{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T06:22:33Z","timestamp":1790144553758,"version":"4.0.1"},"reference-count":68,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2019,12,12]],"date-time":"2019-12-12T00:00:00Z","timestamp":1576108800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Mol. Neurosci."],"DOI":"10.3389\/fnmol.2019.00304","type":"journal-article","created":{"date-parts":[[2019,12,12]],"date-time":"2019-12-12T04:19:50Z","timestamp":1576124390000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":24,"title":["Molecular Architecture of Genetically-Tractable GABA Synapses in C. elegans"],"prefix":"10.3389","volume":"12","author":[{"given":"Xin","family":"Zhou","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Louis","family":"Bessereau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2019,12,12]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1242\/dev.030759","article-title":"An UNC-40 pathway directs postsynaptic membrane extension in Caenorhabditis elegans","volume":"136","author":"Alexander","year":"2009","journal-title":"Development"},{"key":"B2","doi-asserted-by":"publisher","first-page":"31493","DOI":"10.1074\/jbc.r109.052340","article-title":"A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms","volume":"284","author":"Apte","year":"2009","journal-title":"J. Biol. Chem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"5348","DOI":"10.1523\/JNEUROSCI.19-13-05348.1999","article-title":"The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor","volume":"19","author":"Bamber","year":"1999","journal-title":"J. Neurosci."},{"key":"B4","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1038\/sj.bjp.0705119","article-title":"Pharmacological characterization of the homomeric and heteromeric UNC-49 GABA receptors in C. elegans","volume":"138","author":"Bamber","year":"2003","journal-title":"Br. J. Pharmacol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1145","DOI":"10.1038\/nn1136","article-title":"EXP-1 is an excitatory GABA-gated cation channel","volume":"6","author":"Beg","year":"2003","journal-title":"Nat. Neurosci."},{"key":"B7","doi-asserted-by":"publisher","first-page":"221","DOI":"10.3389\/fncel.2018.00221","article-title":"Revisiting netrin-1: one who guides (Axons)","volume":"12","author":"Boyer","year":"2018","journal-title":"Front. Cell. Neurosci."},{"key":"B8","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1093\/genetics\/77.1.71","article-title":"The genetics of Caenorhabditis elegans","volume":"77","author":"Brenner","year":"1974","journal-title":"Genetics"},{"key":"B9","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1007\/s10158-014-0173-5","article-title":"Conserved and divergent processing of neuroligin and neurexin genes: from the nematode C. elegans to human","volume":"14","author":"Calahorro","year":"2014","journal-title":"Invert. Neurosci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.gep.2015.02.002","article-title":"Analysis of splice variants for the C. elegans orthologue of human neuroligin reveals a developmentally regulated transcript","volume":"17","author":"Calahorro","year":"2015","journal-title":"Gene Expr. Patterns"},{"key":"B11","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/s0092-8674(00)81337-9","article-title":"UNC-40, a C. elegans homolog of DCC (deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues","volume":"87","author":"Chan","year":"1996","journal-title":"Cell"},{"key":"B12","doi-asserted-by":"publisher","first-page":"985","DOI":"10.1083\/jcb.201205041","article-title":"The novel synaptogenic protein Farp1 links postsynaptic cytoskeletal dynamics and transsynaptic organization","volume":"199","author":"Cheadle","year":"2012","journal-title":"J. Cell Biol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"7999","DOI":"10.1523\/jneurosci.3950-13.2014","article-title":"Activity-dependent regulation of dendritic complexity by semaphorin 3A through Farp1","volume":"34","author":"Cheadle","year":"2014","journal-title":"J. Neurosci."},{"key":"B14","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1038\/s41586-019-1352-7","article-title":"Whole-animal connectomes of both Caenorhabditis elegans sexes","volume":"571","author":"Cook","year":"2019","journal-title":"Nature"},{"key":"B15","doi-asserted-by":"publisher","first-page":"7104","DOI":"10.1523\/jneurosci.0378-08.2008","article-title":"Behavioral impact of neurotransmitter-activated GPCRs: muscarinic and GABAB receptors regulate C. elegans locomotion","volume":"28","author":"Dittman","year":"2008","journal-title":"J. Neurosci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.schres.2010.12.009","article-title":"ADAMTSL3 as a candidate gene for schizophrenia: gene sequencing and ultra-high density association analysis by imputation","volume":"127","author":"Dow","year":"2011","journal-title":"Schizophr. Res."