomrongkul V, Dobler E, Limthong N, Peck M, Aoki C, Scheiffele P (2007). Silencing of neuroligin function by postsynaptic neurexins. J Neurosci, 27(11): 2815–2824
|
115 |
Todd A J, Watt C, Spike R C, Sieghart W (1996). Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci, 16(3): 974–982
|
116 |
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, Kittler J T (2010). Delivery of GABAARs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin. Neuron, 65(1): 53–65
|
117 |
Uhlhaas P J, Singer W (2010). Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci, 11(2): 100–113
|
118 |
Unwin N (2005). Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol, 346(4): 967–989
|
119 |
Ushkaryov Y A, Petrenko A G, Geppert M, Südhof T C (1992). Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science, 257(5066): 50–56
|
120 |
Varoqueaux F, Aramuni G, Rawson R L, Mohrmann R, Missler M, Gottmann K, Zhang W, Südhof T C, Brose N (2006). Neuroligins determine synapse maturation and function. Neuron, 51(6): 741–754
|
121 |
Varoqueaux F, Jamain S, Brose N (2004). Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol, 83(9): 449–456
|
122 |
Vithlani M, Moss S J (2009). The role of GABAAR phosphorylation in the construction of inhibitory synapses and the efficacy of neuronal inhibition. Biochem Soc Trans, 37(Pt 6): 1355–1358
|
123 |
Wallace R H, Marini C, Petrou S, Harkin L A, Bowser D N, Panchal R G, Williams D A, Sutherland G R, Mulley J C, Scheffer I E, Berkovic S F (2001). Mutant GABA(A) receptor gamma2-subunit in childhood absence epilepsy and febrile seizures. Nat Genet, 28(1): 49–52
|
124 |
Walsh T, McClellan J M, McCarthy S E, Addington A M, Pierce S B, Cooper G M, Nord A S, Kusenda M, Malhotra D, Bhandari A, Stray S M, Rippey C F, Roccanova P, Makarov V, Lakshmi B, Findling R L, Sikich L, Stromberg T, Merriman B, Gogtay N, Butler P, Eckstrand K, Noory L, Gochman P, Long R, Chen Z, Davis S, Baker C, Eichler E E, Meltzer P S, Nelson S F, Singleton A B, Lee M K, Rapoport J L, King M C, Sebat J (2008). Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science, 320(5875): 539–543
|
125 |
Wang H, Bedford F K, Brandon N J, Moss S J, Olsen R W (1999). GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature, 397(6714): 69–72
|
126 |
Wei W, Zhang N, Peng Z, Houser C R, Mody I (2003). Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci, 23(33): 10650–10661
|
127 |
Whatley V J, Mihic S J, Allan A M, McQuilkin S J, Harris R A (1994). Gamma-aminobutyric acidA receptor function is inhibited by microtubule depolymerization. J Biol Chem, 269(30): 19546–19552
|
128 |
Whiting P J (1999). The GABA-A receptor gene family: new targets for therapeutic intervention. Neurochem Int, 34(5): 387–390
|
129 |
Wiśniowiecka-Kowalnik B, Nesteruk M, Peters S U, Xia Z, Cooper M L, Savage S, Amato R S, Bader P, Browning M F, Haun C L, Duda A W 3rd, Cheung S W, Stankiewicz P (2010). Intragenic rearrangements in NRXN1 in three families with autism spectrum disorder, developmental delay, and speech delay. Am J Med Genet B Neuropsychiatr Genet, 153B(5): 983–993
|
130 |
Xin Y, Yu L, Chen Z, Zheng L, Fu Q, Jiang J, Zhang P, Gong R, Zhao S (2001). Cloning, expression patterns, and chromosome localization of three human and two mouse homologues of GABA(A) receptor-associated protein. Genomics, 74(3): 408–413
|
131 |
Xu J, Pang Z P, Shin O H, Südhof T C (2009). Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release. Nat Neurosci, 12(6): 759–766
|
132 |
Yan J, Noltner K, Feng J, Li W, Schroer R, Skinner C, Zeng W, Schwartz C E, Sommer S S (2008). Neurexin 1alpha structural variants associated with autism. Neurosci Lett, 438(3): 368–370
|
133 |
Zahir F R, Baross A, Delaney A D, Eydoux P, Fernandes N D, Pugh T, Marra M A, Friedman J M (2008). A patient with vertebral, cognitive and behavioural abnormalities and a de novo deletion of NRXN1alpha. J Med Genet, 45(4): 239–243
|
134 |
Zhang C, Atasoy D, Araç D, Yang X, Fucillo M V, Robison A J, Ko J, Brunger A T, Südhof T C (2010). Neurexins physically and functionally interact with GABA(A) receptors. Neuron, 66(3): 403–416
|
135 |
Zhang C, Milunsky J M, Newton S, Ko J, Zhao G, Maher T A, Tager-Flusberg H, Bolliger M F, Carter A S, Boucard A A, Powell C M, Südhof T C (2009). A neuroligin-4 missense mutation associated with autism impairs neuroligin-4 folding and endoplasmic reticulum export. J Neurosci, 29(35): 10843–10854
|
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