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Active Zone Assembly

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Abstract

The formation of neurotransmitter release sites, or active zones, is a fundamental process in neuronal development. It allows neurons to communicate with their targets through the regulated exocytosis of neurotransmitter. To this end, active zones, including a complex network of presynaptic scaffolding proteins called the cytomatrix of active zones, have to be formed at defined sites inside an axon. This poses a substantial challenge to cellular transport and assembly mechanisms, because a complex network of cytomatrix proteins has to be formed exactly opposite postsynaptic specializations. A large number of proteins have been implicated in active zone assembly, but how these proteins interact to mediate the transport, recruitment, and organization of the cytomatrix network has remained unclear.

Here I will review and discuss current notions of the various steps required to ultimately form active zones in axons of vertebrate and invertebrate neurons. To execute the whole process, the cell biological machinery of a neuron appears to generate organelles designed for the transport of cytomatrix components; these organelles then undergo trafficking events that are regulated to ensure the deposition of cytomatrix material at nascent active zones. Local signals act to both capture and release cytomatrix material at active zones in a controlled manner. Cell adhesion molecules allow for transsynaptic signalling, to synchronize pre- and postsynaptic assembly. Various cell adhesion systems may cooperate to mediate the local assembly of active zones and to endow each active zone with its specific functional properties. Together, these events act to coordinate the process of active zone assembly, thus generating the output sites for synaptic signalling.

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References

  • Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445–451

    CAS  PubMed  Google Scholar 

  • Ahmed S, Wittenmayer N, Kremer T, Hoeber J, Kiran Akula A et al (2013) Mover is a homomeric phospho-protein present on synaptic vesicles. PLoS One 8:e63474

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aiga M, Levinson JN, Bamji SX (2011) N-cadherin and neuroligins cooperate to regulate synapse formation in hippocampal cultures. J Biol Chem 286:851–858

    CAS  PubMed Central  PubMed  Google Scholar 

  • Andrews-Zwilling YS, Kawabe H, Reim K, Varoqueaux F, Brose N (2006) Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2. J Biol Chem 281:19720–19731

    CAS  PubMed  Google Scholar 

  • Augustin I, Rosenmund C, Sudhof TC, Brose N (1999) Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400:457–461

    CAS  PubMed  Google Scholar 

  • Boeckers TM (2006) The postsynaptic density. Cell Tissue Res 326:409–422

    CAS  PubMed  Google Scholar 

  • Boucard AA, Chubykin AA, Comoletti D, Taylor P, Sudhof TC (2005) A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to α- and β-neurexins. Neuron 48:229–236

    CAS  PubMed  Google Scholar 

  • Bresler T, Shapira M, Boeckers T, Dresbach T, Futter M et al (2004) Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. J Neurosci 24:1507–1520

    CAS  PubMed  Google Scholar 

  • Brose N (2013) Why we need more synaptogenic cell-adhesion proteins. Proc Natl Acad Sci U S A 110:3717–3718

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brose N, Rosenmund C, Rettig J (2000) Regulation of transmitter release by Unc-13 and its homologues. Curr Opin Neurobiol 10:303–311

    CAS  PubMed  Google Scholar 

  • Bury LA, Sabo SL (2011) Coordinated trafficking of synaptic vesicle and active zone proteins prior to synapse formation. Neural Dev 6:24

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bury LA, Sabo SL (2014) Dynamic mechanisms of neuroligin-dependent presynaptic terminal assembly in living cortical neurons. Neural Dev 9:13

    PubMed Central  PubMed  Google Scholar 

  • Cai Q, Gerwin C, Sheng ZH (2005) Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J Cell Biol 170:959–969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cai Q, Pan PY, Sheng ZH (2007) Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J Neurosci 27:7284–7296

    CAS  PubMed  Google Scholar 

  • Cases-Langhoff C, Voss B, Garner AM, Appeltauer U, Takei K et al (1996) Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. Eur J Cell Biol 69:214–223

    CAS  PubMed  Google Scholar 

  • Cheadle L, Biederer T (2012) The novel synaptogenic protein Farp1 links postsynaptic cytoskeletal dynamics and transsynaptic organization. J Cell Biol 199:985–1001

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chia PH, Patel MR, Shen K (2012) NAB-1 instructs synapse assembly by linking adhesion molecules and F-actin to active zone proteins. Nat Neurosci 15:234–242

