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Synapse Formation in the Mammalian Central Nervous System

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The Sticky Synapse

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Abstract

Synapses are highly organized molecular complexes at which neurons communicate with each other in the brain. To form a functional synapse, hundreds of molecules need to be organized at the contact site between the axon and its target in the developing brain. Converging evidence now suggests that several families of cell adhesion molecules (CAMs) play important roles in differentiation, maturation, and maintenance of synapses. In this chapter, we will describe the structure of synapses, pre- and postsynaptic scaffolding molecules, steps of synapse formation, and synaptogenic molecules, including CAMs, in the mammalian central nervous system.

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References

  • Ahmad-Annuar A, Ciani L, Simeonidis I et al. (2006) Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. J Cell Biol 174:127–139

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Altrock WD, tom Dieck S, Sokolov M et al. (2003) Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron 37:787–800

    PubMed  CAS  Google Scholar 

  • Ango F, di Cristo G, Higashiyama H et al. (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119:257–272

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bacci A, Coco S, Pravettoni E et al. (2001) Chronic blockade of glutamate receptors enhances presynaptic release and downregulates the interaction between synaptophysin-synaptobrevin-vesicle-associated membrane protein 2. J Neurosci 21:6588–6596

    PubMed  CAS  Google Scholar 

  • Betz A, Ashery U, Rickmann M et al. (1998) Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21:123–136

    PubMed  CAS  Google Scholar 

  • Biederer T, Sara Y, Mozhayeva M et al. (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525–1531

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Boeckers TM, Bockmann J, Kreutz MR et al. (2002) ProSAP/Shank proteins – a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neurochem 81:903–910

    PubMed  CAS  Google Scholar 

  • Boeckers TM, Kreutz MR, Winter C et al. (1999) Proline-rich synapse-associated protein-1/cortactin binding protein 1 (ProSAP1/CortBP1) is a PDZ-domain protein highly enriched in the postsynaptic density. J Neurosci 19:6506–6518

    PubMed  CAS  Google Scholar 

  • Boucard AA, Chubykin AA, Comoletti D et al. (2005) A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 48:229–236

    PubMed  CAS  Google Scholar 

  • Brose N, Hofmann K, Hata Y et al. (1995) Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J Biol Chem 270:25273–25280

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Burkarth N, Kriebel M, Kranz EU et al. (2007) Neurofascin regulates the formation of gephyrin clusters and their subsequent translocation to the axon hillock of hippocampal neurons. Mol Cell Neurosci 36:59–70

    PubMed  CAS  Google Scholar 

  • Butz S, Okamoto M and Südhof TC (1998) A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94:773–782

    PubMed  CAS  Google Scholar 

  • Carmignoto G and Vicini S (1992) Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258:1007–1011

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Cho KO, Hunt CA and Kennedy MB (1992) The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9:929–942

    PubMed  CAS  Google Scholar 

  • Christopherson KS, Ullian EM, Stokes CC et al. (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120:421–433

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ciani L and Salinas PC (2005) WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 6:351–362

    PubMed  CAS  Google Scholar 

  • Cohen NR, Taylor JS, Scott LB et al. (1998) Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr Biol 8:26–33

    PubMed  CAS  Google Scholar 

  • Collins MO, Husi H, Yu L et al. (2006) Molecular characterization and comparison of the components and multiprotein complexes in the postsynaptic proteome. J Neurochem 97 Suppl 1:16–23

    Google Scholar 

  • Craig AM (1998) Activity and synaptic receptor targeting: the long view. Neuron 21:459–462

    PubMed  CAS  Google Scholar 

  • Craig AM, Graf ER and Linhoff MW (2006) How to build a central synapse: clues from cell culture. Trends Neurosci 29:8–20

    PubMed  CAS  Google Scholar 

  • Cremer H, Chazal G, Carleton A et al. (1998) Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc Natl Acad Sci U S A 95:13242–13247

    PubMed  CAS  Google Scholar 

  • Cremer H, Chazal G, Goridis C et al. (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323–335

    PubMed  CAS  Google Scholar 

  • Dalva MB, Takasu MA, Lin MZ et al. (2000) EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103:945–956

