Saleeba C, Dempsey B, Le S, Goodchild A, McMullan S. A Student’s guide to neural circuit tracing. Front Neurosci. 2019;13:1–19.
Google Scholar
Herculano-Houzel S. The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci. 2009;3:31.
PubMed
PubMed Central
Google Scholar
Colón-Ramos DA. Synapse formation in developing neural circuits. Curr Top Dev Biol. 2009;87(09):53–79.
PubMed
Google Scholar
Comer JD, Alvarez S, Butler SJ, Kaltschmidt JA. Commissural axon guidance in the developing spinal cord: from Cajal to the present day. Neural Dev. 2019;14(1):1–16.
CAS
Google Scholar
Chia PH, Li P, Shen K. Cell biology in neuroscience: cellular and molecular mechanisms underlying presynapse formation. J Cell Biol. 2013;203(1):11–22.
CAS
PubMed
PubMed Central
Google Scholar
Jessell TM, Kandel ER. Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Cell. 1993;72(1):1–30.
PubMed
Google Scholar
Südhof TC. Towards an understanding of synapse formation. Neuron. 2018;100(2):276–93.
PubMed
PubMed Central
Google Scholar
Cammarata GM, Bearce EA, Lowery LA. Cytoskeletal social networking in the growth cone: how +TIPs mediate microtubule-actin cross-linking to drive axon outgrowth and guidance. Cytoskeleton. 2016;73(9):461–76.
CAS
PubMed
Google Scholar
Lowery LA, Van Vactor D. The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol. 2009;10(5):332–43.
CAS
PubMed
PubMed Central
Google Scholar
Jin Y, Garner CC. Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol. 2008;24:237–62.
CAS
PubMed
Google Scholar
Ackermann F, Waites CL, Garner CC. Presynaptic active zones in invertebrates and vertebrates. EMBO Rep. 2015;16(8):923–38.
CAS
PubMed
PubMed Central
Google Scholar
Südhof TC. The presynaptic active zone. Neuron. 2012;75(1):11–25.
PubMed
PubMed Central
Google Scholar
Zhai RG, Bellen HJ. The architecture of the active zone in the presynaptic nerve terminal. Physiology. 2004;19(5):262–70.
PubMed
Google Scholar
Ehmann N, Owald D, Kittel RJ. Drosophila active zones: from molecules to behaviour. Neurosci Res. 2018;127:14–24Available from:. https://doi.org/10.1016/j.neures.2017.11.015.
Article
CAS
PubMed
Google Scholar
Sheng M, Kim E. The postsynaptic organization of synapses. Cold Spring Harb Perspect Biol. 2011;3(12):a005678.
Scannevin RH, Huganir RL. Postsynaptic organisation and regulation of excitatory synapses. Nat Rev Neurosci. 2000;1(2):133–41.
CAS
PubMed
Google Scholar
Sheng M, Kim MJ. Postsynaptic signaling and plasticity mechanisms. Science (80- ). 2002;298(5594):776–80.
CAS
Google Scholar
Van Vactor D, Sigrist SJ. Presynaptic morphogenesis, active zone organization and structural plasticity in drosophila. Curr Opin Neurobiol. 2017;43:119–29 [cited 2020 Feb 10]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28388491.
PubMed
PubMed Central
Google Scholar
Rushton E, Rohrbough J, Broadie K. Presynaptic secretion of mind-the-gap organizes the synaptic extracellular matrix-integrin interface and postsynaptic environments. Dev Dyn. 2009;238(3):554–71.
CAS
PubMed
PubMed Central
Google Scholar
Collins CA, DiAntonio A. Synaptic development: insights from drosophila. Curr Opin Neurobiol. 2007;17(1):35–42.
CAS
PubMed
Google Scholar
Kohsaka H, Okusawa S, Itakura Y, Fushiki A, Nose A. Development of larval motor circuits in drosophila. Dev Growth Differ. 2012;54(3):408–19.
CAS
PubMed
Google Scholar
Kohsaka H, Guertin PA, Nose A. Neural circuits underlying Fly larval locomotion. Curr Pharm Des. 2017;23(12):1722–33.
CAS
PubMed
PubMed Central
Google Scholar
Keshishian H, Kim YS. Orchestrating development and function: retrograde BMP signaling in the drosophila nervous system. Trends Neurosci. 2004;27(3):143–7.
CAS
PubMed
Google Scholar
Bayat V, Jaiswal M, Bellen HJ. The BMP signaling pathway at the drosophila neuromuscular junction and its links to neurodegenerative diseases. Curr Opin Neurobiol. 2011;21(1):182–8.
CAS
PubMed
Google Scholar
Speese SD, Budnik V. Wnts: up-and-coming at the synapse. Trends Neurosci. 2007;30(6):268–75.
CAS
PubMed
PubMed Central
Google Scholar
Koles K, Budnik V. Wnt signaling in neuromuscular junction development. Cold Spring Harb Perspect Biol. 2012;4(6):1–22.
Google Scholar
Packard M, Koo ES, Gorczyca M, Sharpe J, Cumberledge S, Budnik V. The drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell. 2002;111(3):319–30.
CAS
PubMed
PubMed Central
Google Scholar
Sen A, Yokokura T, Kankel MW, Dimlich DN, Manent J, Sanyal S, et al. Modeling spinal muscular atrophy in drosophila links Smn to FGF signaling. J Cell Biol. 2011;192(3):481–95.
CAS
PubMed
PubMed Central
Google Scholar
Han KA, Jeon S, Um JW, Ko J. Emergent synapse organizers: LAR-RPTPs and their companions. Int Rev Cell Mol Biol. 2016;324:39–65.
CAS
PubMed
Google Scholar
Um JW, Ko J. LAR-RPTPs: synaptic adhesion molecules that shape synapse development. Trends Cell Biol. 2013;23(10):465–75.
CAS
PubMed
Google Scholar
Johnson KG, Tenney AP, Ghose A, Duckworth AM, Higashi ME, Parfitt K, et al. The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron. 2006;49(4):517–31.
CAS
PubMed
Google Scholar
Dunah AW, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, et al. LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci. 2005;8(4):458–67.
CAS
PubMed
Google Scholar
Petanjek Z, Judaš M, Šimić G, Rašin MR, Uylings HBM, Rakic P, et al. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A. 2011;108(32):13281–6.
CAS
PubMed
PubMed Central
Google Scholar
Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science (80- ). 2001;294(5544):1030–8.
CAS
Google Scholar
Bailey CH, Kandel ER, Harris KM. Structural components of synaptic plasticity and memory consolidation. Cold Spring Harb Perspect Biol. 2015;7(7):1–29.
CAS
Google Scholar
Thalhammer A, Cingolani LA. Cell adhesion and homeostatic synaptic plasticity. Neuropharmacology. 2014;78:23–30.
CAS
PubMed
Google Scholar
Giagtzoglou N, Ly C V., Bellen HJ. Cell adhesion, the backbone of the synapse: “vertebrate” and “invertebrate” perspectives. Cold Spring Harb Perspect Biol. 2009;1(4):a003079.
Hagler DJ, Goda Y. Synaptic adhesion: the building blocks of memory? Neuron. 1998;20(6):1059–62.
CAS
PubMed
Google Scholar
Lai KO, Ip NY. Synapse development and plasticity: roles of ephrin/Eph receptor signaling. Curr Opin Neurobiol. 2009;19(3):275–83.
CAS
PubMed
Google Scholar
Singh A, Winterbottom E, Daar IO. Eph/ephrin signaling in cell-cell and cell-substrate adhesion. Front Biosci. 2012;17(2):473–97.
CAS
Google Scholar
Sun MK, Xie W. Cell adhesion molecules in drosophila synapse development and function. Sci China Life Sci. 2012;55(1):20–6.
