Dynamic mechanisms of neuroligin-dependent presynaptic terminal assembly in living cortical neurons

Neural Development

Shasta L Sabo²  Luke AD Bury¹ 

[1] Department of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA;Neuroscience, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA

关键词: Trans-synaptic adhesion;    Presynaptic;    Syncam;    Neurexin;    Neuroligin;    Axonal transport;    Synaptogenesis;   

Others  :  802497
DOI  :  10.1186/1749-8104-9-13

 received in 2014-02-05, accepted in 2014-05-12,  发布年份 2014

【 摘 要 】

Background

Synapse formation occurs when synaptogenic signals trigger coordinated development of pre and postsynaptic structures. One of the best-characterized synaptogenic signals is trans-synaptic adhesion. However, it remains unclear how synaptic proteins are recruited to sites of adhesion. In particular, it is unknown whether synaptogenic signals attract synaptic vesicle (SV) and active zone (AZ) proteins to nascent synapses or instead predominantly function to create sites that are capable of forming synapses. It is also unclear how labile synaptic proteins are at developing synapses after their initial recruitment. To address these issues, we used long-term, live confocal imaging of presynaptic terminal formation in cultured cortical neurons after contact with the synaptogenic postsynaptic adhesion proteins neuroligin-1 or SynCAM-1.

Results

Surprisingly, we find that trans-synaptic adhesion does not attract SV or AZ proteins nor alter their transport. In addition, although neurexin (the presynaptic partner of neuroligin) typically accumulates over the entire region of contact between axons and neuroligin-1-expressing cells, SV proteins selectively assemble at spots of enhanced neurexin clustering. The arrival and maintenance of SV proteins at these sites is highly variable over the course of minutes to hours, and this variability correlates with neurexin levels at individual synapses.

Conclusions

Together, our data support a model of synaptogenesis where presynaptic proteins are trapped at specific axonal sites, where they are stabilized by trans-synaptic adhesion signaling.