    PubMed  CAS  Google Scholar 

  • Demyanenko GP, Tsai AY and Maness PF (1999) Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knockout mice. J Neurosci 19:4907–4920

    PubMed  CAS  Google Scholar 

  • Dick O, tom Dieck S, Altrock WD et al. (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775–786

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Du Y, Weed SA, Xiong WC et al. (1998) Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol Cell Biol 18:5838–5851

    PubMed  CAS  Google Scholar 

  • Durand GM and Konnerth A (1996) Long-term potentiation as a mechanism of functional synapse induction in the developing hippocampus. J Physiol Paris 90:313–315

    PubMed  CAS  Google Scholar 

  • Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6:231–242

    PubMed  CAS  Google Scholar 

  • Feldman DE and Knudsen EI (1998) Experience-dependent plasticity and the maturation of glutamatergic synapses. Neuron 20:1067–1071

    PubMed  CAS  Google Scholar 

  • Feng G, Mellor RH, Bernstein M et al. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41–51

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Fiala JC, Feinberg M, Popov V et al. (1998) Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900–8911

    PubMed  CAS  Google Scholar 

  • Fischer F, Kneussel M, Tintrup H et al. (2000) Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. J Comp Neurol 427:634–648

    PubMed  CAS  Google Scholar 

  • Flanagan JG and Vanderhaeghen P (1998) The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309–345

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Fuerst PG, Koizumi A, Masland RH et al. (2008) Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451:470–474

    PubMed  CAS  Google Scholar 

  • Garcia EP, Mehta S, Blair LA et al. (1998) SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron 21:727–739

    PubMed  CAS  Google Scholar 

  • Garner CC, Waites CL and Ziv NE (2006) Synapse development: still looking for the forest, still lost in the trees. Cell Tissue Res 326:249–262

    PubMed  Google Scholar 

  • Gerrow K, Romorini S, Nabi SM et al. (2006) A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 49:547–562

    PubMed  CAS  Google Scholar 

  • Goddard CA, Butts DA and Shatz CJ (2007) Regulation of CNS synapses by neuronal MHC class I. Proc Natl Acad Sci U S A 104:6828–6833

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Gray EG (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 93:420–433

    PubMed  CAS  Google Scholar 

  • Grutzendler J, Kasthuri N and Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812–816

    PubMed  CAS  Google Scholar 

  • Hall AC, Lucas FR and Salinas PC (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100:525–535

    PubMed  CAS  Google Scholar 

  • Harris KM (1999) Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 9:343–348

    PubMed  CAS  Google Scholar 

  • Harris KM, Jensen FE and Tsao B (1992) Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12:2685–2705

    PubMed  CAS  Google Scholar 

  • Harris KM and Stevens JK (1989) Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982–2997

    PubMed  CAS  Google Scholar 

  • Hata Y, Butz S and Südhof TC (1996) CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 16:2488–2494

    PubMed  CAS  Google Scholar 

  • Hayashi MK, Tang C, Verpelli C et al. (2009) The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137:159–171

    Google Scholar 

  • Henkemeyer M, Itkis OS, Ngo M et al. (2003) Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163:1313–1326

    PubMed  CAS  Google Scholar 

  • Honda T, Sakisaka T, Yamada T et al. (2006) Involvement of nectins in the formation of puncta adherentia junctions and the mossy fiber trajectory in the mouse hippocampus. Mol Cell Neurosci 31:315–325

    PubMed  CAS  Google Scholar 

  • Hsueh YP, Yang FC, Kharazia V et al. (1998) Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol 142:139–151

    PubMed  CAS  Google Scholar 

  • Huh GS, Boulanger LM, Du H et al. (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290:2155–2159

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Isaac JT, Crair MC, Nicoll RA et al. (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269–280

    PubMed  CAS  Google Scholar 

  • Isaac JT, Nicoll RA and Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427–434

    PubMed  CAS  Google Scholar 

  • Kadowaki M, Nakamura S, Machon O et al. (2007) N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304:22–33