CAS
PubMed
Google Scholar
Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, et al. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science (80- ). 2002;297(5586):1525–31.
CAS
Google Scholar
Fogel AI, Akins MR, Krupp AJ, Stagi M, Stein V, Biederer T. SynCAMs organize synapses through heterophilic adhesion. J Neurosci. 2007;27(46):12516–30.
CAS
PubMed
PubMed Central
Google Scholar
Frei JA, Andermatt I, Gesemann M, Stoeckli ET. The SynCAM synaptic cell adhesion molecules are involved in sensory axon pathfinding by regulating axon-axon contacts. J Cell Sci. 2014;127(24):5288–302.
PubMed
Google Scholar
Brasch J, Katsamba PS, Harrison OJ, Ahlsén G, Troyanovsky RB, Indra I, et al. Homophilic and Heterophilic interactions of type II Cadherins identify specificity groups underlying cell-adhesive behavior. Cell Rep. 2018;23(6):1840–52.
CAS
PubMed
PubMed Central
Google Scholar
Ounkomol C, Yamada S, Heinrich V. Single-cell adhesion tests against functionalized microspheres arrayed on AFM cantilevers confirm heterophilic E- and N-cadherin binding. Biophys J. 2010;99(12):L100–2.
CAS
PubMed
PubMed Central
Google Scholar
Prakasam AK, Maruthamuthu V, Leckband DE. Similarities between heterophilic and homophilic cadherin adhesion. Proc Natl Acad Sci U S A. 2006;103(42):15434–9.
CAS
PubMed
PubMed Central
Google Scholar
Basu R, Taylor MR, Williams ME. The classic cadherins in synaptic specificity. Cell Adh Migr. 2015;9(3):193–201.
CAS
PubMed
PubMed Central
Google Scholar
Lüthi A, Laurent JP, Figurovt A, Mullert D, Schachnert M. Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature. 1994;372(6508):777–9.
PubMed
Google Scholar
Muller D, Wang C, Skibo G, Toni N, Cremer H, Calaora V, et al. PSA-NCAM is required for activity-induced synaptic plasticity. Neuron. 1996;17(3):413–22.
CAS
PubMed
Google Scholar
Schuster CM, Davis GW, Fetter RD, Goodman CS. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron. 1996;17(4):641–54.
CAS
PubMed
Google Scholar
Davis GW, Schuster CM, Goodman CS. Genetic analysis of the mechanisms controlling target selection: target-derived Fasciclin II regulates the pattern of synapse formation. Neuron. 1997;19(3):561–73.
CAS
PubMed
Google Scholar
Beumer K, Matthies HJG, Bradshaw A, Broadie K. Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development. Development. 2002;129(14):3381–91.
CAS
PubMed
Google Scholar
Agarwala KL, Ganesh S, Amano K, Suzuki T, Yamakawa K. DSCAM, a highly conserved gene in mammals, expressed in differentiating mouse brain. Biochem Biophys Res Commun. 2001;281(3):697–705.
CAS
PubMed
Google Scholar
Agarwala KL, Nakamura S, Tsutsumi Y, Yamakawa K. Down syndrome cell adhesion molecule DSCAM mediates homophilic intercellular adhesion. Mol Brain Res. 2000;79(1–2):118–26.
CAS
PubMed
Google Scholar
Suzuki SC, Takeichi M. Cadherins in neuronal morphogenesis and function. Dev Growth Differ. 2008;50(Suppl 1):S119–30.
CAS
PubMed
Google Scholar
Hirano S, Takeichi M. Cadherins in brain morphogenesis and wiring. Physiol Rev. 2012;92(2):597–634.
CAS
PubMed
Google Scholar
Brigidi GS, Bamji SX. Cadherin-catenin adhesion complexes at the synapse. Curr Opin Neurobiol. 2011;21(2):208–14.
CAS
PubMed
Google Scholar
Seong E, Yuan L, Arikkath J. Cadherins and catenins in dendrite and synapse morphogenesis. Cell Adh Migr. 2015;9(3):202–13.
CAS
PubMed
PubMed Central
Google Scholar
Yamagata M, Herman JP, Sanes JR. Lamina-specific expression of adhesion molecules in developing chick optic tectum. J Neurosci. 1995;15(6):4556–71.
CAS
PubMed
PubMed Central
Google Scholar
Uchida N, Honjo Y, Johnson KR, Wheelock MJ, Takeichi M. The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J Cell Biol. 1996;135(3):767–79.
CAS
PubMed
Google Scholar
Yam PT, Pincus Z, Gupta GD, Bashkurov M, Charron F, Pelletier L, et al. N-cadherin relocalizes from the periphery to the center of the synapse after transient synaptic stimulation in hippocampal neurons. PLoS One. 2013;8(11):1–12.
Google Scholar
Vitureira N, Letellier M, White IJ, Goda Y. Differential control of presynaptic efficacy by postsynaptic N-cadherin and β-catenin. Nat Neurosci. 2012;15(1):81–9.
CAS
Google Scholar
Jüngling K, Eulenburg V, Moore R, Kemler R, Lessmann V, Gottmann K. N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons. J Neurosci. 2006;26(26):6968–78.
PubMed
PubMed Central
Google Scholar
Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M. Cadherin regulates dendritic spine morphogenesis. Neuron. 2002;35(1):77–89.
CAS
PubMed
Google Scholar
Abe K, Chisaka O, Van Roy F, Takeichi M. Stability of dendritic spines and synaptic contacts is controlled by αN-catenin. Nat Neurosci. 2004;7(4):357–63.
CAS
PubMed
Google Scholar
Mendez P, De Roo M, Poglia L, Klauser P, Muller D. N-cadherin mediates plasticity-induced long-term spine stabilization. J Cell Biol. 2010;189(3):589–600.
CAS
PubMed
PubMed Central
Google Scholar
Okamura K, Tanaka H, Yagita Y, Saeki Y, Taguchi A, Hiraoka Y, et al. Cadherin activity is required for activity-induced spine remodeling. J Cell Biol. 2004;167(5):961–72.
CAS
PubMed
PubMed Central
Google Scholar
Bozdagi O, Bin WX, Nikitczuk JS, Anderson TR, Bloss EB, Radice GL, et al. Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J Neurosci. 2010;30(30):9984–9.
CAS
PubMed
PubMed Central
Google Scholar
Bozdagi O, Shan W, Tanaka H, Benson DL, Huntley GW. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron. 2000;28(1):245–59.
CAS
PubMed
Google Scholar
Ashley J, Packard M, Ataman B, Budnik V. Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/mint. J Neurosci. 2005;25(25):5943–55.
CAS
PubMed
PubMed Central
Google Scholar
Yu H-H, Yang JS, Wang J, Huang Y, Lee T. Endodomain diversity in the drosophila Dscam and its roles in neuronal morphogenesis. J Neurosci. 2009;29(6):1904–14.
CAS
PubMed
PubMed Central
Google Scholar
Wang J, Zugates CT, Liang IH, Lee CHJ, Lee T. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron. 2002;33(4):559–71.
CAS
PubMed
Google Scholar
Hutchinson KM, Vonhoff F, Duch C. Dscam1 is required for Normal dendrite growth and branching but not for dendritic spacing in drosophila Motoneurons. J Neurosci. 2014;34(5):1924–31.
CAS
PubMed
PubMed Central
Google Scholar
Spring AM, Brusich DJ, Frank CA. C-terminal Src kinase gates homeostatic synaptic plasticity and regulates Fasciclin II expression at the drosophila neuromuscular junction. PLoS Genet. 2016;12(2):1–31.
Google Scholar
Kohsaka H, Takasu E, Nose A. In vivo induction of postsynaptic molecular assembly by the cell adhesion molecule Fasciclin2. J Cell Biol. 2007;179(6):1289–300.
