Extracellular matrix molecules and synaptic plasticity (original) (raw)

• Ruoslahti, E. Brain extracellular matrix. Glycobiology 6, 489–492 (1996).
  CAS PubMed Google Scholar
• Nicholson, C. & Sykova, E. Extracellular space structure revealed by diffusion analysis. Trends Neurosci. 21, 207–215 (1998).
  CAS PubMed Google Scholar
• Bruckner, G. et al. Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8, 183–200 (1993).
  CAS PubMed Google Scholar
• Celio, M. R., Spreafico, R., de Biasi, S. & Vitellaro-Zuccarello, L. Perineuronal nets: past and present. Trends Neurosci. 21, 510–515 (1998). This article provides a historical overview on visualization, composition and possible functions of perineuronal nets.
  CAS PubMed Google Scholar
• Yamaguchi, Y. Lecticans: organizers of the brain extracellular matrix. Cell. Mol. Life Sci. 57, 276–289 (2000).
  CAS PubMed Google Scholar
• Bruckner, G. et al. Extracellular matrix organization in various regions of rat brain grey matter. J. Neurocytol. 25, 333–346 (1996).
  CAS PubMed Google Scholar
• Matthews, R. T. et al. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 22, 7536–7547 (2002).
  CAS PubMed PubMed Central Google Scholar
• Faissner, A. & Steindler, D. Boundaries and inhibitory molecules in developing neural tissues. Glia 13, 233–254 (1995).
  CAS PubMed Google Scholar
• Stichel, C. C. & Muller, H. W. The CNS lesion scar: new vistas on an old regeneration barrier. Cell Tissue Res. 294, 1–9 (1998).
  CAS PubMed Google Scholar
• Deller, T., Haas, C. A. & Frotscher, M. Reorganization of the rat fascia dentata after a unilateral entorhinal cortex lesion. Role of the extracellular matrix. Ann. NY Acad. Sci. 911, 207–220 (2000).
  CAS PubMed Google Scholar
• Jones, F. S. & Jones, P. L. The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev. Dyn. 218, 235–259 (2000).
  CAS PubMed Google Scholar
• Bandtlow, C. E. & Zimmermann, D. R. Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 80, 1267–1290 (2000). References 5, 11 and 12 describe interaction partners and functions of ECM molecules.
  CAS PubMed Google Scholar
• Geiger, B., Bershadsky, A., Pankov, R. & Yamada, K. M. Transmembrane crosstalk between the extracellular matrix–cytoskeleton crosstalk. Nature Rev. Mol. Cell Biol. 2, 793–805 (2001).
  CAS Google Scholar
• Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355–405 (2002).
  CAS PubMed Google Scholar
• Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31–39 (1993).
  CAS PubMed Google Scholar
• Malenka, R. C. & Nicoll, R. A. Long-term potentiation — a decade of progress? Science 285, 1870–1874 (1999).
  CAS PubMed Google Scholar
• Lisman, J., Schulman, H. & Cline, H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nature Rev. Neurosci. 3, 175–190 (2002).
  CAS Google Scholar
• Ali, D. W. & Salter, M. W. NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr. Opin. Neurobiol. 11, 336–342 (2001).
  CAS PubMed Google Scholar
• Kandel, E. R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030–1038 (2001).
  CAS PubMed Google Scholar
• Malinow, R. & Malenka, R. C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103–126 (2002). References 14–16 and 20 give nice introductions to the synaptic plasticity field.
  CAS PubMed Google Scholar
• Zakharenko, S. S., Zablow, L. & Siegelbaum, S. A. Visualization of changes in presynaptic function during long-term synaptic plasticity. Nature Neurosci. 4, 711–717 (2001).
  CAS PubMed Google Scholar
• Antonova, I. et al. Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294, 1547–1550 (2001).
  CAS PubMed Google Scholar
• Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).