    CAS  PubMed  Google Scholar 

  • Chia PH, Li P, Shen K (2013) Cell biology in neuroscience: cellular and molecular mechanisms underlying presynapse formation. J Cell Biol 203:11–22

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chih B, Engelman H, Scheiffele P (2005) Control of excitatory and inhibitory synapse formation by neuroligins. Science 307:1324–1328

    CAS  PubMed  Google Scholar 

  • Chih B, Gollan L, Scheiffele P (2006) Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51:171–178

    CAS  PubMed  Google Scholar 

  • Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET et al (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54:919–931

    CAS  PubMed Central  PubMed  Google Scholar 

  • Couteaux R, Pecot-Dechavassine M (1970) Synaptic vesicles and pouches at the level of “active zones” of the neuromuscular junction. C R Acad Sci Hebd Seances Acad Sci D Sci Nat 271:2346–2349

    CAS  Google Scholar 

  • Dai Y, Taru H, Deken SL, Grill B, Ackley B et al (2006) SYD-2 Liprin-α organizes presynaptic active zone formation through ELKS. Nat Neurosci 9:1479–1487

    CAS  PubMed  Google Scholar 

  • Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: signalling functions at the synapse. Nat Rev Neurosci 8:206–220

    CAS  PubMed  Google Scholar 

  • Dani A, Huang B, Bergan J, Dulac C, Zhuang X (2010) Superresolution imaging of chemical synapses in the brain. Neuron 68:843–856

    CAS  PubMed Central  PubMed  Google Scholar 

  • de Wit J, Ghosh A (2014) Control of neural circuit formation by leucine-rich repeat proteins. Trends Neurosci 37:539–550

    PubMed  Google Scholar 

  • de Wit J, Sylwestrak E, O’Sullivan ML, Otto S, Tiglio K et al (2009) LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 64:799–806

    PubMed Central  PubMed  Google Scholar 

  • Dean C, Dresbach T (2006) Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29:21–29

    CAS  PubMed  Google Scholar 

  • Dean C, Scholl FG, Choih J, DeMaria S, Berger J et al (2003) Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6:708–716

    CAS  PubMed Central  PubMed  Google Scholar 

  • Deng L, Kaeser PS, Xu W, Sudhof TC (2011) RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 69:317–331

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ding M, Chao D, Wang G, Shen K (2007) Spatial regulation of an E3 ubiquitin ligase directs selective synapse elimination. Science 317:947–951

    CAS  PubMed  Google Scholar 

  • Dresbach T, Qualmann B, Kessels MM, Garner CC, Gundelfinger ED (2001) The presynaptic cytomatrix of brain synapses. Cell Mol Life Sci 58:94–116

    CAS  PubMed  Google Scholar 

  • Dresbach T, Fejtova A, Gundelfinger ED (2006a) Assembly of presynaptic active zones. In: Dityatev A, El-Husseini A (eds) Molecular mechanisms of synaptogenesis. Springer, Berlin/Heidelberg, pp 235–244

    Google Scholar 

  • Dresbach T, Torres V, Wittenmayer N, Altrock WD, Zamorano P et al (2006b) Assembly of active zone precursor vesicles: obligatory trafficking of presynaptic cytomatrix proteins bassoon and piccolo via a trans-golgi compartment. J Biol Chem 281:6038–6047

    CAS  PubMed  Google Scholar 

  • Easley-Neal C, Fierro J Jr, Buchanan J, Washbourne P (2013) Late recruitment of synapsin to nascent synapses is regulated by Cdk5. Cell Rep 3:1199–1212

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fejtova A, Gundelfinger ED (2006) Molecular organization and assembly of the presynaptic active zone of neurotransmitter release. Results Probl Cell Differ 43:49–68

    CAS  PubMed  Google Scholar 

  • Fejtova A, Davydova D, Bischof F, Lazarevic V, Altrock WD et al (2009) Dynein light chain regulates axonal trafficking and synaptic levels of Bassoon. J Cell Biol 185:341–355

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fenster SD, Chung WJ, Zhai R, Cases-Langhoff C, Voss B et al (2000) Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron 25:203–214