    PubMed  CAS  Google Scholar 

  • Kennedy MB (2000) Signal-processing machines at the postsynaptic density. Science 290:750–754

    PubMed  CAS  Google Scholar 

  • Kim E and Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neurosci 5:771–781

    PubMed  CAS  Google Scholar 

  • Kim S, Burette A, Chung HS et al. (2006) NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 9:1294–1301

    Google Scholar 

  • Kneussel M, Brandstatter JH, Laube B et al. (1999) Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J Neurosci 19:9289–9297

    PubMed  CAS  Google Scholar 

  • Ko J, Kim S, Chung HS et al. (2006) SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron 50:233–245

    PubMed  CAS  Google Scholar 

  • Kornau HC, Schenker LT, Kennedy MB et al. (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737–1740

    PubMed  CAS  Google Scholar 

  • Ksiazek I, Burkhardt C, Lin S et al. (2007) Synapse loss in cortex of agrin-deficient mice after genetic rescue of perinatal death. J Neurosci 27:7183–7195

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Leal-Ortiz S, Waites CL, Terry-Lorenzo R et al. (2008) Piccolo modulation of Synapsin1a dynamics regulates synaptic vesicle exocytosis. J Cell Biol 181:831–846

    PubMed  CAS  Google Scholar 

  • Levi S, Logan SM, Tovar KR et al. (2004) Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J Neurosci 24:207–217

    PubMed  CAS  Google Scholar 

  • Liao D, Hessler NA and Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400–404

    PubMed  CAS  Google Scholar 

  • Liao D, Zhang X, O’Brien R et al. (1999) Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci 2:37–43

    PubMed  CAS  Google Scholar 

  • Linhoff MW, Lauren J, Cassidy RM et al. (2009) An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 61:734–749

    Google Scholar 

  • Livet J, Weissman TA, Kang H et al. (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450:56–62

    PubMed  CAS  Google Scholar 

  • Logan CY and Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810

    PubMed  CAS  Google Scholar 

  • Lonart G (2002) RIM1: an edge for presynaptic plasticity. Trends Neurosci 25:329–332

    PubMed  CAS  Google Scholar 

  • Lucas FR and Salinas PC (1997) WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev Biol 192:31–44

    PubMed  CAS  Google Scholar 

  • Maruyama IN and Brenner S (1991) A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc Natl Acad Sci U S A 88:5729–5733

    PubMed  CAS  Google Scholar 

  • Maximov A, Südhof TC and Bezprozvanny I (1999) Association of neuronal calcium channels with modular adaptor proteins. J Biol Chem 274:24453–24456

    PubMed  CAS  Google Scholar 

  • McAllister AK (2007) Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 30:425–450

    PubMed  CAS  Google Scholar 

  • McLaughlin T and O’Leary DD (2005) Molecular gradients and development of retinotopic maps. Annu Rev Neurosci 28:327–355

    PubMed  CAS  Google Scholar 

  • Mi R, Tang X, Sutter R et al. (2002) Differing mechanisms for glutamate receptor aggregation on dendritic spines and shafts in cultured hippocampal neurons. J Neurosci 22:7606–7616

    PubMed  CAS  Google Scholar 

  • Morita A, Yamashita N, Sasaki Y et al. (2006) Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J Neurosci 26:2971–2980

    PubMed  CAS  Google Scholar 

  • Naisbitt S, Kim E, Tu JC et al. (1999) Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23:569–582

    PubMed  CAS  Google Scholar 

  • Nam CI and Chen L (2005) Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci U S A 102:6137–6142

    PubMed  CAS  Google Scholar 

  • Nguyen T and Südhof TC (1997) Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J Biol Chem 272:26032–26039

    PubMed  CAS  Google Scholar 

  • O’Brien R, Xu D, Mi R et al. (2002) Synaptically targeted narp plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons. J Neurosci 22:4487–4498

    PubMed  Google Scholar 

  • O’Brien RJ, Xu D, Petralia RS et al. (1999) Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23:309–323

    PubMed  Google Scholar 

  • Okabe S, Collin C, Auerbach JM et al. (1998) Hippocampal synaptic plasticity in mice overexpressing an embryonic subunit of the NMDA receptor. J Neurosci 18:4177–4188