CAS
PubMed
PubMed Central
Google Scholar
Mayford M, Barzilai A, Keller F, Schacher S, Kandel ER. Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in aplysia. Science (80- ). 1992;256(5057):638–44.
CAS
Google Scholar
Knight D, Xie W, Boulianne GL. Neurexins and neuroligins: recent insights from invertebrates. Mol Neurobiol. 2011;44(3):426–40.
CAS
PubMed
PubMed Central
Google Scholar
Craig AM, Kang Y. Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol. 2007;17(1):43–52.
CAS
PubMed
PubMed Central
Google Scholar
Bottos A, Rissone A, Bussolino F, Arese M. Neurexins and neuroligins: synapses look out of the nervous system. Cell Mol Life Sci. 2011;68(16):2655–66.
CAS
PubMed
Google Scholar
Südhof TC. Neuroligins and neurexins link synaptic function to cognitive disease. Nature. 2008;455(7215):903–11.
PubMed
PubMed Central
Google Scholar
Mosca TJ. On the Teneurin track: a new synaptic organization molecule emerges. Front Cell Neurosci. 2015;9:1–14.
Google Scholar
Tucker RP, Chiquet-Ehrismann R. Teneurins: a conserved family of transmembrane proteins involved in intercellular signaling during development. Dev Biol. 2006;290(2):237–45.
CAS
PubMed
Google Scholar
Zinn K, Özkan E. Neural immunoglobulin superfamily interaction networks. Curr Opin Neurobiol. 2017;45:99–105.
CAS
PubMed
PubMed Central
Google Scholar
Morey M. Dpr-DIP matching expression in drosophila synaptic pairs. Fly (Austin). 2017;11(1):19–26.
Google Scholar
Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell. 2004;119(7):1013–26.
CAS
PubMed
PubMed Central
Google Scholar
Scheiffele P, Fan J, Choih J, Fetter R, Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell. 2000;101(6):657–69.
CAS
PubMed
Google Scholar
Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K, et al. Neuroligins determine synapse maturation and function. Neuron. 2006;51(6):741–54.
CAS
PubMed
Google Scholar
Li J, Ashley J, Budnik V, Bhat MA. Crucial role of drosophila Neurexin in proper active zone apposition to postsynaptic densities, synaptic growth, and synaptic transmission. Neuron. 2007;55(5):741–55.
CAS
PubMed
PubMed Central
Google Scholar
Chen K, Gracheva EO, Yu SC, Sheng Q, Richmond J, Featherstone DE. Neurexin in embryonic drosophila neuromuscular junctions. PLoS One. 2010;5(6):e11115.
Etherton MR, Blaiss CA, Powell CM, Südhof TC. Mouse neurexin-1α deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc Natl Acad Sci U S A. 2009;106(42):17998–8003.
CAS
PubMed
PubMed Central
Google Scholar
Chen LY, Jiang M, Zhang B, Gokce O, Südhof TC. Conditional deletion of all Neurexins defines diversity of essential synaptic organizer functions for Neurexins. Neuron. 2017;94(3):611–625.e4.
CAS
PubMed
PubMed Central
Google Scholar
Owald D, Khorramshahi O, Gupta VK, Banovic D, Depner H, Fouquet W, et al. Cooperation of Syd-1 with Neurexin synchronizes pre- with postsynaptic assembly. Nat Neurosci. 2012;15(9):1219–26.
CAS
PubMed
Google Scholar
Banerjee S, Venkatesan A, Bhat MA. Neurexin, Neuroligin and wishful thinking coordinate synaptic cytoarchitecture and growth at neuromuscular junctions. Mol Cell Neurosci. 2017;78:9–24.
CAS
PubMed
Google Scholar
Chih B, Engelman H, Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science (80- ). 2005;307(5713):1324–8.
CAS
Google Scholar
Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR, et al. Activity-dependent validation of excitatory versus inhibitory synapses by Neuroligin-1 versus Neuroligin-2. Neuron. 2007;54(6):919–31.
CAS
PubMed
PubMed Central
Google Scholar
Chen Y-C, Lin YQ, Banerjee S, Venken K, Li J, Ismat A, et al. Drosophila Neuroligin 2 is required Presynaptically and Postsynaptically for proper synaptic differentiation and synaptic transmission. J Neurosci. 2012;32(45):16018–30.
CAS
PubMed
PubMed Central
Google Scholar
Banovic D, Khorramshahi O, Owald D, Wichmann C, Riedt T, Fouquet W, et al. Drosophila Neuroligin 1 promotes growth and postsynaptic differentiation at glutamatergic neuromuscular junctions. Neuron. 2010;66(5):724–38.
CAS
PubMed
Google Scholar
Xing G, Li M, Sun Y, Rui M, Zhuang Y, Lv H, et al. Neurexin–neuroligin 1 regulates synaptic morphology and functions via the WAVE regulatory complex in drosophila neuromuscular junction. Elife. 2018;7:1–23.
Google Scholar
Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, Lengyel JA, et al. A drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell. 1996;87(6):1059–68.
CAS
PubMed
Google Scholar
Bellen HJ, Lu Y, Beckstead R, Bhat MA. Neurexin IV, caspr and paranodin - novel members of the neurexin family: encounters of axons and glia. Trends Neurosci. 1998;21(10):444–9.
CAS
PubMed
Google Scholar
Peles E, Nativ M, Lustig M, Grumet M, Schilling J, Martinez R, et al. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J. 1997;16(5):978–88.
CAS
PubMed
PubMed Central
Google Scholar
Böhme MA, Beis C, Reddy-Alla S, Reynolds E, Mampell MM, Grasskamp AT, et al. Active zone scaffolds differentially accumulate Unc13 isoforms to tune Ca2+ channel-vesicle coupling. Nat Neurosci. 2016;19(10):1311–20.
PubMed
Google Scholar
Maruyama IN, Brenner S. A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc Natl Acad Sci. 1991;88(13):5729–33.
CAS
PubMed
Google Scholar
Lai Y, Choi UB, Leitz J, Rhee HJ, Lee C, Altas B, et al. Molecular mechanisms of synaptic vesicle priming by Munc13 and Munc18. Neuron. 2017;95(3):591–607.e10.
CAS
PubMed
PubMed Central
Google Scholar
Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS. Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron. 2002;33(3):411–24.
CAS
PubMed
Google Scholar
Zweier C, de Jong EK, Zweier M, Orrico A, Ousager LB, Collins AL, et al. CNTNAP2 and NRXN1 are mutated in autosomal-recessive Pitt-Hopkins-like mental retardation and determine the level of a common synaptic protein in drosophila. Am J Hum Genet. 2009;85(5):655–66.
CAS
PubMed
PubMed Central
Google Scholar
McNeill EM, Warinner C, Alkins S, Taylor A, Heggeness H, DeLuca TF, et al. The conserved microRNA miR-34 regulates synaptogenesis via coordination of distinct mechanisms in presynaptic and postsynaptic cells. Nat Commun. 2020;11(1):1092.
CAS
PubMed
PubMed Central
Google Scholar
Leamey CA, Sawatari A. The teneurins: new players in the generation of visual topography. Semin Cell Dev Biol. 2014;35:173–9.
CAS
PubMed
Google Scholar
Mosca TJ, Hong W, Dani VS, Favaloro V, Luo L. Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature. 2012;484(7393):237–41.
CAS
PubMed
PubMed Central
Google Scholar
Ataman B, Ashley J, Gorczyca M, Ramachandran P, Fouquet W, Sigrist SJ, et al. Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling. Neuron. 2008;57:705–18.
CAS
PubMed
PubMed Central
Google Scholar
Piccioli ZD, Littleton JT. Retrograde BMP signaling modulates rapid activity-dependent synaptic growth via presynaptic LIM kinase regulation of cofilin. J Neurosci. 2014;34(12):4371–81.
