{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T11:29:08Z","timestamp":1791804548375,"version":"4.3.4"},"reference-count":56,"publisher":"Frontiers Media SA","funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["RA 1804\/2-1"],"award-info":[{"award-number":["RA 1804\/2-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Neurosci."],"DOI":"10.3389\/fncel.2016.00207","type":"journal-article","created":{"date-parts":[[2016,9,4]],"date-time":"2016-09-04T23:07:00Z","timestamp":1473030420000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":26,"title":["The Drosophila KIF1A Homolog unc-104 Is Important for Site-Specific Synapse Maturation"],"prefix":"10.3389","volume":"10","author":[{"given":"Yao V.","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shabab B.","family":"Hannan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zeenna A.","family":"Stapper","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeannine V.","family":"Kern","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas R.","family":"Jahn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tobias M.","family":"Rasse","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2016,9,5]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"923","DOI":"10.15252\/embr.201540434","article-title":"Presynaptic active zones in invertebrates and vertebrates","volume":"16","author":"Ackermann","year":"2015","journal-title":"EMBO Rep."},{"key":"B2","doi-asserted-by":"publisher","first-page":"I2","DOI":"10.1007\/s102860200013","article-title":"Hereditary sensory and autonomic neuropathies. Familial dysautonomia and other HSANs","volume":"12","author":"Axelrod","year":"2002","journal-title":"Clin. Auton. Res."},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1523\/ENEURO.0031-16.2016","article-title":"Rab3-GEF controls active zone development at the Drosophila neuromuscular junction","volume":"3","author":"Bae","year":"2016","journal-title":"eNeuro"},{"key":"B4","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1091\/mbc.e07-03-0261","article-title":"Identification of an axonal kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides","volume":"19","author":"Barkus","year":"2008","journal-title":"Mol. Biol. Cell"},{"key":"B5","doi-asserted-by":"publisher","first-page":"17048","DOI":"10.1523\/JNEUROSCI.3267-12.2012","article-title":"Fife, a Drosophila Piccolo-RIM homolog, promotes active zone organization and neurotransmitter release","volume":"32","author":"Bruckner","year":"2012","journal-title":"J. Neurosci."},{"key":"B6","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1177\/1073858415596131","article-title":"Building a terminal: mechanisms of presynaptic development in the CNS","volume":"22","author":"Bury","year":"2015","journal-title":"Neuroscientist"},{"key":"B7","doi-asserted-by":"publisher","first-page":"3623","DOI":"10.1093\/hmg\/ddv107","article-title":"Impaired retrograde transport by the dynein\/dynactin complex contributes to tau-induced toxicity","volume":"24","author":"Butzlaff","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"B8","doi-asserted-by":"publisher","first-page":"e0136938","DOI":"10.1371\/journal.pone.0136938","article-title":"Mutational analysis of rab3 function for controlling active zone protein composition at the Drosophila neuromuscular junction","volume":"10","author":"Chen","year":"2015","journal-title":"PLoS One"},{"key":"B9","doi-asserted-by":"publisher","first-page":"2684","DOI":"10.1007\/s00415-015-7899-9","article-title":"Variants in KIF1A gene in dominant and sporadic forms of hereditary spastic paraparesis","volume":"262","author":"Citterio","year":"2015","journal-title":"J. Neurol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.neuron.2005.11.032","article-title":"A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle","volume":"49","author":"Daniels","year":"2006","journal-title":"Neuron"},{"key":"B11","doi-asserted-by":"publisher","first-page":"10466","DOI":"10.1523\/JNEUROSCI.3001-04.2004","article-title":"Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content","volume":"24","author":"Daniels","year":"2004","journal-title":"J. Neurosci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1111\/j.1365-2990.2004.00587.x","article-title":"The extent of axonal loss in the long tracts in hereditary spastic paraplegia","volume":"30","author":"Deluca","year":"2004","journal-title":"Neuropathol. Appl. Neurobiol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"658","DOI":"10.1101\/gr.117143.110","article-title":"Exome sequencing and disease-network analysis of a single family implicate a mutation in KIF1A in hereditary spastic paraparesis","volume":"21","author":"Erlich","year":"2011","journal-title":"Genome Res."},{"key":"B14","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1002\/acn3.198","article-title":"De novo mutations in KIF1A cause progressive encephalopathy and brain atrophy","volume":"2","author":"Esmaeeli Nieh","year":"2015","journal-title":"Ann. Clin. Transl. Neurol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1083\/jcb.200812150","article-title":"Maturation of active zone assembly by Drosophila Bruchpilot","volume":"186","author":"Fouquet","year":"2009","journal-title":"J. Cell Biol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"17560","DOI":"10.1523\/JNEUROSCI.3261-13.2013","article-title":"New approaches for studying synaptic development, function and plasticity using Drosophila as a model system","volume":"33","author":"Frank","year":"2013","journal-title":"J. Neurosci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"e1003066","DOI":"10.1371\/journal.pgen.1003066","article-title":"Spastic paraplegia mutation N256S in the neuronal microtubule motor KIF5A disrupts axonal transport in a Drosophila HSP model","volume":"8","author":"Fuger","year":"2012","journal-title":"PLoS Genet."