},{"key":"B17","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1146\/annurev-neuro-062111-150433","article-title":"Evolution of synapse complexity and diversity","volume":"35","author":"Emes","year":"2012","journal-title":"Ann. Rev. Neurosci."},{"key":"B18","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.pbiomolbio.2015.04.001","article-title":"Signaling mechanism of the netrin-1 receptor DCC in axon guidance","volume":"118","author":"Finci","year":"2015","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/j.tins.2008.02.006","article-title":"Gephyrin: where do we stand, where do we go?","volume":"31","author":"Fritschy","year":"2008","journal-title":"Trends Neurosci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"2591","DOI":"10.1523\/jneurosci.23-07-02591.2003","article-title":"GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans","volume":"23","author":"Gally","year":"2003","journal-title":"J. Neurosci."},{"key":"B21","doi-asserted-by":"publisher","first-page":"e17686","DOI":"10.7554\/eLife.17686","article-title":"A cellular and regulatory map of the GABAergic nervous system of C. elegans","volume":"5","author":"Gendrel","year":"2016","journal-title":"Elife"},{"key":"B22","doi-asserted-by":"publisher","first-page":"1137","DOI":"10.1038\/nn959","article-title":"SYD-1, a presynaptic protein with PDZ, C2 and rhoGAP-like domains, specifies axon identity in C. elegans","volume":"5","author":"Hallam","year":"2002","journal-title":"Nat. Neurosci."},{"key":"B23","doi-asserted-by":"publisher","first-page":"2488","DOI":"10.1523\/jneurosci.16-08-02488.1996","article-title":"CASK: a novel dlg\/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins","volume":"16","author":"Hata","year":"1996","journal-title":"J. Neurosci."},{"key":"B24","doi-asserted-by":"publisher","first-page":"1485","DOI":"10.1002\/humu.23299","article-title":"Identification and functional analysis of an ADAMTSL1 variant associated with a complex phenotype including congenital glaucoma, craniofacial and other systemic features in a three generation human pedigree","volume":"38","author":"Hendee","year":"2017","journal-title":"Hum. Mutat."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1895\/wormbook.1.161.1","article-title":"The neuronal genome of Caenorhabditis elegans","volume":"13","author":"Hobert","year":"2018","journal-title":"WormBook"},{"key":"B26","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1093\/genetics\/103.1.43","article-title":"Male phenotypes and mating efficiency in Caenorhabditis elegans","volume":"103","author":"Hodgkin","year":"1983","journal-title":"Genetics"},{"key":"B27","doi-asserted-by":"publisher","first-page":"366","DOI":"10.1242\/dmm.003442","article-title":"Neuroligin-deficient mutants of C. elegans have sensory processing deficits and are hypersensitive to oxidative stress and mercury toxicity","volume":"3","author":"Hunter","year":"2010","journal-title":"Dis. Model. Mech."},{"key":"B28","doi-asserted-by":"publisher","first-page":"2803","DOI":"10.1523\/jneurosci.4557-14.2015","article-title":"Spillover transmission is mediated by the excitatory GABA receptor LGC-35 in C. elegans","volume":"35","author":"Jobson","year":"2015","journal-title":"J. Neurosci."},{"key":"B29","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1007\/s10158-008-0068-4","article-title":"The cys-loop ligand-gated ion channel gene superfamily of the nematode, Caenorhabditis elegans","volume":"8","author":"Jones","year":"2008","journal-title":"Invert. Neurosci."},{"key":"B30","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/s1044-5781(06)80030-7","article-title":"Neuromuscular junctions in the nematode C. elegans","volume":"6","author":"Jorgensen","year":"1995","journal-title":"Semin. Dev. Biol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/s0092-8674(00)81336-7","article-title":"Deleted in colorectal cancer (DCC) encodes a netrin receptor","volume":"87","author":"Keino-Masu","year":"1996","journal-title":"Cell"},{"key":"B32","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1038\/71096","article-title":"Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin","volume":"3","author":"Kins","year":"2000","journal-title":"Nat. Neurosci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1006\/mcne.2001.0983","article-title":"Gephyrin-independent clustering of postsynaptic GABAA receptor subtypes","volume":"17","author":"Kneussel","year":"2001","journal-title":"Mol. Cell. Neurosci."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1282","DOI":"10.1016\/j.cub.2015.03.028","article-title":"Transcriptional coordination of synaptogenesis and neurotransmitter signaling","volume":"25","author":"Kratsios","year":"2015","journal-title":"Curr. Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"150.e4","DOI":"10.1016\/j.neuron.2018.09.007","article-title":"\u03b3-neurexin and frizzled mediate parallel synapse assembly pathways antagonized by receptor endocytosis","volume":"100","author":"Kurshan","year":"2018","journal-title":"Neuron"},{"key":"B36","doi-asserted-by":"publisher","first-page":"e1129486","DOI":"10.1080\/21624054.2015.1129486","article-title":"Neural circuit rewiring: insights from DD synapse remodeling","volume":"5","author":"Kurup","year":"2015","journal-title":"Worm"},{"key":"B37","doi-asserted-by":"publisher","first-page":"362","DOI":"10.1007\/s12031-013-0194-2","article-title":"Tracking the origin and divergence of cholinesterases and neuroligins: the evolution of synaptic proteins","volume":"53","author":"Lenfant","year":"2014","journal-title":"J. Mol. Neurosci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"895","DOI":"10.1038\/nmeth.1252","article-title":"Optogenetic analysis of synaptic function","volume":"5","author":"Liewald","year":"2008","journal-title":"Nat. Methods"},{"key":"B39","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1002\/dneu.20307","article-title":"A quantum of neurotransmitter causes minis in multiple postsynaptic cells at the Caenorhabditis elegans neuromuscular junction","volume":"67","author":"Liu","year":"2007","journal-title":"Dev. Neurobiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1420","DOI":"10.1016\/j.neuron.2015.05.015","article-title":"MADD-4\/punctin and neurexin Organize C. elegans GABAergic postsynapses through neuroligin","volume":"86","author":"Maro","year":"2015","journal-title":"Neuron"},{"key":"B41","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1038\/364334a0","article-title":"Genes required for GABA function in Caenorhabditis elegans","volume":"364","author":"McIntire","year":"","journal-title":"Nature"},{"key":"B42","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1038\/364337a0","article-title":"The GABAergic nervous system of Caenorhabditis elegans","volume":"364","author":"McIntire","year":"","journal-title":"Nature"},{"key":"B43","doi-asserted-by":"publisher","first-page":"870","DOI":"10.1038\/39908","article-title":"Identification and characterization of the vesicular GABA transporter","volume":"389","author":"McIntire","year":"1997","journal-title":"Nature"},{"key":"B44","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1016\/s0896-6273(02)01020-6","article-title":"Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase","volume":"36","author":"Misgeld","year":"2002","journal-title":"Neuron"},{"key":"B45","doi-asserted-by":"publisher","first-page":"94","DOI":"10.3389\/fncir.2018.00094","article-title":"A pipeline for volume electron microscopy of the Caenorhabditis elegans nervous system","volume":"12","author":"Mulcahy","year":"2018","journal-title":"Front. Neural Circuits"},{"key":"B46","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1038\/nature13313","article-title":"C. elegans Punctin specifies cholinergic versus GABAergic identity of postsynaptic domains","volume":"511","author":"Pinan-Lucarr\u00e9","year":"2014","journal-title":"Nature"},{"key":"B48","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1038\/14755","article-title":"UNC-13 is required for synaptic vesicle fusion in C. elegans","volume":"2","author":"Richmond","year":"1999","journal-title":"Nat. Neurosci."},{"key":"B47","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1038\/12160","article-title":"One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction","volume":"2","author":"Richmond","year":"1999","journal-title":"Nat. Neurosci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"701","DOI":"10.1038\/nrn2717","article-title":"The origin and evolution of synapses","volume":"10","author":"Ryan","year":"2009","journal-title":"Nat. Rev. Neurosci."},{"key":"B50","doi-asserted-by":"publisher","first-page":"e506","DOI":"10.1371\/journal.pone.0000506","article-title":"A post-synaptic scaffold at the origin of the animal kingdom","volume":"2","author":"Sakarya","year":"2007","journal-title":"PLoS One"},{"key":"B51","doi-asserted-by":"publisher","first-page":"817","DOI":"10.1152\/jn.00578.2010","article-title":"Optogenetic analysis of GABAB receptor signaling in Caenorhabditis elegans motor neurons","volume":"106","author":"Schultheis","year":"2011","journal-title":"J. Neurophysiol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1016\/j.tins.2004.05.005","article-title":"The GABA nervous system in C. elegans","volume":"27","author":"Schuske","year":"2004","journal-title":"Trends in Neurosci."