【 授权许可】

   
2014 Bury and Sabo; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Sudhof TC: Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
• [2]Missler M, Sudhof TC, Biederer T: Synaptic cell adhesion. Cold Spring Harb Perspect Biol 2012, 4:a005694.
• [3]Tallafuss A, Constable JR, Washbourne P: Organization of central synapses by adhesion molecules. Eur J Neurosci 2010, 32:198-206.
• [4]de Wit J, Sylwestrak E, O’Sullivan ML, Otto S, Tiglio K, Savas JN, Yates JR 3rd, Comoletti D, Taylor P, Ghosh A: LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 2009, 64:799-806.
• [5]Linhoff MW, Lauren J, Cassidy RM, Dobie FA, Takahashi H, Nygaard HB, Airaksinen MS, Strittmatter SM, Craig AM: An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 2009, 61:734-749.
• [6]Ko J, Fuccillo MV, Malenka RC, Sudhof TC: LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 2009, 64:791-798.
• [7]Lucido AL, Suarez Sanchez F, Thostrup P, Kwiatkowski AV, Leal-Ortiz S, Gopalakrishnan G, Liazoghli D, Belkaid W, Lennox RB, Grutter P, Garner CC, Colman DR: Rapid assembly of functional presynaptic boutons triggered by adhesive contacts. J Neurosci 2009, 29:12449-12466.
• [8]Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, Kim K, Kim H, Weinberg RJ, Kim E: NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 2006, 9:1294-1301.
• [9]Nguyen T, Sudhof TC: Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J Biol Chem 1997, 272:26032-26039.
• [10]Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Sudhof TC: Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 1995, 81:435-443.
• [11]Scheiffele P, Fan J, Choih J, Fetter R, Serafini T: Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 2000, 101:657-669.
• [12]Ripley B, Otto S, Tiglio K, Williams ME, Ghosh A: Regulation of synaptic stability by AMPA receptor reverse signaling. Proc Natl Acad Sci U S A 2011, 108:367-372.
• [13]Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Sudhof TC: SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 2002, 297:1525-1531.
• [14]Fogel AI, Akins MR, Krupp AJ, Stagi M, Stein V, Biederer T: SynCAMs organize synapses through heterophilic adhesion. J Neurosci 2007, 27:12516-12530.
• [15]Stan A, Pielarski KN, Brigadski T, Wittenmayer N, Fedorchenko O, Gohla A, Lessmann V, Dresbach T, Gottmann K: Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation. Proc Natl Acad Sci U S A 2010, 107:11116-11121.
• [16]Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P: Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 2003, 6:708-716.
• [17]Gokce O, Sudhof TC: Membrane-tethered monomeric neurexin LNS-domain triggers synapse formation. J Neurosci 2013, 33:14617-14628.
• [18]Tsuriel S, Geva R, Zamorano P, Dresbach T, Boeckers T, Gundelfinger ED, Garner CC, Ziv NE: Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol 2006, 4:e271.
• [19]Kalla S, Stern M, Basu J, Varoqueaux F, Reim K, Rosenmund C, Ziv NE, Brose N: Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice. J Neurosci 2006, 26:13054-13066.
• [20]Tsuriel S, Fisher A, Wittenmayer N, Dresbach T, Garner CC, Ziv NE: Exchange and redistribution dynamics of the cytoskeleton of the active zone molecule bassoon. J Neurosci 2009, 29:351-358.
• [21]Fisher-Lavie A, Zeidan A, Stern M, Garner CC, Ziv NE: Use dependence of presynaptic tenacity. J Neurosci 2011, 31:16770-16780.
• [22]Staras K, Branco T: Sharing vesicles between central presynaptic terminals: implications for synaptic function. Front Synaptic Neurosci 2010, 2:20.
• [23]Darcy KJ, Staras K, Collinson LM, Goda Y: Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 2006, 9:315-321.
• [24]Zeidan A, Ziv NE: Neuroligin-1 loss is associated with reduced tenacity of excitatory synapses. PLoS One 2012, 7:e42314.
• [25]Herzog E, Nadrigny F, Silm K, Biesemann C, Helling I, Bersot T, Steffens H, Schwartzmann R, Nagerl UV, El Mestikawy S, Rhee J, Kirchhoff F, Brose N: In vivo imaging of intersynaptic vesicle exchange using VGLUT1 Venus knock-in mice. J Neurosci 2011, 31:15544-15559.
• [26]Hall DH, Hedgecock EM: Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 1991, 65:837-847.
• [27]Kraszewski K, Mundigl O, Daniell L, Verderio C, Matteoli M, De Camilli P: Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J Neurosci 1995, 15:4328-4342.