PubMed
PubMed Central
Google Scholar
Berke B, Wittnam J, McNeill E, Van Vactor DL, Keshishian H. Retrograde BMP signaling at the synapse: a permissive signal for synapse maturation and activity-dependent plasticity. J Neurosci. 2013;33(45):17937–50.
CAS
PubMed
PubMed Central
Google Scholar
Zito K, Parnas D, Fetter RD, Isacoff EY, Goodman CS. Watching a synapse grow: noninvasive confocal imaging of synaptic growth in drosophila. Neuron. 1999;22(4):719–29.
CAS
PubMed
Google Scholar
Fuentes-Medel Y, Logan MA, Ashley J, Ataman B, Budnik V, Freeman MR. Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. PLoS Biol. 2009;7(8):e1000184.
PubMed
PubMed Central
Google Scholar
Johansen J, Halpern M, Johansen K, Keshishian H. Stereotypic morphology of glutamatergic synapses on identified muscle cells of drosophila larvae. J Neurosci. 1989;9(2):710–25.
CAS
PubMed
PubMed Central
Google Scholar
Hoang B, Chiba A. Single-cell analysis of drosophila larval neuromuscular synapses. Dev Biol. 2001;229(1):55–70.
CAS
PubMed
Google Scholar
Ataman B, Ashley J, Gorczyca D, Gorczyca M, Mathew D, Wichmann C, et al. Nuclear trafficking of drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc Natl Acad Sci U S A. 2006;103(20):7841–6.
CAS
PubMed
PubMed Central
Google Scholar
Vasin A, Zueva L, Torrez C, Volfson D, Littleton JT, Bykhovskaia M. Synapsin regulates activity-dependent outgrowth of synaptic boutons at the drosophila neuromuscular junction. J Neurosci. 2014;34(32):10554–63.
PubMed
PubMed Central
Google Scholar
Kaufmann N, DeProto J, Ranjan R, Wan H, Van Vactor D. Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron. 2002;34(1):27–38.
CAS
PubMed
Google Scholar
Miller K, Chou VT, Van Vactor D. Liprin-α and assembly of the synaptic Cytomatrix. In: Reference module in neuroscience and biobehavioral psychology. Basel: Elsevier; 2017. p. 1–8.
Owald D, Fouquet W, Schmidt M, Wichmann C, Mertel S, Depner H, et al. A Syd-1 homologue regulates pre- and postsynaptic maturation in drosophila. J Cell Biol. 2010;188(4):565–79.
CAS
PubMed
PubMed Central
Google Scholar
Dai Y, Taru H, Deken SL, Grill B, Ackley B, Nonet ML, et al. SYD-2 Liprin-α organizes presynaptic active zone formation through ELKS. Nature Neuroscience; 2006;9(12):1479–87.
Patel MR, Lehrman EK, Poon VY, Crump JG, Zhen M, Bargmann CI, et al. Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat Neurosci. 2006;9(12):1488–98.
CAS
PubMed
PubMed Central
Google Scholar
Wentzel C, Sommer JE, Nair R, Stiefvater A, Sibarita JB, Scheiffele P. MSYD1A, a mammalian synapse-Defective-1 protein, regulates Synaptogenic signaling and vesicle docking. Neuron. 2013;78(6):1012–23.
CAS
PubMed
PubMed Central
Google Scholar
Phillips GR, Huang JK, Wang Y, Tanaka H, Shapiro L, Zhang W, et al. The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron. 2001;32(1):63–77.
CAS
PubMed
Google Scholar
Chakrabarti R, Wichmann C. Nanomachinery organizing release at neuronal and ribbon synapses. Int J Mol Sci. 2019;20(9):23–32.
Google Scholar
Lenzi D, Von Gersdorff H. Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines. BioEssays. 2001;23(9):831–40.
CAS
PubMed
Google Scholar
Muresan V, Lyass A, Schnapp BJ. The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J Neurosci. 1999;19(3):1027–37.
CAS
PubMed
PubMed Central
Google Scholar
Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ. The architecture of active zone material at the frog’s neuromuscular junction. Nature. 2001;409(6819):479–84.
CAS
PubMed
Google Scholar
Jiao W, Masich S, Franzén O, Shupliakov O. Two pools of vesicles associated with the presynaptic cytosolic projection in drosophila neuromuscular junctions. J Struct Biol. 2010;172(3):389–94.
PubMed
Google Scholar
Goldstein AYN, Wang X, Schwarz TL. Axonal transport and the delivery of pre-synaptic components. Curr Opin Neurobiol. 2008;18(5):495–503.
CAS
PubMed
PubMed Central
Google Scholar
Maeder CI, Shen K, Hoogenraad CC. Axon and dendritic trafficking. Curr Opin Neurobiol. 2014;27:165–70.
CAS
PubMed
Google Scholar
Pack-Chung E, Kurshan PT, Dickman DK, Schwarz TL. A drosophila kinesin required for synaptic Bouton formation and synaptic vesicle transport. Nat Neurosci. 2007;10(8):980–9.
CAS
PubMed
Google Scholar
Pilling AD, Horiuchi D, Lively CM, Saxton WM. Kinesin-1 and dynein are the primary Motors for Fast Transport of mitochondria in drosophila motor axons. Mol Biol Cell. 2006;17(4):2057–68.
CAS
PubMed
PubMed Central
Google Scholar
Hurd DD, Saxton WM. Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in drosophila. Genetics. 1996;144(3):1075–85.
CAS
PubMed
PubMed Central
Google Scholar
Miller KE, Heidemann SR. What is slow axonal transport? Exp Cell Res. 2008;314(10):1981–90.
CAS
PubMed
Google Scholar
Popov S, Poo MM. Diffusional transport of macromolecules in developing nerve processes. J Neurosci. 1992;12(1):77–85.
CAS
PubMed
PubMed Central
Google Scholar
Shapira M, Zhai RG, Dresbach T, Bresler T, Torres VI, Gundelfinger ED, et al. Unitary assembly of presynaptic active zones from piccolo-bassoon transport vesicles. Neuron. 2003;38(2):237–52.
CAS
PubMed
Google Scholar
Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, et al. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron. 2001;29(1):131–43.
CAS
PubMed
Google Scholar
Tao-Cheng JH. Ultrastructural localization of active zone and synaptic vesicle proteins in a preassembled multi-vesicle transport aggregate. Neuroscience. 2007;150(3):575–84.
CAS
PubMed
PubMed Central
Google Scholar
Ziv NE, Garner CC. Cellular and molecular mechanisms of presynaptic assembly. Nat Rev Neurosci. 2004;5(5):385–99.
CAS
PubMed
Google Scholar
Waites CL, Craig AM, Garner CC. Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci. 2005;28(1):251–74.
CAS
PubMed
Google Scholar
Bury LAD, Sabo SL. Coordinated trafficking of synaptic vesicle and active zone proteins prior to synapse formation. Neural Dev. 2011;6(1):1–14.
Google Scholar
Wu YE, Huo L, Maeder CI, Feng W, Shen K. The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses. Neuron. 2013;78(6):994–1011.
CAS
PubMed
PubMed Central
Google Scholar
Lipton DM, Maeder CI, Shen K. Rapid assembly of presynaptic materials behind the growth cone in dopaminergic neurons is mediated by precise regulation of axonal transport. Cell Rep. 2018;24(10):2709–22.
CAS
PubMed
PubMed Central
Google Scholar
Petzoldt AG, Lützkendorf J, Sigrist SJ. Mechanisms controlling assembly and plasticity of presynaptic active zone scaffolds. Curr Opin Neurobiol. 2016;39:69–76.
CAS
PubMed
Google Scholar
Vukoja A, Rey U, Petzoldt AG, Ott C, Vollweiter D, Quentin C, et al. Presynaptic biogenesis requires axonal transport of lysosome-related vesicles. Neuron. 2018;99(6):1216–1232.e7.