    CAS  PubMed  Google Scholar 

  • Fernandez-Busnadiego R, Zuber B, Maurer UE, Cyrklaff M, Baumeister W, Lucic V (2010) Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J Cell Biol 188:145–156

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fogel AI, Akins MR, Krupp AJ, Stagi M, Stein V, Biederer T (2007) SynCAMs organize synapses through heterophilic adhesion. J Neurosci 27:12516–12530

    CAS  PubMed  Google Scholar 

  • Friedman HV, Bresler T, Garner CC, Ziv NE (2000) Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57–69

    CAS  PubMed  Google Scholar 

  • Garcia EP, McPherson PS, Chilcote TJ, Takei K, De Camilli P (1995) rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J Cell Biol 129:105–120

    CAS  PubMed  Google Scholar 

  • Giagtzoglou N, Ly CV, Bellen HJ (2009) Cell adhesion, the backbone of the synapse: “vertebrate” and “invertebrate” perspectives. Cold Spring Harb Perspect Biol 1:a003079

    PubMed Central  PubMed  Google Scholar 

  • Gokce O, Sudhof TC (2013) Membrane-tethered monomeric neurexin LNS-domain triggers synapse formation. J Neurosci 33:14617–14628

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goldstein AY, Wang X, Schwarz TL (2008) Axonal transport and the delivery of pre-synaptic components. Curr Opin Neurobiol 18:495–503

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goodwin PR, Sasaki JM, Juo P (2012) Cyclin-dependent kinase 5 regulates the polarized trafficking of neuropeptide-containing dense-core vesicles in Caenorhabditis elegans motor neurons. J Neurosci 32:8158–8172

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gotow T, Miyaguchi K, Hashimoto PH (1991) Cytoplasmic architecture of the axon terminal: filamentous strands specifically associated with synaptic vesicles. Neuroscience 40:587–598

    CAS  PubMed  Google Scholar 

  • Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013–1026

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gray EG (1963) Electron microscopy of presynaptic organelles of the spinal chord. J Anat 97:101–106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gundelfinger ED, Fejtova A (2012) Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol 22(3):423–430

    CAS  PubMed  Google Scholar 

  • Hallam SJ, Goncharov A, McEwen J, Baran R, Jin Y (2002) SYD-1, a presynaptic protein with PDZ, C2 and rhoGAP-like domains, specifies axon identity in C. elegans. Nat Neurosci 5:1137–1146

    CAS  PubMed  Google Scholar 

  • Hirokawa N, Sobue K, Kanda K, Harada A, Yorifuji H (1989) The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J Cell Biol 108:111–126

    CAS  PubMed  Google Scholar 

  • Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M et al (1995) Neuroligin 1: a splice site-specific ligand for β-neurexins. Cell 81:435–443

    CAS  PubMed  Google Scholar 

  • Jin Y, Garner CC (2008) Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol 24:237–262

    CAS  PubMed  Google Scholar 

  • Kleijer KT, Schmeisser MJ, Krueger DD, Boeckers TM, Scheiffele P et al (2014) Neurobiology of autism gene products: towards pathogenesis and drug targets. Psychopharmacology 231:1037–1062

    CAS  PubMed  Google Scholar 

  • Ko J, Fuccillo MV, Malenka RC, Sudhof TC (2009) LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 64:791–798

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kremer T, Kempf C, Wittenmayer N, Nawrotzki R, Kuner T et al (2007) Mover is a novel vertebrate-specific presynaptic protein with differential distribution at subsets of CNS synapses. FEBS Lett 581:4727–4733

    CAS  PubMed  Google Scholar 

  • Landis DM, Hall AK, Weinstein LA, Reese TS (1988) The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron 1:201–209

    CAS  PubMed  Google Scholar 

  • Langnaese K, Seidenbecher C, Wex H, Seidel B, Hartung K et al (1996) Protein components of a rat brain synaptic junctional protein preparation. Brain Res Mol Brain Res 42:118–122

    CAS  PubMed  Google Scholar 

  • Lee SH, Peng IF, Ng YG, Yanagisawa M, Bamji SX et al (2008) Synapses are regulated by the cytoplasmic tyrosine kinase Fer in a pathway mediated by p120catenin, Fer, SHP-2, and β-catenin. J Cell Biol 183:893–908

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee SJ, Uemura T, Yoshida T, Mishina M (2012) GluRδ2 assembles four neurexins into trans-synaptic triad to trigger synapse formation. J Neurosci 32:4688–4701