},{"key":"B18","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1146\/annurev.neuro.21.1.75","article-title":"RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion","volume":"21","author":"Geppert","year":"1998","journal-title":"Annu. Rev. Neurosci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"621","DOI":"10.1111\/j.1460-9568.2008.06049.x","article-title":"The evolutionarily conserved gene LNP-1 is required for synaptic vesicle trafficking and synaptic transmission","volume":"27","author":"Ghila","year":"2008","journal-title":"Eur. J. Neurosci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1016\/j.neuron.2009.11.029","article-title":"Rab3 GTPase lands Bruchpilot","volume":"64","author":"Giagtzoglou","year":"2009","journal-title":"Neuron"},{"key":"B21","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1016\/j.neuron.2009.11.002","article-title":"Rab3 dynamically controls protein composition at active zones","volume":"64","author":"Graf","year":"2009","journal-title":"Neuron"},{"key":"B22","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1016\/j.ajhg.2011.02.001","article-title":"Excess of de novo deleterious mutations in genes associated with glutamatergic systems in nonsyndromic intellectual disability","volume":"88","author":"Hamdan","year":"2011","journal-title":"Am. J. Hum. Genet."},{"key":"B23","doi-asserted-by":"publisher","first-page":"I33","DOI":"10.1007\/s102860200017","article-title":"Assessment and evaluation of hereditary sensory and autonomic neuropathies with autonomic and neurophysiological examinations","volume":"12","author":"Hilz","year":"2002","journal-title":"Clin. Auton. Res."},{"key":"B24","doi-asserted-by":"publisher","first-page":"1114","DOI":"10.1177\/0883073816639718","article-title":"Novel de novo mutations in KIF1A as a cause of hereditary spastic paraplegia with progressive central nervous system involvement","volume":"31","author":"Hotchkiss","year":"2016","journal-title":"J. Child Neurol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"2833","DOI":"10.1152\/jn.90342.2008","article-title":"Delayed synaptic transmission in Drosophila cacophonynull embryos","volume":"100","author":"Hou","year":"2008","journal-title":"J. Neurophysiol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"e1000193","DOI":"10.1371\/journal.pbio.1000193","article-title":"Negative regulation of active zone assembly by a newly identified SR protein kinase","volume":"7","author":"Johnson","year":"2009","journal-title":"PLoS Biol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/s0896-6273(02)00643-8","article-title":"Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis","volume":"34","author":"Kaufmann","year":"2002","journal-title":"Neuron"},{"key":"B28","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1523\/jneurosci.3553-03.2004","article-title":"Active zone localization of presynaptic calcium channels encoded by the cacophony locus of Drosophila","volume":"24","author":"Kawasaki","year":"2004","journal-title":"J. Neurosci."},{"key":"B29","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1534\/genetics.113.151639","article-title":"The kinesin-3, unc-104 regulates dendrite morphogenesis and synaptic development in Drosophila","volume":"195","author":"Kern","year":"2013","journal-title":"Genetics"},{"key":"B30","doi-asserted-by":"publisher","first-page":"1051","DOI":"10.1126\/science.1126308","article-title":"Bruchpilot promotes active zone assembly, Ca2+ channel clustering and vesicle release","volume":"312","author":"Kittel","year":"2006","journal-title":"Science"},{"key":"B31","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1038\/ejhg.2011.261","article-title":"KIF1A missense mutations in SPG30, an autosomal recessive spastic paraplegia: distinct phenotypes according to the nature of the mutations","volume":"20","author":"Klebe","year":"2012","journal-title":"Eur. J. Hum. Genet."},{"key":"B32","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1002\/humu.22709","article-title":"De novo mutations in the motor domain of KIF1A cause cognitive impairment, spastic paraparesis, axonal neuropathy and cerebellar atrophy","volume":"36","author":"Lee","year":"2015","journal-title":"Hum. Mutat."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1565","DOI":"10.1126\/science.1212991","article-title":"RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release","volume":"334","author":"Liu","year":"2011","journal-title":"Science"},{"key":"B34","doi-asserted-by":"publisher","first-page":"518","DOI":"10.1016\/j.expneurol.2014.06.011","article-title":"Hereditary spastic paraplegia: clinical-genetic characteristics and evolving molecular mechanisms","volume":"261","author":"Lo Giudice","year":"2014","journal-title":"Exp. Neurol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1016\/j.modgep.2005.07.006","article-title":"The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain","volume":"6","author":"Mahr","year":"2006","journal-title":"Gene Expr. Patterns"},{"key":"B36","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1016\/j.neuron.2011.01.025","article-title":"Rab3-GAP controls the progression of synaptic homeostasis at a late stage of vesicle release","volume":"69","author":"M\u00fcller","year":"2011","journal-title":"Neuron"},{"key":"B37","doi-asserted-by":"publisher","first-page":"e1000700","DOI":"10.1371\/journal.pgen.1000700","article-title":"Bruchpilot in ribbon-like axonal agglomerates, behavioral defects and early death in SRPK79D kinase mutants of Drosophila","volume":"5","author":"Nieratschker","year":"2009","journal-title":"PLoS Genet."