CAS
PubMed
Google Scholar
Fouquet W, Owald D, Wichmann C, Mertel S, Depner H, Dyba M, et al. Maturation of active zone assembly by drosophila Bruchpilot. J Cell Biol. 2009;186(1):129–45.
CAS
PubMed
PubMed Central
Google Scholar
Zhen M, Jin Y. The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature. 1999;401(6751):371–5.
CAS
PubMed
Google Scholar
Astigarraga S, Hofmeyer K, Farajian R, Treisman JE. Three drosophila liprins interact to control synapse formation. J Neurosci. 2010;30(46):15358–68.
CAS
PubMed
PubMed Central
Google Scholar
Stigloher C, Zhan H, Zhen M, Richmond J, Bessereau J-L. The presynaptic dense projection of the Caenorhabiditis elegans cholinergic neuromuscular junction localizes synaptic vesicles at the active zone through SYD-2/Liprin and UNC-10/RIM-dependent interactions. J Neurosci. 2011;31(12):4388–96.
CAS
PubMed
PubMed Central
Google Scholar
Spinner MA, Walla DA, Herman TG. Drosophila syd-1 has rhogap activity that is required for presynaptic clustering of bruchpilot/elks but not neurexin-1. Genetics. 2018;208(2):705–16.
CAS
PubMed
Google Scholar
Li L, Tian X, Zhu M, Bulgari D, Böhme MA, Goettfert F, et al. Drosophila Syd-1, Liprin-α, and protein phosphatase 2A B’ subunit Wrd function in a linear pathway to prevent ectopic accumulation of synaptic materials in distal axons. J Neurosci. 2014;34(25):8474–87.
PubMed
PubMed Central
Google Scholar
Hallam SJ, Goncharov A, McEwen J, Baran R, Jin Y. SYD-1, a presynaptic protein with PDZ, C2 and rhoGAP-like domains, specifies axon identity in C. elegans. Nat Neurosci. 2002;5(11):1137–46.
CAS
PubMed
Google Scholar
Spangler SA, Hoogenraad CC. Liprin-alpha proteins: scaffold molecules for synapse maturation. Biochem Soc Trans. 2007;35(Pt 5):1278–82.
CAS
PubMed
Google Scholar
Serra-Pagès C, Medley QG, Tang M, Hart A, Streuli M. Liprins, a family of LAR transmembrane protein-tyrosine phosphatase- interacting proteins. J Biol Chem. 1998;273(25):15611–20.
PubMed
Google Scholar
Serra-Pagès C, Kedersha NL, Fazikas L, Medley Q, Debant A, Streuli M. The LAR transmembrane protein tyrosine phosphatase and a coiled-coil LAR-interacting protein co-localize at focal adhesions. EMBO J. 1995;14(12):2827–38.
PubMed
PubMed Central
Google Scholar
Brose N, Hofmann K, Hata Y, Sudhof TC. Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J Biol Chem. 1995;270(42):25273–80.
CAS
PubMed
Google Scholar
Augustin I, Rosenmund C, Südhof TC, Brose N. Munc13–1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature. 1999;400(6743):457–61.
CAS
PubMed
Google Scholar
Palfreyman MT, Jorgensen EM. Unc13 aligns SNAREs and Superprimes synaptic vesicles. Neuron. 2017;95(3):473–5.
CAS
PubMed
Google Scholar
Xu J, Camacho M, Xu Y, Esser V, Liu X, Trimbuch T, et al. Mechanistic insights into neurotransmitter release and presynaptic plasticity from the crystal structure of Munc13–1 C1C2BMUN. Elife. 2017;6:e22567.
Wang Y, Okamoto M, Schmitz F, Hofmann K, Südhof TC. Rim is a putative rab3 effector in regulating synaptic-vesicle fusion. Nature. 1997;388(6642):593–8.
CAS
PubMed
Google Scholar
Mittelstaedt T, Alvaréz-Baron E, Schoch S. RIM proteins and their role in synapse function. Biol Chem. 2010;391(6):599–606.
CAS
PubMed
Google Scholar
Lu J, Machius M, Dulubova I, Dai H, Südhof TC, Tomchick DR, et al. Structural basis for a Munc13–1 homodimer to Munc13–1/RIM heterodimer switch. PLoS Biol. 2006;4(7):1159–72.
CAS
Google Scholar
Deng L, Kaeser PS, Xu W, Südhof TC. RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of munc13. Neuron. 2011;69(2):317–31.
CAS
PubMed
PubMed Central
Google Scholar
Kaeser P. Pushing synaptic vesicles over the RIM. Cell Logist. 2011;1(3):106–10.
PubMed
PubMed Central
Google Scholar
Castillo PE, Schoch S, Schmitz F, Südhof TC, Malenka RC. RIM1α is required for presynaptic long-term potentiation. Nature. 2002;415(6869):327–30.
CAS
PubMed
Google Scholar
Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, et al. RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature. 2002;415(6869):321–6.
CAS
PubMed
Google Scholar
Graf ER, Valakh V, Wright CM, Wu C, Liu Z, Zhang YQ, et al. RIM promotes Calcium Channel accumulation at active zones of the drosophila neuromuscular junction. J Neurosci. 2012;32(47):16586–96.
CAS
PubMed
PubMed Central
Google Scholar
Han Y, Babai N, Kaeser P, Südhof TC, Schneggenburger R. RIM1 and RIM2 redundantly determine ca 2+ channel density and readily releasable pool size at a large hindbrain synapse. J Neurophysiol. 2015;113(1):255–63.
CAS
PubMed
Google Scholar
Kaeser PS, Deng L, Wang Y, Dulubova I, Liu X, Rizo J, et al. RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell. 2011;144(2):282–95.
CAS
PubMed
PubMed Central
Google Scholar
Mittelstaedt T, Schoch S. Structure and evolution of RIM-BP genes: identification of a novel family member. Gene. 2007;403(1–2):70–9.
CAS
PubMed
Google Scholar
Wang Y, Sugita S, Südhof TC. The RIM/NIM family of neuronal C2 domain proteins: interactions with Rab3 and a new class of Src homology 3 domain proteins. J Biol Chem. 2000;275(26):20033–44.
CAS
PubMed
Google Scholar
Hibino H, Pironkova R, Onwumere O, Vologodskaia M, Hudspeth AJ, Lesage F. RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca2+ channels. Neuron. 2002;34(3):411–23.
CAS
PubMed
PubMed Central
Google Scholar
Liu KSY, Siebert M, Mertel S, Knoche E, Wegener S, Wichmann C, et al. RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science. 2011;334(6062):1565–9.
CAS
PubMed
Google Scholar
Matkovic T, Siebert M, Knoche E, Depner H, Mertel S, Owald D, et al. The Bruchpilot cytomatrix determines the size of the readily releasable pool of synaptic vesicles. J Cell Biol. 2013;202(4):667–83.
CAS
PubMed
PubMed Central
Google Scholar
Kittel RJ, Wichmann C, Rasse TM, Fouquet W, Schmidt M, Schmid A, et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science (80- ). 2006;312(5776):1051–4.
CAS
Google Scholar
Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Dürrbeck H, et al. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in drosophila. Neuron. 2006;49:833–44.
CAS
PubMed
Google Scholar
Sugie A, Hakeda-Suzuki S, Suzuki E, Silies M, Shimozono M, Möhl C, et al. Molecular remodeling of the presynaptic active zone of drosophila photoreceptors via activity-dependent feedback. Neuron. 20156;86(3):711–25.
Schmid A, Hallermann S, Kittel RJ, Khorramshahi O, Frölich AMJ, Quentin C, et al. Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat Neurosci. 2008;11(6):659–66.
CAS
PubMed
Google Scholar
Ehmann N, van de Linde S, Alon A, Ljaschenko D, Keung XZ, Holm T, et al. Quantitative super-resolution imaging of Bruchpilot distinguishes active zone states. Nat Commun. 2014;5:4650.