• [28]Okada Y, Yamazaki H, Sekine-Aizawa Y, Hirokawa N: The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 1995, 81:769-780.
• [29]Dai Z, Peng HB: Dynamics of synaptic vesicles in cultured spinal cord neurons in relationship to synaptogenesis. Mol Cell Neurosci 1996, 7:443-452.
• [30]Waterman-Storer CM, Karki SB, Kuznetsov SA, Tabb JS, Weiss DG, Langford GM, Holzbaur EL: The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci U S A 1997, 94:12180-12185.
• [31]Nakata T, Terada S, Hirokawa N: Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J Cell Biol 1998, 140:659-674.
• [32]Yonekawa Y, Harada A, Okada Y, Funakoshi T, Kanai Y, Takei Y, Terada S, Noda T, Hirokawa N: Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice. J Cell Biol 1998, 141:431-441.
• [33]Ahmari SE, Buchanan J, Smith SJ: Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 2000, 3:445-451.
• [34]Kaether C, Skehel P, Dotti CG: Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol Biol Cell 2000, 11:1213-1224.
• [35]Zhao C, Takita J, Tanaka Y, Setou M, Nakagawa T, Takeda S, Yang HW, Terada S, Nakata T, Takei Y, Saito M, Tsuji S, Hayashi Y, Hirokawa N: Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 2001, 105:587-597.
• [36]LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascano J, Tokito M, Van Winkle T, Howland DS, Holzbaur EL: Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 2002, 34:715-727.
• [37]Nakamura N, Miyake Y, Matsushita M, Tanaka S, Inoue H, Kanazawa H: KIF1Bbeta2, capable of interacting with CHP, is localized to synaptic vesicles. J Biochem 2002, 132:483-491.
• [38]Sabo SL, Gomes RA, McAllister AK: Formation of presynaptic terminals at predefined sites along axons. J Neurosci 2006, 26:10813-10825.
• [39]Tao-Cheng JH: Ultrastructural localization of active zone and synaptic vesicle proteins in a preassembled multi-vesicle transport aggregate. Neuroscience 2007, 150:575-584.
• [40]Lee H, Dean C, Isacoff E: Alternative splicing of neuroligin regulates the rate of presynaptic differentiation. J Neurosci 2010, 30:11435-11446.
• [41]Bury LA, Sabo SL: Coordinated trafficking of synaptic vesicle and active zone proteins prior to synapse formation. Neural Dev 2011, 6:24. BioMed Central Full Text
• [42]Scott DA, Das U, Tang Y, Roy S: Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron 2011, 70:441-454.
• [43]Kondo M, Takei Y, Hirokawa N: Motor protein KIF1A is essential for hippocampal synaptogenesis and learning enhancement in an enriched environment. Neuron 2012, 73:743-757.
• [44]Krueger DD, Tuffy LP, Papadopoulos T, Brose N: The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr Opin Neurobiol 2012, 22:412-422.
• [45]Peixoto RT, Kunz PA, Kwon H, Mabb AM, Sabatini BL, Philpot BD, Ehlers MD: Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 2012, 76:396-409.
• [46]Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM: Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 2004, 119:1013-1026.
• [47]Biermann B, Sokoll S, Klueva J, Missler M, Wiegert JS, Sibarita JB, Heine M: Imaging of molecular surface dynamics in brain slices using single-particle tracking. Nat Commun 2014, 5:3024.
• [48]Fairless R, Masius H, Rohlmann A, Heupel K, Ahmad M, Reissner C, Dresbach T, Missler M: Polarized targeting of neurexins to synapses is regulated by their C-terminal sequences. J Neurosci 2008, 28:12969-12981.
• [49]Owald D, Khorramshahi O, Gupta VK, Banovic D, Depner H, Fouquet W, Wichmann C, Mertel S, Eimer S, Reynolds E, Holt M, Aberle H, Sigrist SJ: Cooperation of Syd-1 with Neurexin synchronizes pre- with postsynaptic assembly. Nat Neurosci 2012, 15:1219-1226.
• [50]Shcherbakova DM, Verkhusha VV: Near-infrared fluorescent proteins for multicolor in vivo imaging. Nat Methods 2013, 10:751-754.
• [51]Cantallops I, Cline HT: Synapse formation: if it looks like a duck and quacks like a duck. Curr Biol 2000, 10:R620-R623.
• [52]Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC: Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 2001, 29:131-143.
• [53]Shapira M, Zhai RG, Dresbach T, Bresler T, Torres VI, Gundelfinger ED, Ziv NE, Garner CC: Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 2003, 38:237-252.
• [54]Dresbach T, Torres V, Wittenmayer N, Altrock WD, Zamorano P, Zuschratter W, Nawrotzki R, Ziv NE, Garner CC, Gundelfinger ED: Assembly of active zone precursor vesicles: obligatory trafficking of presynaptic cytomatrix proteins Bassoon and Piccolo via a trans-Golgi compartment. J Biol Chem 2006, 281:6038-6047.