    PubMed  CAS  Google Scholar 

  • Okabe S, Miwa A and Okado H (2001) Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 21:6105–6114

    PubMed  CAS  Google Scholar 

  • Oliveira AL, Thams S, Lidman O et al. (2004) A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl Acad Sci USA 101:17843–17848

    PubMed  CAS  Google Scholar 

  • Ornitz DM, Xu J, Colvin JS et al. (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292–15297

    PubMed  CAS  Google Scholar 

  • Palay SL (1956) Synapses in the central nervous system. J Biophys Biochem Cytol 2:193–202

    Article  PubMed  CAS  Google Scholar 

  • Paradis S, Harrar DB, Lin Y et al. (2007) An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 53:217–232

    PubMed  CAS  Google Scholar 

  • Perin MS, Fried VA, Mignery GA et al. (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345:260–263

    PubMed  CAS  Google Scholar 

  • Petralia RS, Sans N, Wang YX et al. (2005) Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 29:436–452

    PubMed  CAS  Google Scholar 

  • Pravettoni E, Bacci A, Coco S et al. (2000) Different localizations and functions of L-type and N-type calcium channels during development of hippocampal neurons. Dev Biol 227:581–594

    PubMed  CAS  Google Scholar 

  • Richter K, Langnaese K, Kreutz MR et al. (1999) Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. J Comp Neurol 408:437–448

    PubMed  CAS  Google Scholar 

  • Roche KW, Ly CD, Petralia RS et al. (1999) Postsynaptic density-93 interacts with the delta2 glutamate receptor subunit at parallel fiber synapses. J Neurosci 19:3926–3934

    PubMed  CAS  Google Scholar 

  • Rougon G and Hobert O (2003) New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci 26:207–238

    PubMed  CAS  Google Scholar 

  • Sanes JR and Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389–442

    PubMed  CAS  Google Scholar 

  • Sara Y, Biederer T, Atasoy D et al. (2005) Selective capability of SynCAM and neuroligin for functional synapse assembly. J Neurosci 25:260–270

    PubMed  CAS  Google Scholar 

  • Scannevin RH and Huganir RL (2000) Postsynaptic organization and regulation of excitatory synapses. Nat Rev Neurosci 1:133–141

    PubMed  CAS  Google Scholar 

  • Scheiffele P (2003) Cell-cell signaling during synapse formation in the CNS. Annu Rev Neurosci 26:485–508

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schoch S, Castillo PE, Jo T et al. (2002) RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415:321–326

    PubMed  CAS  Google Scholar 

  • Serizawa S, Miyamichi K, Takeuchi H et al. (2006) A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127:1057–1069

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sheng M (2001) Molecular organization of the postsynaptic specialization. Proc Natl Acad Sci U S A 98:7058–7061

    PubMed  CAS  Google Scholar 

  • Sheng M, Cummings J, Roldan LA et al. (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144–147

    PubMed  CAS  Google Scholar 

  • Sheng M and Kim E (2000) The Shank family of scaffold proteins. J Cell Sci 113 (Pt 11):1851–1856

    PubMed  CAS  Google Scholar 

  • Sherrington CS (1897) The central nervous system, Vol. III. In: M. Foster (Ed.) A Textbook of Physiology, 7th Edition. London: Macmillan. p. 60

    Google Scholar 

  • Song JY, Ichtchenko K, Südhof TC et al. (1999) Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci U S A 96:1100–1105

    PubMed  CAS  Google Scholar 

  • Südhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509–547

    PubMed  Google Scholar 

  • Takao-Rikitsu E, Mochida S, Inoue E 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

    PubMed  CAS  Google Scholar 

  • Tepass U, Truong K, Godt D et al. (2000) Cadherins in embryonic and neural morphogenesis. Nat Rev Mol Cell Biol 1:91–100

    PubMed  CAS  Google Scholar 

  • tom Dieck S, Sanmarti-Vila L, Langnaese K 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

    PubMed  CAS  Google Scholar 

  • Trachtenberg JT, Chen BE, Knott GW et al. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788–794