CAS
PubMed
PubMed Central
Google Scholar
Sudhof TC. The synaptic vesicle cycle. Annu Rev Neurosci. 2004;27:509–47.
PubMed
Google Scholar
Held RG, Kaeser PS. ELKS active zone proteins as multitasking scaffolds for secretion. Open Biol. 2018;8(2):170258.
Kaeser PS, Regehr WG. The readily releasable pool of synaptic vesicles. Curr Opin Neurobiol. 2017;43(1):63–70.
CAS
PubMed
PubMed Central
Google Scholar
Ge WP, Yang XJ, Zhang Z, Wang HK, Shen W, Deng QD, et al. Long-term potentiation of neuron-glia synapses mediated by Ca2+−permeable AMPA receptors. Science (80- ). 2006;312(5779):1533–7.
CAS
Google Scholar
Jabs R, Pivneva T, Hüttmann K, Wyczynski A, Nolte C, Kettenmann H, et al. Synaptic transmission onto hippocampal glial cells with hGFAP promoter activity. J Cell Sci. 2005;118(16):3791–803.
CAS
PubMed
Google Scholar
Bergles DE, Roberts JDB, Somogyi P, Jahr CE. Glutamatergic synapses on OPCs in the hippocampus. Nature. 2000;405(1996):187–91.
CAS
PubMed
Google Scholar
Lin SC, Bergles DE. Synaptic signaling between neurons and glia. Glia. 2004;47(3):290–8.
PubMed
Google Scholar
Lin SC, Bergles DE. Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci. 2004;7(1):24–32.
CAS
PubMed
Google Scholar
Kennedy MB. Signal-processing machines at the postsynaptic density. Science (80- ). 2000;290(5492):750–4.
CAS
Google Scholar
Palay SL. Synapses in the central nervous system. J Biophys Biochem Cytol. 1956;2(4 Suppl):193–202.
CAS
PubMed
PubMed Central
Google Scholar
Gray EG. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat. 1959;93(4 Suppl):420–33.
CAS
PubMed
PubMed Central
Google Scholar
Scheefhals N, MacGillavry HD. Functional organization of postsynaptic glutamate receptors. Mol Cell Neurosci. 2018;91:82–94.
CAS
PubMed
PubMed Central
Google Scholar
DiAntonio A. Glutamate receptors at the drosophila neuromuscular junction. Int Rev Neurobiol. 2006;75(06):165–79.
CAS
PubMed
Google Scholar
Littleton JT. A genomic analysis of membrane trafficking and neurotransmitter release in drosophila. J Cell Biol. 2000;150(2):77–81.
PubMed Central
Google Scholar
Han TH, Dharkar P, Mayer ML, Serpe M. Functional reconstitution of Drosophila melanogaster NMJ glutamate receptors. Proc Natl Acad Sci U S A. 2015;112(19):6182–7.
CAS
PubMed
PubMed Central
Google Scholar
Qin G, Schwarz T, Kittel RJ, Schmid A, Rasse TM, Kappei D, et al. Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of drosophila. J Neurosci. 2005;25(12):3209–18.
CAS
PubMed
PubMed Central
Google Scholar
Featherstone DE, Rushton E, Rohrbough J, Liebl F, Karr J, Sheng Q, et al. An essential drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci. 2005;25(12):3199–208.
CAS
PubMed
PubMed Central
Google Scholar
Schuster CM, Ultsch A, Schloss P, Cox JA, Schmrrr B, Betzt H. Molecular cloning of an invertebrate glutamate receptor subunit expressed in drosophila muscle. Science. 2019;254(5028):112–4.
Marrus SB, DiAntonio A. Preferential localization of glutamate receptors opposite sites of high presynaptic release. Curr Biol. 2004;14(11):924–31.
CAS
PubMed
Google Scholar
Petersen SA, Fetter RD, Noordermeer JN, Goodman CS, DiAntonio A. Genetic analysis of glutamate receptors in drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron. 1997;19(6):1237–48.
CAS
PubMed
Google Scholar
DiAntonio A, Petersen SA, Heckmann M, Goodman CS. Glutamate receptor expression regulates quantal size and quantal content at the drosophila neuromuscular junction. J Neurosci. 1999;19(8):3023–32.
CAS
PubMed
PubMed Central
Google Scholar
Kim YJ, Igiesuorobo O, Ramos CI, Bao H, Zhang B, Serpe M. Prodomain removal enables Neto to stabilize glutamate receptors at the drosophila neuromuscular junction. PLoS Genet. 2015;11(2):1–26.
Google Scholar
Kim YJ, Bao H, Bonanno L, Zhang B, Serpel M. Drosophila neto is essential for clustering glutamate receptors at the neuromuscular junction. Genes Dev. 2012;26(9):974–87.
CAS
PubMed
PubMed Central
Google Scholar
Ramos CI, Igiesuorobo O, Wang Q, Serpe M. Neto-mediated intracellular interactions shape postsynaptic composition at the drosophila neuromuscular junction. PLoS Genet. 2015;11(4):1–26.
Google Scholar
Zhang W, St-Gelais F, Grabner CP, Trinidad JC, Sumioka A, Morimoto-Tomita M, et al. A transmembrane accessory subunit that modulates Kainate-type glutamate receptors. Neuron. 2009;61(3):385–96.
CAS
PubMed
PubMed Central
Google Scholar
Ng D, Pitcher GM, Szilard RK, Sertié A, Kanisek M, Clapcote SJ, et al. Neto1 is a novel CUB-domain NMDA receptor-interacting protein required for synaptic plasticity and learning. PLoS Biol. 2009;7(2):0278–300.
CAS
Google Scholar
Sigrist SJ, Thiel PR, Reiff DF, Schuster CM. The postsynaptic glutamate receptor subunit DGluR-IIA mediates long-term plasticity in drosophila. J Neurosci. 2002;22(17):7362–72.
CAS
PubMed
PubMed Central
Google Scholar
Zhao Z, Manser E. PAK family kinases. Cell Logist. 2012;2(2):59–68.
PubMed
PubMed Central
Google Scholar
Civiero L, Greggio E. PAKs in the brain: function and dysfunction. Biochim Biophys Acta - Mol Basis Dis. 2018;1864(2):444–53.
CAS
PubMed
Google Scholar
Sulkowski MJ, Han TH, Ott C, Wang Q, Verheyen EM, Lippincott-Schwartz J, et al. A novel, noncanonical BMP pathway modulates synapse maturation at the drosophila neuromuscular junction. PLoS Genet. 2016;12(1):1–31.
Google Scholar
Rasse TM, Fouquet W, Schmid A, Kittel RJ, Mertel S, Sigrist CB, et al. Glutamate receptor dynamics organizing synapse formation in vivo. Nat Neurosci. 2005;8(7):898–905.
CAS
PubMed
Google Scholar
Sone M, Suzuki E, Hoshino M, Hou D, Kuromi H, Fukata M, et al. Synaptic development is controlled in the periactive zones of drosophila synapses. Development. 2000;127(19):4157–68.
CAS
PubMed
Google Scholar
Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, Goodman CS. Highwire regulates synaptic growth in drosophila. Neuron. 2000;26(2):313–29.
CAS
PubMed
Google Scholar
Parnas D, Haghighi AP, Fetter RD, Kim SW, Goodman CS. Regulation of postsynaptic structure and protein localization by the rho-type guanine nucleotide exchange factor dPix. Neuron. 2001;32(3):415–24.
CAS
PubMed
Google Scholar
Albin SD, Davis GW. Coordinating structural and functional synapse development: postsynaptic p21-activated kinase independently specifies glutamate receptor abundance and postsynaptic morphology. J Neurosci. 2004;24(31):6871–9.