    CAS  PubMed  Google Scholar 

  • Levinson JN, Chery N, Huang K, Wong TP, Gerrow K et al (2005) Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1β in neuroligin-induced synaptic specificity. J Biol Chem 280:17312–17319

    CAS  PubMed  Google Scholar 

  • Liao EH, Hung W, Abrams B, Zhen M (2004) An SCF-like ubiquitin ligase complex that controls presynaptic differentiation. Nature 430:345–350

    CAS  PubMed  Google Scholar 

  • Limbach C, Laue MM, Wang X, Hu B, Thiede N et al (2011) Molecular in situ topology of Aczonin/Piccolo and associated proteins at the mammalian neurotransmitter release site. Proc Natl Acad Sci U S A 108:E392–E401

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maas C, Torres VI, Altrock WD, Leal-Ortiz S, Wagh D et al (2012) Formation of Golgi-derived active zone precursor vesicles. J Neurosci 32:11095–11108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maeder CI, Shen K, Hoogenraad CC (2014) Axon and dendritic trafficking. Curr Opin Neurobiol 27:165–170

    CAS  PubMed  Google Scholar 

  • Mah W, Ko J, Nam J, Han K, Chung WS, Kim E (2010) Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation. J Neurosci 30:5559–5568

    CAS  PubMed  Google Scholar 

  • Mishina M, Uemura T, Yasumura M, Yoshida T (2012) Molecular mechanism of parallel fiber-Purkinje cell synapse formation. Front Neural Circuits 6:90

    CAS  PubMed Central  PubMed  Google Scholar 

  • Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE et al (2003) Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423:939–948

    CAS  PubMed  Google Scholar 

  • Nakata K, Abrams B, Grill B, Goncharov A, Huang X et al (2005) Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120:407–420

    CAS  PubMed  Google Scholar 

  • Ohtsuka T, Takao-Rikitsu E, Inoue E, Inoue M, Takeuchi M et al (2002) Cast: a novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13-1. J Cell Biol 158:577–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ou CY, Shen K (2010) Setting up presynaptic structures at specific positions. Curr Opin Neurobiol 20:489–493

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ou CY, Poon VY, Maeder CI, Watanabe S, Lehrman EK et al (2010) Two cyclin-dependent kinase pathways are essential for polarized trafficking of presynaptic components. Cell 141:846–858

    CAS  PubMed Central  PubMed  Google Scholar 

  • Owald D, Sigrist SJ (2009) Assembling the presynaptic active zone. Curr Opin Neurobiol 19:311–318

    CAS  PubMed  Google Scholar 

  • Owald D, Fouquet W, Schmidt M, Wichmann C, Mertel S et al (2010) A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J Cell Biol 188:565–579

    CAS  PubMed Central  PubMed  Google Scholar 

  • Owald D, Khorramshahi O, Gupta VK, Banovic D, Depner H et al (2012) Cooperation of Syd-1 with Neurexin synchronizes pre- with postsynaptic assembly. Nat Neurosci 15:1219–1226

    CAS  PubMed  Google Scholar 

  • Pack-Chung E, Kurshan PT, Dickman DK, Schwarz TL (2007) A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat Neurosci 10:980–989

    CAS  PubMed  Google Scholar 

  • Patel MR, Lehrman EK, Poon VY, Crump JG, Zhen M et al (2006) Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat Neurosci 9:1488–1498

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pfenninger K, Sandri C, Akert K, Eugster CH (1969) Contribution to the problem of structural organization of the presynaptic area. Brain Res 12:10–18

    CAS  PubMed  Google Scholar 

  • Phillips GR, Huang JK, Wang Y, Tanaka H, Shapiro L et al (2001) The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 32:63–77

    CAS  PubMed  Google Scholar 

  • Prange O, Wong TP, Gerrow K, Wang YT, El-Husseini A (2004) A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc Natl Acad Sci U S A 101:13915–13920

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reissner C, Runkel F, Missler M (2013) Neurexins. Genome Biol 14:213

    PubMed Central  PubMed  Google Scholar 

  • Sabo SL, Gomes RA, McAllister AK (2006) Formation of presynaptic terminals at predefined sites along axons. J Neurosci 26:10813–10825