• [55]Maas C, Torres VI, Altrock WD, Leal-Ortiz S, Wagh D, Terry-Lorenzo RT, Fejtova A, Gundelfinger ED, Ziv NE, Garner CC: Formation of Golgi-derived active zone precursor vesicles. J Neurosci 2012, 32:11095-11108.
• [56]Su Q, Cai Q, Gerwin C, Smith CL, Sheng ZH: Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol 2004, 6:941-953.
• [57]Cai Q, Pan PY, Sheng ZH: Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J Neurosci 2007, 27:7284-7296.
• [58]Fejtova A, Davydova D, Bischof F, Lazarevic V, Altrock WD, Romorini S, Schone C, Zuschratter W, Kreutz MR, Garner CC, Ziv NE, Gundelfinger ED: Dynein light chain regulates axonal trafficking and synaptic levels of Bassoon. J Cell Biol 2009, 185:341-355.
• [59]Friedman HV, Bresler T, Garner CC, Ziv NE: Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 2000, 27:57-69.
• [60]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, 78:994-1011.
• [61]Robbins EM, Krupp AJ, Perez de Arce K, Ghosh AK, Fogel AI, Boucard A, Sudhof TC, Stein V, Biederer T: SynCAM 1 adhesion dynamically regulates synapse number and impacts plasticity and learning. Neuron 2010, 68:894-906.
• [62]Craig AM, Kang Y: Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 2007, 17:43-52.
• [63]Klassen MP, Wu YE, Maeder CI, Nakae I, Cueva JG, Lehrman EK, Tada M, Gengyo-Ando K, Wang GJ, Goodman M, Mitani S, Kontani K, Katada T, Shen K: An Arf-like small G protein, ARL-8, promotes the axonal transport of presynaptic cargoes by suppressing vesicle aggregation. Neuron 2010, 66:710-723.
• [64]Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B, Reichardt LF: Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 2003, 40:719-731.
• [65]Bamji SX, Rico B, Kimes N, Reichardt LF: BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions. J Cell Biol 2006, 174:289-299.
• [66]Suarez F, Thostrup P, Colman D, Grutter P: Dynamics of presynaptic protein recruitment induced by local presentation of artificial adhesive contacts. Dev Neurobiol 2013, 73:98-106.
• [67]Goldstein AY, Wang X, Schwarz TL: Axonal transport and the delivery of pre-synaptic components. Curr Opin Neurobiol 2008, 18:495-503.
• [68]Hirokawa N, Noda Y, Tanaka Y, Niwa S: Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 2009, 10:682-696.
• [69]Verhey KJ, Hammond JW: Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 2009, 10:765-777.
• [70]Hirokawa N, Niwa S, Tanaka Y: Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 2010, 68:610-638.
• [71]Hamdan FF, Gauthier J, Araki Y, Lin DT, Yoshizawa Y, Higashi K, Park AR, Spiegelman D, Dobrzeniecka S, Piton A, Tomitori H, Daoud H, Massicotte C, Henrion E, Diallo O, Shekarabi M, Marineau C, Shevell M, Maranda B, Mitchell G, Nadeau A, D’Anjou G, Vanasse M, Srour M, Lafrenière RG, Drapeau P, Lacaille JC, Kim E, Lee JR, S2D Group, et al.: Excess of de novo deleterious mutations in genes associated with glutamatergic systems in nonsyndromic intellectual disability. Am J Hum Genet 2011, 88:306-316.
• [72]Hopf FW, Waters J, Mehta S, Smith SJ: Stability and plasticity of developing synapses in hippocampal neuronal cultures. J Neurosci 2002, 22:775-781.
• [73]Murthy VN, Schikorski T, Stevens CF, Zhu Y: Inactivity produces increases in neurotransmitter release and synapse size. Neuron 2001, 32:673-682.
• [74]Matz J, Gilyan A, Kolar A, McCarvill T, Krueger SR: Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release. Proc Natl Acad Sci U S A 2010, 107:8836-8841.
• [75]Holderith N, Lorincz A, Katona G, Rozsa B, Kulik A, Watanabe M, Nusser Z: Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat Neurosci 2012, 15:988-997.
• [76]Minerbi A, Kahana R, Goldfeld L, Kaufman M, Marom S, Ziv NE: Long-term relationships between synaptic tenacity, synaptic remodeling, and network activity. PLoS Biol 2009, 7:e1000136.
• [77]Staras K, Branco T, Burden JJ, Pozo K, Darcy K, Marra V, Ratnayaka A, Goda Y: A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron 2010, 66:37-44.
• [78]Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH: Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 2004, 304:1815-1819.