CAS
PubMed
PubMed Central
Google Scholar
Teodoro RO, Pekkurnaz G, Nasser A, Higashi-Kovtun ME, Balakireva M, Mclachlan IG, et al. Ral mediates activity-dependent growth of postsynaptic membranes via recruitment of the exocyst. EMBO J. 2013;32(14):2039–55.
CAS
PubMed
PubMed Central
Google Scholar
Quan A, Robinson PJ. Syndapin - a membrane remodelling and endocytic F-BAR protein. FEBS J. 2013;280(21):5198–212.
CAS
PubMed
Google Scholar
Kumar V, Fricke R, Bhar D, Reddy-Alla S, Krishnan KS, Bogdan S, et al. Syndapin promotes formation of a postsynaptic membrane system in drosophila. Mol Biol Cell. 2009;20:2254–64 Available from: http://www.molbiolcell.org/cgi/doi/10.1091/mbc. E08.
CAS
PubMed
PubMed Central
Google Scholar
Kessels MM, Qualmann B. Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 2002;21(22):6083–94.
CAS
PubMed
PubMed Central
Google Scholar
Oh E, Robinson I. Barfly: sculpting membranes at the drosophila neuromuscular junction. Dev Neurobiol. 2012;72(1):33–56.
CAS
PubMed
Google Scholar
Wang S, Yang J, Tsai A, Kuca T, Sanny J, Lee J, et al. Drosophila adducin regulates Dlg phosphorylation and targeting of Dlg to the synapse and epithelial membrane. Dev Biol. 2011;357(2):392–403.
CAS
PubMed
Google Scholar
Wang SJH, Tsai A, Wang M, Yoo SH, Kim HY, Yoo B, et al. Phospho-regulated drosophila adducin is a determinant of synaptic plasticity in a complex with Dlg and PIP2 at the larval neuromuscular junction. Biol Open. 2014;3(12):1196–206.
PubMed
PubMed Central
Google Scholar
Pielage J, Bulat V, Zuchero JB, Fetter RD, Davis GW. Hts/Adducin controls synaptic elaboration and elimination. Neuron. 2011;69(6):1114–31.
CAS
PubMed
PubMed Central
Google Scholar
Loya CM, McNeill EM, Bao H, Zhang B, Van Vactor D. miR-8 controls synapse structure by repression of the actin regulator enabled. Development. 2014;141(9):1864–74.
CAS
PubMed
PubMed Central
Google Scholar
Pielage J, Fetter RD, Davis GW. A postsynaptic Spectrin scaffold defines active zone size, spacing, and efficacy at the drosophila neuromuscular junction. J Cell Biol. 2006;175(3):491–503.
CAS
PubMed
PubMed Central
Google Scholar
Pielage J, Fetter RD, Davis GW. Presynaptic spectrin is essential for synapse stabilization. Curr Biol. 2005;15(10):918–28.
CAS
PubMed
Google Scholar
Pielage J, Cheng L, Fetter RD, Carlton PM, Sedat JW, Davis GW. A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron. 2008;58(2):195–209.
CAS
PubMed
PubMed Central
Google Scholar
Koch I, Schwarz H, Beuchle D, Goellner B, Langegger M, Aberle H. Drosophila Ankyrin 2 is required for synaptic stability. Neuron. 2008;58(2):210–22.
CAS
PubMed
Google Scholar
Tejedor FJ, Bokhari A, Rogero O, Gorczyca M, Zhang J, Kim E, et al. Essential role for dlg in synaptic clustering of shaker K+ channels in vivo. J Neurosci. 1997;17(1):152–9.
CAS
PubMed
PubMed Central
Google Scholar
Thomas U, Kim E, Kuhlendahl S, Koh YH, Gundelfinger ED, Sheng M, et al. Synaptic clustering of the cell adhesion molecule Fasciclin II by discs-large and its role in the regulation of presynaptic structure. Neuron. 1997;19(4):787–99.
CAS
PubMed
PubMed Central
Google Scholar
Chen K, Featherston DE. Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in drosophila. BMC Biol. 2005;3:1–13.
PubMed
PubMed Central
Google Scholar
Rao A, Kim E, Sheng M, Craig AM. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci. 1998;18(4):1217–29.
CAS
PubMed
PubMed Central
Google Scholar
Budnik V, Koh YH, Guan B, Hartmann B, Hough C, Woods D, et al. Regulation of synapse structure and function by the drosophila tumor suppressor gene dlg. Neuron. 1996;17(4):627–40.
CAS
PubMed
PubMed Central
Google Scholar
Astorga C, Jorquera RA, Ramírez M, Kohler A, López E, Delgado R, et al. Presynaptic DLG regulates synaptic function through the localization of voltage-activated Ca2+ channels. Sci Rep. 2016;6:1–14.
Google Scholar
Hoogenraad CC, Feliu-Mojer MI, Spangler SA, Milstein AD, Dunah AW, Hung AY, et al. Liprinα1 degradation by calcium/calmodulin-dependent protein kinase II regulates LAR receptor tyrosine phosphatase distribution and dendrite development. Dev Cell. 2007;12(4):587–602.
CAS
PubMed
Google Scholar
Mathew D, Ataman B, Chen J, Zhang Y, Cumberledge S, Budnik V. Cell signaling: wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science (80- ). 2005;310(5752):1344–7.
CAS
Google Scholar
Dear ML, Dani N, Parkinson W, Zhou S, Broadie K. Two classes of matrix metalloproteinases reciprocally regulate synaptogenesis. Dev. 2016;143(1):75–87 [cited 2020 Jun 21]. Available from: https://pubmed.ncbi.nlm.nih.gov/26603384/.
CAS
Google Scholar
Miech C, Pauer H-U, He X, Schwarz TL. Presynaptic local signaling by a canonical wingless pathway regulates development of the drosophila neuromuscular junction. J Neurosci. 2008;28(43):10875–84.
CAS
PubMed
PubMed Central
Google Scholar
Franco B, Bogdanik L, Bobinnec Y, Debec A, Bockaert J, Parmentier ML, et al. Shaggy, the homolog of glycogen synthase kinase 3, controls neuromuscular junction growth in drosophila. J Neurosci. 2004;24(29):6573–7.
CAS
PubMed
PubMed Central
Google Scholar
Gögel S, Wakefield S, Tear G, Klämbt C, Gordon-Weeks PR. The drosophila microtubule associated protein Futsch is phosphorylated by shaggy/Zeste-white 3 at an homologous GSK3β phosphorylation site in MAP 1B. Mol Cell Neurosci. 2006;33(2):188–99.
PubMed
Google Scholar
McCabe BD, Marqués G, Haghighi AP, Fetter RD, Crotty ML, Haerry TE, et al. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the drosophila neuromuscular junction. Neuron. 2003;39(2):241–54.
CAS
PubMed
Google Scholar
Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhães TR, Goodman CS. Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in drosophila. Neuron. 2002;33(4):545–58.
CAS
PubMed
Google Scholar
McCabe BD, Hom S, Aberle H, Fetter RD, Marques G, Haerry TE, et al. Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron. 2004;41(6):891–905.
CAS
PubMed
Google Scholar
Ball RW, Warren-Paquin M, Tsurudome K, Liao EH, Elazzouzi F, Cavanagh C, et al. Retrograde BMP signaling controls synaptic growth at the nmj by regulating trio expression in motor neurons. Neuron. 2010;27;66(4):536–49.
Goold CP, Davis GW. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron. 2007;56(1):109–23 [cited 2020 Jun 21]. Available from: /pmc/articles/PMC2699048/?report=abstract.
CAS
PubMed
PubMed Central
Google Scholar
Hoover KM, Gratz SJ, Qi N, Herrmann KA, Liu Y, Perry-Richardson JJ, et al. The calcium channel subunit α2δ-3 organizes synapses via an activity-dependent and autocrine BMP signaling pathway. Nat Commun. 2019;10(1) [cited 2020 Jun 21]. Available from: https://pubmed.ncbi.nlm.nih.gov/31811118/.