    CAS  PubMed  Google Scholar 

  • Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657–669

    CAS  PubMed  Google Scholar 

  • Schoch S, Gundelfinger ED (2006) Molecular organization of the presynaptic active zone. Cell Tissue Res 326:379–391

    CAS  PubMed  Google Scholar 

  • Shapira M, Zhai RG, Dresbach T, Bresler T, Torres VI et al (2003) Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 38:237–252

    CAS  PubMed  Google Scholar 

  • Shen K, Scheiffele P (2010) Genetics and cell biology of building specific synaptic connectivity. Annu Rev Neurosci 33:473–507

    CAS  PubMed Central  PubMed  Google Scholar 

  • Siksou L, Rostaing P, Lechaire JP, Boudier T, Ohtsuka T et al (2007) Three-dimensional architecture of presynaptic terminal cytomatrix. J Neurosci 27:6868–6877

    CAS  PubMed  Google Scholar 

  • Siksou L, Varoqueaux F, Pascual O, Triller A, Brose N, Marty S (2009) A common molecular basis for membrane docking and functional priming of synaptic vesicles. Eur J Neurosci 30:49–56

    PubMed  Google Scholar 

  • Siksou L, Triller A, Marty S (2011) Ultrastructural organization of presynaptic terminals. Curr Opin Neurobiol 21:261–268

    CAS  PubMed  Google Scholar 

  • Song YS, Kim E (2013) Presynaptic proteoglycans: sweet organizers of synapse development. Neuron 79:609–611

    CAS  PubMed  Google Scholar 

  • Stan A, Pielarski KN, Brigadski T, Wittenmayer N, Fedorchenko O et al (2010) Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation. Proc Natl Acad Sci U S A 107:11116–11121

    CAS  PubMed Central  PubMed  Google Scholar 

  • Su Q, Cai Q, Gerwin C, Smith CL, Sheng ZH (2004) Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol 6:941–953

    CAS  PubMed  Google Scholar 

  • Sudhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455:903–911

    PubMed Central  PubMed  Google Scholar 

  • Sudhof TC (2012) The presynaptic active zone. Neuron 75:11–25

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sudhof TC (2013) Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80:675–690

    CAS  PubMed  Google Scholar 

  • Takahashi H, Craig AM (2013) Protein tyrosine phosphatases PTPδ, PTPσ, and LAR: presynaptic hubs for synapse organization. Trends Neurosci 36:522–534

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi H, Arstikaitis P, Prasad T, Bartlett TE, Wang YT et al (2011) Postsynaptic TrkC and presynaptic PTPσ function as a bidirectional excitatory synaptic organizing complex. Neuron 69:287–303

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi H, Katayama K, Sohya K, Miyamoto H, Prasad T, Matsumoto Y, Ota M, Yasuda H, Tsumoto T, Aruga J, Craig AM (2012) Selective control of inhibitory synapse development by Slitrk3-PTPδ trans-synaptic interaction. Nat Neurosci 15:389–398

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takao-Rikitsu E, Mochida S, Inoue E, Deguchi-Tawarada M, Inoue M et al (2004) Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release. J Cell Biol 164:301–311

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tao-Cheng JH (2007) Ultrastructural localization of active zone and synaptic vesicle proteins in a preassembled multi-vesicle transport aggregate. Neuroscience 150:575–584

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tatsuoka H, Reese TS (1989) New structural features of synapses in the anteroventral cochlear nucleus prepared by direct freezing and freeze-substitution. J Comp Neurol 290:343–357

    CAS  PubMed  Google Scholar 

  • tom Dieck S, Sanmarti-Vila L, Langnaese K, Richter K, Kindler S et al (1998) Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J Cell Biol 142:499–509

    CAS  PubMed  Google Scholar 

  • Triller A, Korn H (1985) Activity-dependent deformations of presynaptic grids at central synapses. J Neurocytol 14:177–192

    CAS  PubMed  Google Scholar 

  • Tsuriel S, Fisher A, Wittenmayer N, Dresbach T, Garner CC, Ziv NE (2009) Exchange and redistribution dynamics of the cytoskeleton of the active zone molecule bassoon. J Neurosci 29:351–358