},{"key":"B53","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1016\/j.devcel.2011.07.020","article-title":"MADD-4 is a secreted cue required for midline-oriented guidance in Caenorhabditis elegans","volume":"21","author":"Seetharaman","year":"2011","journal-title":"Dev. Cell"},{"key":"B54","doi-asserted-by":"publisher","first-page":"304.e4","DOI":"10.1016\/j.neuron.2017.03.029","article-title":"Formation and maintenance of functional spines in the absence of presynaptic glutamate release","volume":"94","author":"Sigler","year":"2017","journal-title":"Neuron"},{"key":"B56","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1038\/nature07456","article-title":"Neuroligins and neurexins link synaptic function to cognitive disease","volume":"455","author":"S\u00fcdhof","year":"2008","journal-title":"Nature"},{"key":"B57","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1093\/genetics\/124.4.855","article-title":"Genetic analysis of defecation in Caenorhabditis elegans","volume":"124","author":"Thomas","year":"1990","journal-title":"Genetics"},{"key":"B58","doi-asserted-by":"publisher","first-page":"e09648","DOI":"10.7554\/eLife.09648","article-title":"A network of autism linked genes stabilizes two pools of synaptic GABAA receptors","volume":"4","author":"Tong","year":"2015","journal-title":"ELife"},{"key":"B59","doi-asserted-by":"publisher","first-page":"23","DOI":"10.3389\/fncel.2012.00023","article-title":"Gephyrin, the enigmatic organizer at GABAergic synapses","volume":"6","author":"Tretter","year":"2012","journal-title":"Front. Cell. Neurosci."},{"key":"B60","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1093\/molbev\/msl188","article-title":"The evolution of GABAA receptor-like genes","volume":"24","author":"Tsang","year":"2007","journal-title":"Mol. Biol. Evol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"1407","DOI":"10.1016\/j.neuron.2015.05.013","article-title":"C. elegans punctin clusters GABAA receptors via neuroligin binding and UNC-40\/DCC recruitment","volume":"86","author":"Tu","year":"2015","journal-title":"Neuron"},{"key":"B62","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1038\/nrn3670","article-title":"Gephyrin: a master regulator of neuronal function?","volume":"15","author":"Tyagarajan","year":"2014","journal-title":"Nat. Rev. Neurosci."},{"key":"B63","doi-asserted-by":"publisher","first-page":"2786","DOI":"10.1242\/jcs.086199","article-title":"Collybistin splice variants differentially interact with gephyrin and Cdc42 to regulate gephyrin clustering at GABAergic synapses","volume":"124","author":"Tyagarajan","year":"2011","journal-title":"J. Cell Sci."},{"key":"B64","doi-asserted-by":"publisher","first-page":"9037","DOI":"10.1073\/pnas.122623799","article-title":"Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming","volume":"99","author":"Varoqueaux","year":"2002","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"B65","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1016\/j.neuron.2008.02.019","article-title":"An RNAi screen identifies genes that regulate GABA synapses","volume":"58","author":"Vashlishan","year":"2008","journal-title":"Neuron"},{"key":"B67","doi-asserted-by":"publisher","first-page":"764","DOI":"10.1038\/271764a0","article-title":"Connectivity changes in a class of motoneurone during the development of a nematode","volume":"271","author":"White","year":"1978","journal-title":"Nature"},{"key":"B66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1098\/rstb.1986.0056","article-title":"The structure of the nervous system of the nematode Caenorhabditis elegans","volume":"314","author":"White","year":"1986","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"B68","doi-asserted-by":"publisher","first-page":"3833","DOI":"10.1523\/JNEUROSCI.4978-04.2005","article-title":"Identification of genes involved in synaptogenesis using a fluorescent active zone marker in Caenorhabditis elegans","volume":"25","author":"Yeh","year":"2005","journal-title":"J. Neurosci."},{"key":"B70","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1016\/s0896-6273(00)81167-8","article-title":"Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain","volume":"26","author":"Zhen","year":"2000","journal-title":"Neuron"},{"key":"B69","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1038\/43886","article-title":"The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans","volume":"401","author":"Zhen","year":"1999","journal-title":"Nature"}],"container-title":["Frontiers in Molecular Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fnmol.2019.00304\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,11]],"date-time":"2021-02-11T19:44:57Z","timestamp":1613072697000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fnmol.2019.00304\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,12]]},"references-count":68,"alternative-id":["10.3389\/fnmol.2019.00304"],"URL":"https:\/\/doi.org\/10.3389\/fnmol.2019.00304","relation":{},"ISSN":["1662-5099"],"issn-type":[{"value":"1662-5099","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,12]]},"article-number":"304"}}