James RE, Hoover KM, Bulgari D, McLaughlin CN, Wilson CG, Wharton KA, et al. Crimpy enables discrimination of presynaptic and postsynaptic pools of a BMP at the drosophila neuromuscular junction. Dev Cell. 2014;31(5):586–98 [cited 2020 Jun 21]. Available from: https://pubmed.ncbi.nlm.nih.gov/25453556/.
CAS
PubMed
PubMed Central
Google Scholar
Eaton BA, Davis GW. LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron. 2005;47(5):695–708.
CAS
PubMed
Google Scholar
Yoshihara M, Adolfsen B, Galle KT, Littleton JT. Retrograde signaling by Syt 4 induces presynaptic release and synapse-specific growth. Science (80- ). 2005;310(5749):858–63.
CAS
Google Scholar
Barber CF, Jorquera RA, Melom JE, Littleton JT. Postsynaptic regulation of synaptic plasticity by synaptotagmin 4 requires both C2 domains. J Cell Biol. 2009;187(2):295–310.
CAS
PubMed
PubMed Central
Google Scholar
Yoshihara M, Littleton JT. Synaptotagmin functions as a calcium sensor to synchronize neurotransmitter release. Neuron. 2002;36(5):897–908.
CAS
PubMed
Google Scholar
Dani N, Broadie K. Glycosylated synaptomatrix regulation of trans-synaptic signaling. Dev Neurobiol. 2012;72(1):2–21.
CAS
PubMed
PubMed Central
Google Scholar
Kamimura K, Ueno K, Nakagawa J, Hamada R, Saitoe M, Maeda N. Perlecan regulates bidirectional Wnt signaling at the drosophila neuromuscular junction. J Cell Biol. 2013;200(2):219–33.
CAS
PubMed
PubMed Central
Google Scholar
Kamimura K, Odajima A, Ikegawa Y, Maru C, Maeda N. The HSPG Glypican regulates experience-dependent synaptic and behavioral plasticity by modulating the non-canonical BMP pathway. Cell Rep. 2019;28(12):3144–3156.e4 [cited 2020 Jun 21]. Available from: https://pubmed.ncbi.nlm.nih.gov/31533037/.
CAS
PubMed
Google Scholar
Bateman J, Shu H, Van Vactor D. The guanine nucleotide exchange factor trio mediates axonal development in the drosophila embryo. Neuron. 2000;26(1):93–106.
CAS
PubMed
Google Scholar
Debant A, Serra-Pagès C, Seipel K, O’Brien S, Tang M, Park SH, et al. The multidomain protein trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains. Proc Natl Acad Sci U S A. 1996;93(11):5466–71.
CAS
PubMed
PubMed Central
Google Scholar
Friedman SH, Dani N, Rushton E, Broadie K. Fragile X mental retardation protein regulates trans-synaptic signaling in drosophila. Dis Model Mech. 2013;6(6):1400–13.
CAS
PubMed
PubMed Central
Google Scholar
Rohrbough J, Kent KS, Broadie K, Weiss JB. Jelly belly trans-synaptic signaling to anaplastic lymphoma kinase regulates neurotransmission strength and synapse architecture. Dev Neurobiol. 2013;73(3):189–208.
CAS
PubMed
Google Scholar
Rohrbough J, Rushton E, Woodruff E, Fergestad T, Vigneswaran K, Broadie K. Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation. Genes Dev. 2007;21(20):2607–28.
CAS
PubMed
PubMed Central
Google Scholar
Rohrbough J, Broadie K. Anterograde jelly belly ligand to Alk receptor signaling at developing synapses is regulated by mind the gap. Development. 2010;137(20):3523–33.
CAS
PubMed
PubMed Central
Google Scholar
Rushton E, Rohrbough J, Deutsch K, Broadie K. Structure-function analysis of endogenous lectin mind-the-gap in synaptogenesis. Dev Neurobiol. 2012;72(8):1161–79.
CAS
PubMed
PubMed Central
Google Scholar
Fox MA, Sanes JR, Borza DB, Eswarakumar VP, Fässler R, Hudson BG, et al. Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell. 2007;129(1):179–93.
CAS
PubMed
Google Scholar
Muha V, Müller HAJ. Functions and mechanisms of fibroblast growth factor (FGF) signalling in Drosophila melanogaster. Int J Mol Sci. 2013;14(3):5920–37.
CAS
PubMed
PubMed Central
Google Scholar
Chang HC-H, Dimlich DN, Yokokura T, Mukherjee A, Kankel MW, Sen A, et al. Modeling spinal muscular atrophy in drosophila. PLoS One. 2008;3(9):e3209.
PubMed
PubMed Central
Google Scholar
Chan YB, Miguel-Aliaga I, Franks C, Thomas N, Trülzsch B, Sattelle DB, et al. Neuromuscular defects in a drosophila survival motor neuron gene mutant. Hum Mol Genet. 2003;12(12):1367–76.
CAS
PubMed
Google Scholar
Kariya S, Park GH, Maeno-Hikichi Y, Leykekhman O, Lutz C, Arkovitz MS, et al. Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum Mol Genet. 2008;17(16):2552–69.
CAS
PubMed
PubMed Central
Google Scholar
McNeill EM, Thompson C, Berke B, Chou VT, Rusch J, Duckworth A, et al. Drosophila enabled promotes synapse morphogenesis and regulates active zone form and function. Neural Dev. 2020;15(1):4.
CAS
PubMed
PubMed Central
Google Scholar
Nesler KR, Sand RI, Symmes BA, Pradhan SJ, Boin NG, Laun AE, et al. The miRNA pathway controls rapid changes in activity-dependent synaptic structure at the Drosophila melanogaster neuromuscular junction. PLoS One. 2013;8(7):e68385.
Lahey T, Gorczyca M, Jia XX, Budnik V. The drosophila tumor suppressor gene dlg is required for normal synaptic Bouton structure. Neuron. 1994;13(4):823–35.
CAS
PubMed
PubMed Central
Google Scholar
Guan B, Hartmann B, Kho YH, Gorczyca M, Budnik V. The drosophila tumor suppressor gene, dlg, is involved in structural plasticity at a glutamatergic synapse. Curr Biol. 1996;6(6):695–706.
CAS
PubMed
PubMed Central
Google Scholar
Van Vactor D, Wall DP, Johnson KG. Heparan sulfate proteoglycans and the emergence of neuronal connectivity. Curr Opin Neurobiol. 2006;16(1):40–51.
PubMed
Google Scholar
Lin T-Y, Huang C-H, Kao H-H, Liou G-G, Yeh S-R, Cheng C-M, et al. Abi plays an opposing role to Abl in drosophila axonogenesis and synaptogenesis. Development. 2009;136(18):3099–107.
CAS
PubMed
Google Scholar
Pawson C, Eaton BA, Davis GW. Formin-dependent synaptic growth: evidence that Dlar signals via diaphanous to modulate synaptic actin and dynamic pioneer microtubules. J Neurosci. 2008;28(44):11111–23.
CAS
PubMed
PubMed Central
Google Scholar
Goel P, Dufour Bergeron D, Böhme MA, Nunnelly L, Lehmann M, Buser C, et al. Homeostatic scaling of active zone scaffolds maintains global synaptic strength. J Cell Biol. 2019;218(5):1706–24.
CAS
PubMed
PubMed Central
Google Scholar
Pandey UB, Nichols CD. Human disease models in. Pharmacol Rev. 2011;63(2):411–36.
CAS
PubMed
PubMed Central
Google Scholar
Reiter LT, Potocki L, Chien S, Gribskov M, Bier E. A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res. 2001;11(6):1114–25.
CAS
PubMed
PubMed Central
Google Scholar