    CAS  PubMed Central  PubMed  Google Scholar 

  • Uemura T, Lee SJ, Yasumura M, Takeuchi T, Yoshida T et al (2010) Trans-synaptic interaction of GluRδ2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141:1068–1079

    CAS  PubMed  Google Scholar 

  • Valnegri P, Montrasio C, Brambilla D, Ko J, Passafaro M, Sala C (2011) The X-linked intellectual disability protein IL1RAPL1 regulates excitatory synapse formation by binding PTPδ and RhoGAP2. Hum Mol Genet 20:4797–4809

    CAS  PubMed Central  PubMed  Google Scholar 

  • Varoqueaux F, Sigler A, Rhee JS, Brose N, Enk C et al (2002) Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci U S A 99:9037–9042

    CAS  PubMed Central  PubMed  Google Scholar 

  • Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M et al (2006) Neuroligins determine synapse maturation and function. Neuron 51:741–754

    CAS  PubMed  Google Scholar 

  • Vaughn JE (1989) Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255–285

    CAS  PubMed  Google Scholar 

  • Waites CL, Leal-Ortiz SA, Okerlund N, Dalke H, Fejtova A et al (2013) Bassoon and Piccolo maintain synapse integrity by regulating protein ubiquitination and degradation. EMBO J 32:954–969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, Goodman CS (2000) Highwire regulates synaptic growth in Drosophila. Neuron 26:313–329

    CAS  PubMed  Google Scholar 

  • Wang Y, Okamoto M, Schmitz F, Hofmann K, Sudhof TC (1997) Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388:593–598

    CAS  PubMed  Google Scholar 

  • Wang X, Kibschull M, Laue MM, Lichte B, Petrasch-Parwez E, Kilimann MW (1999) Aczonin, a 550-kD putative scaffolding protein of presynaptic active zones, shares homology regions with Rim and Bassoon and binds profilin. J Cell Biol 147:151–162

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang X, Hu B, Zieba A, Neumann NG, Kasper-Sonnenberg M et al (2009) A protein interaction node at the neurotransmitter release site: domains of Aczonin/Piccolo, Bassoon, CAST, and rim converge on the N-terminal domain of Munc13-1. J Neurosci 29:12584–12596

    CAS  PubMed  Google Scholar 

  • Wentzel C, Sommer JE, Nair R, Stiefvater A, Sibarita JB, Scheiffele P (2013) mSYD1A, a mammalian synapse-defective-1 protein, regulates synaptogenic signaling and vesicle docking. Neuron 78:1012–1023

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wittenmayer N, Korber C, Liu H, Kremer T, Varoqueaux F et al (2009) Postsynaptic Neuroligin1 regulates presynaptic maturation. Proc Natl Acad Sci U S A 106:13564–13569

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wong MY, Zhou C, Shakiryanova D, Lloyd TE, Deitcher DL, Levitan ES (2012) Neuropeptide delivery to synapses by long-range vesicle circulation and sporadic capture. Cell 148:1029–1038

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu YE, Huo L, Maeder CI, Feng W, Shen K (2013) The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses. Neuron 78:994–1011

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yan D, Wu Z, Chisholm AD, Jin Y (2009) The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138:1005–1018

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yim YS, Kwon Y, Nam J, Yoon HI, Lee K et al (2013) Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases. Proc Natl Acad Sci U S A 110:4057–4062

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoshida T, Yasumura M, Uemura T, Lee SJ, Ra M et al (2011) IL-1 receptor accessory protein-like 1 associated with mental retardation and autism mediates synapse formation by trans-synaptic interaction with protein tyrosine phosphatase δ. J Neurosci 31:13485–13499

    CAS  PubMed  Google Scholar 

  • Yoshida T, Shiroshima T, Lee SJ, Yasumura M, Uemura T et al (2012) Interleukin-1 receptor accessory protein organizes neuronal synaptogenesis as a cell adhesion molecule. J Neurosci 32:2588–2600

    CAS  PubMed  Google Scholar 

  • Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED et al (2001) Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29:131–143

    CAS  PubMed  Google Scholar 

  • Zhen M, Huang X, Bamber B, Jin Y (2000) Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26:331–343

    CAS  PubMed  Google Scholar 

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Correspondence to Thomas Dresbach .

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Dresbach, T. (2015). Active Zone Assembly. In: Mochida, S. (eds) Presynaptic Terminals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55166-9_2

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