• [79]Berry CT, Sceniak MP, Zhou L, Sabo SL: Developmental up-regulation of vesicular glutamate transporter-1 promotes neocortical presynaptic terminal development. PLoS One 2012, 7:e50911.
• [80]Sceniak MP, Berry CT, Sabo SL: Facilitation of neocortical presynaptic terminal development by NMDA receptor activation. Neural Dev 2012, 7:8. BioMed Central Full Text
• [81]Kwon HB, Sabatini BL: Glutamate induces de novo growth of functional spines in developing cortex. Nature 2011, 474:100-104.
• [82]Mozhayeva MG, Sara Y, Liu X, Kavalali ET: Development of vesicle pools during maturation of hippocampal synapses. J Neurosci 2002, 22:654-665.
• [83]Owald D, Fouquet W, Schmidt M, Wichmann C, Mertel S, Depner H, Christiansen F, Zube C, Quentin C, Korner J, Urlaub H, Mechtler K, Sigrist SJ: A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J Cell Biol 2010, 188:565-579.
• [84]Dai Y, Taru H, Deken SL, Grill B, Ackley B, Nonet ML, Jin Y: SYD-2 liprin-alpha organizes presynaptic active zone formation through ELKS. Nat Neurosci 2006, 9:1479-1487.
• [85]Patel MR, Lehrman EK, Poon VY, Crump JG, Zhen M, Bargmann CI, Shen K: Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat Neurosci 2006, 9:1488-1498.
• [86]Kaufmann N, DeProto J, Ranjan R, Wan H, Van Vactor D: Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 2002, 34:27-38.
• [87]Miller KE, DeProto J, Kaufmann N, Patel BN, Duckworth A, Van Vactor D: Direct observation demonstrates that liprin-alpha is required for trafficking of synaptic vesicles. Curr Biol 2005, 15:684-689.
• [88]Spangler SA, Hoogenraad CC: Liprin-alpha proteins: scaffold molecules for synapse maturation. Biochem Soc Trans 2007, 35:1278-1282.
• [89]Holbrook S, Finley JK, Lyons EL, Herman TG: Loss of syd-1 from R7 neurons disrupts two distinct phases of presynaptic development. J Neurosci 2012, 32:18101-18111.
• [90]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, 78:1012-1023.
• [91]Zhang W, Benson DL: Stages of synapse development defined by dependence on F-actin. J Neurosci 2001, 21:5169-5181.
• [92]Sun Y, Bamji SX: Beta-Pix modulates actin-mediated recruitment of synaptic vesicles to synapses. J Neurosci 2011, 31:17123-17133.
• [93]Chia PH, Patel MR, Shen K: NAB-1 instructs synapse assembly by linking adhesion molecules and F-actin to active zone proteins. Nat Neurosci 2012, 15:234-242.
• [94]Martinez A, Alcantara S, Borrell V, Del Rio JA, Blasi J, Otal R, Campos N, Boronat A, Barbacid M, Silos-Santiago I, Soriano E: TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. J Neurosci 1998, 18:7336-7350.
• [95]Collin C, Vicario-Abejon C, Rubio ME, Wenthold RJ, McKay RD, Segal M: Neurotrophins act at presynaptic terminals to activate synapses among cultured hippocampal neurons. Eur J Neurosci 2001, 13:1273-1282.
• [96]Otal R, Martinez A, Soriano E: Lack of TrkB and TrkC signaling alters the synaptogenesis and maturation of mossy fiber terminals in the hippocampus. Cell Tissue Res 2005, 319:349-358.
• [97]Melo CV, Mele M, Curcio M, Comprido D, Silva CG, Duarte CB: BDNF regulates the expression and distribution of vesicular glutamate transporters in cultured hippocampal neurons. PLoS One 2013, 8:e53793.
• [98]Washbourne P, Bennett JE, McAllister AK: Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat Neurosci 2002, 5:751-759.
• [99]Sabo SL, McAllister AK: Mobility and cycling of synaptic protein-containing vesicles in axonal growth cone filopodia. Nat Neurosci 2003, 6:1264-1269.
• [100]Dresbach T, Hempelmann A, Spilker C, tom Dieck S, Altrock WD, Zuschratter W, Garner CC, Gundelfinger ED: Functional regions of the presynaptic cytomatrix protein bassoon: significance for synaptic targeting and cytomatrix anchoring. Mol Cell Neurosci 2003, 23:279-291.
• [101]Wienisch M, Klingauf J: Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat Neurosci 2006, 9:1019-1027.
• [102]de Wit J, Toonen RF, Verhage M: Matrix-dependent local retention of secretory vesicle cargo in cortical neurons. J Neurosci 2009, 29:23-37.
• [103]Hoy JL, Constable JR, Vicini S, Fu Z, Washbourne P: SynCAM1 recruits NMDA receptors via protein 4.1B. Mol Cell Neurosci 2009, 42:466-483.
• [104]Hirao K, Hata Y, Ide N, Takeuchi M, Irie M, Yao I, Deguchi M, Toyoda A, Sudhof TC, Takai Y: A novel multiple PDZ domain-containing molecule interacting with N-methyl-D-aspartate receptors and neuronal cell adhesion proteins. J Biol Chem 1998, 273:21105-21110.