},{"key":"B38","doi-asserted-by":"publisher","first-page":"1269","DOI":"10.1038\/ncb1785","article-title":"KIF1B\u03b2- and KIF1A-mediated axonal transport of presynaptic regulator Rab3 occurs in a GTP-dependent manner through DENN\/MADD","volume":"10","author":"Niwa","year":"2008","journal-title":"Nat. Cell Biol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1038\/jhg.2015.108","article-title":"De novo KIF1A mutations cause intellectual deficit, cerebellar atrophy, lower limb spasticity and visual disturbance","volume":"60","author":"Ohba","year":"2015","journal-title":"J. Hum. Genet."},{"key":"B41","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1083\/jcb.200908055","article-title":"A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila","volume":"188","author":"Owald","year":"2010","journal-title":"J. Cell Biol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/j.conb.2009.03.003","article-title":"Assembling the presynaptic active zone","volume":"19","author":"Owald","year":"2009","journal-title":"Curr. Opin. Neurobiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"980","DOI":"10.1038\/nn1936","article-title":"A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport","volume":"10","author":"Pack-Chung","year":"2007","journal-title":"Nat. Neurosci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"3209","DOI":"10.1523\/jneurosci.4194-04.2005","article-title":"Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila","volume":"25","author":"Qin","year":"2005","journal-title":"J. Neurosci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1002\/neu.1072","article-title":"Visualization of neuropeptide expression, transport and exocytosis in Drosophila melanogaster","volume":"49","author":"Rao","year":"2001","journal-title":"J. Neurobiol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1038\/nn1484","article-title":"Glutamate receptor dynamics organizing synapse formation in vivo","volume":"8","author":"Rasse","year":"2005","journal-title":"Nat. Neurosci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/s0959-4388(02)00360-4","article-title":"The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans","volume":"12","author":"Richmond","year":"2002","journal-title":"Curr. Opin. Neurobiol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/j.ajhg.2011.06.013","article-title":"KIF1A, an axonal transporter of synaptic vesicles, is mutated in hereditary sensory and autonomic neuropathy type 2","volume":"89","author":"Rivi\u00e8re","year":"2011","journal-title":"Am. J. Hum. Genet."},{"key":"B48","doi-asserted-by":"publisher","first-page":"896","DOI":"10.1038\/nn1719","article-title":"Activity-dependent synaptic capture of transiting peptidergic vesicles","volume":"9","author":"Shakiryanova","year":"2006","journal-title":"Nat. Neurosci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"11393","DOI":"10.1074\/jbc.m211874200","article-title":"Association of the kinesin motor KIF1A with the multimodular protein liprin-alpha","volume":"278","author":"Shin","year":"2003","journal-title":"J. Biol. Chem."},{"key":"B50","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.neuron.2012.06.012","article-title":"The presynaptic active zone","volume":"75","author":"S\u00fcdhof","year":"2012","journal-title":"Neuron"},{"key":"B51","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1016\/j.neuron.2006.02.008","article-title":"Bruchpilot, a protein with homology to ELKS\/CAST, is required for structural integrity and function of synaptic active zones in Drosophila","volume":"49","author":"Wagh","year":"2006","journal-title":"Neuron"},{"key":"B52","doi-asserted-by":"publisher","first-page":"1427","DOI":"10.1038\/ejhg.2014.297","article-title":"Dominant transmission of de novo KIF1A motor domain variant underlying pure spastic paraplegia","volume":"23","author":"Ylikallio","year":"2015","journal-title":"Eur. J. Hum. Genet."},{"key":"B53","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1083\/jcb.141.2.431","article-title":"Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice","volume":"141","author":"Yonekawa","year":"1998","journal-title":"J. Cell Biol."},{"key":"B54","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"},{"key":"B55","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1126\/science.8310297","article-title":"Paralysis and early death in cysteine string protein mutants of Drosophila","volume":"263","author":"Zinsmaier","year":"1994","journal-title":"Science"},{"key":"B56","doi-asserted-by":"publisher","first-page":"15","DOI":"10.3109\/01677069009084150","article-title":"A cysteine-string protein is expressed in retina and brain of Drosophila","volume":"7","author":"Zinsmaier","year":"1990","journal-title":"J. Neurogenet."}],"container-title":["Frontiers in Cellular Neuroscience"],"original-title":[],"deposited":{"date-parts":[[2016,10,4]],"date-time":"2016-10-04T13:05:22Z","timestamp":1475586322000},"score":1,"resource":{"primary":{"URL":"http:\/\/journal.frontiersin.org\/Article\/10.3389\/fncel.2016.00207\/abstract"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,9,5]]},"references-count":56,"URL":"https:\/\/doi.org\/10.3389\/fncel.2016.00207","relation":{},"ISSN":["1662-5102"],"issn-type":[{"value":"1662-5102","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,9,5]]}}}