    PubMed  CAS  Google Scholar 

  • Tsui CC, Copeland NG, Gilbert DJ et al. (1996) Narp, a novel member of the pentraxin family, promotes neurite outgrowth and is dynamically regulated by neuronal activity. J Neurosci 16:2463–2478

    PubMed  CAS  Google Scholar 

  • Tu JC, Xiao B, Naisbitt S et al. (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23:583–592

    PubMed  CAS  Google Scholar 

  • Umemori H, Linhoff MW, Ornitz DM et al. (2004) FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118:257–270

    PubMed  CAS  Google Scholar 

  • Umemori H and Sanes JR (2008) Signal regulatory proteins (SIRPS) are secreted presynaptic organizing molecules. J Biol Chem 283:34053–34061

    Google Scholar 

  • Valtschanoff JG and Weinberg RJ (2001) Laminar organization of the NMDA receptor complex within the postsynaptic density. J Neurosci 21:1211–1217

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Verhage M, Maia AS, Plomp JJ et al. (2000) Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287:864–869

    PubMed  CAS  Google Scholar 

  • Waites CL, Craig AM and Garner CC (2005) Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28:251–274

    PubMed  CAS  Google Scholar 

  • Wang PY, Seabold GK and Wenthold RJ (2008) Synaptic adhesion-like molecules (SALMs) promote neurite outgrowth. Mol Cell Neurosci 39:83–94

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Wang Y, Sugita S and Südhof TC (2000) 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 275:20033–20044

    PubMed  CAS  Google Scholar 

  • Webb DJ, Zhang H, Majumdar D et al. (2007) alpha5 integrin signaling regulates the formation of spines and synapses in hippocampal neurons. J Biol Chem 282:6929–6935

    PubMed  CAS  Google Scholar 

  • Weiner JA, Wang X, Tapia JC et al. (2005) Gamma protocadherins are required for synaptic development in the spinal cord. Proc Natl Acad Sci U S A 102:8–14

    PubMed  CAS  Google Scholar 

  • Woo J, Kwon SK, Choi S et al. (2009) Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat Neurosci 12:428–437

    Google Scholar 

  • Wu G, Malinow R and Cline HT (1996) Maturation of a central glutamatergic synapse. Science 274:972–976

    PubMed  CAS  Google Scholar 

  • Yamagata M and Sanes JR (2008) Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451:465–469

    PubMed  CAS  Google Scholar 

  • Yamagata M, Sanes JR and Weiner JA (2003) Synaptic adhesion molecules. Curr Opin Cell Biol 15:621–632

    PubMed  CAS  Google Scholar 

  • Yamaguchi Y and Pasquale EB (2004) Eph receptors in the adult brain. Curr Opin Neurobiol 14:288–296

    PubMed  CAS  Google Scholar 

  • Yao I, Hata Y, Hirao K et al. (1999) Synamon, a novel neuronal protein interacting with synapse-associated protein 90/postsynaptic density-95-associated protein. J Biol Chem 274:27463–27466

    PubMed  CAS  Google Scholar 

  • Yuste R and Bonhoeffer T (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24–34

    PubMed  CAS  Google Scholar 

  • Zhai R, Olias G, Chung WJ et al. (2000) Temporal appearance of the presynaptic cytomatrix protein bassoon during synaptogenesis. Mol Cell Neurosci 15:417–428

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Zhang W and Benson DL (2001) Stages of synapse development defined by dependence on F-actin. J Neurosci 21:5169–5181

    PubMed  CAS  Google Scholar 

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  1. Molecular and Behavioral Neuroscience Institute, University of Michigan, Ann Arbor, MI, 48109, USA

    Masahiro Yasuda & Hisashi Umemori

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  1. Masahiro Yasuda
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  2. Hisashi Umemori
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Correspondence to Hisashi Umemori .

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    Yasuda, M., Umemori, H. (2009). Synapse Formation in the Mammalian Central Nervous System. In: Umemori, H., Hortsch, M. (eds) The Sticky Synapse. Springer, New York, NY. https://doi.org/10.1007/978-0-387-92708-4_4

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