  CAS PubMed Google Scholar
• Toni, N., Buchs, P. A., Nikonenko, I., Bron, C. R. & Muller, D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421–425 (1999).
  CAS PubMed Google Scholar
• Geinisman, Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb. Cortex 10, 952–962 (2000).
  CAS PubMed Google Scholar
• Abraham, W. C. & Bear, M. F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126–130 (1996).
  CAS PubMed Google Scholar
• Abraham, W. C. & Tate, W. P. Metaplasticity: a new vista across the field of synaptic plasticity. Prog. Neurobiol. 52, 303–323 (1997).
  CAS PubMed Google Scholar
• Wagner, J. J. & Alger, B. E. GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus. J. Neurosci. 15, 1577–1586 (1995).
  CAS PubMed PubMed Central Google Scholar
• Sanes, J. R. & Lichtman, J. W. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nature Rev. Neurosci. 2, 791–805 (2001).
  CAS Google Scholar
• Persohn, E., Pollerberg, G. E. & Schachner, M. Immunoelectron-microscopic localization of the 180 kD component of the neural cell adhesion molecule N-CAM in postsynaptic membranes. J. Comp. Neurol. 288, 92–100 (1989).
  CAS PubMed Google Scholar
• Kalb, R. G. & Hockfield, S. Molecular evidence for early activity-dependent development of hamster motor neurons. J. Neurosci. 8, 2350–2360 (1988).
  CAS PubMed PubMed Central Google Scholar
• Guimaraes, A., Zaremba, S. & Hockfield, S. Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. J. Neurosci. 10, 3014–3024 (1990).
  CAS PubMed PubMed Central Google Scholar
• Staubli, U., Vanderklish, P. & Lynch, G. An inhibitor of integrin receptors blocks long-term potentiation. Behav. Neural Biol. 53, 1–5 (1990).
  CAS PubMed Google Scholar
• Mayford, M., Barzilai, A., Keller, F., Schacher, S. & Kandel, E. R. Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256, 638–644 (1992).
  CAS PubMed Google Scholar
• Lauri, S. E., Rauvala, H., Kaila, K. & Taira, T. Effect of heparin-binding growth-associated molecule (HB-GAM) on synaptic transmission and early LTP in rat hippocampal slices. Eur. J. Neurosci. 10, 188–194 (1998). This study describes the first evidence for the importance of the ECM component HB-GAM in hippocampal LTP.
  CAS PubMed Google Scholar
• Saghatelyan, A. K. et al. The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA1 region of the hippocampus. Eur. J. Neurosci. 12, 3331–3342 (2000). This work and reference 85 provide the first evidence for the importance of tenascin-R and its associated HNK-1 carbohydrate in regulation of perisomatic inhibition and LTP.
  CAS PubMed Google Scholar
• Nakagami, Y., Abe, K., Nishiyama, N. & Matsuki, N. Laminin degradation by plasmin regulates long-term potentiation. J. Neurosci. 20, 2003–2010 (2000).
  CAS PubMed PubMed Central Google Scholar
• Bukalo, O., Schachner, M. & Dityatev, A. Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104, 359–369 (2001). The study is the first to highlight the function of CSPGs in hippocampal LTP and LTD.
  CAS PubMed Google Scholar
• Evers, M. R. et al. Impairment of L-type Ca2+ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J. Neurosci. 22, 7177–7194 (2002). The analysis of seven forms of long-term synaptic plasticity in the dentate gyrus and CA1 and CA3 areas of the hippocampus in the TN-C-deficient mutant disclosed an interplay between TN-C and Ca 2+ channels.
  CAS PubMed PubMed Central Google Scholar
• Wright, J. W., Kramar, E. A., Meighan, S. E. & Harding, J. W. Extracellular matrix molecules, long-term potentiation, memory consolidation and the brain angiotensin system. Peptides 23, 221–246 (2002).
  CAS PubMed Google Scholar
• Sanes, J. R. & Lichtman, J. W. Can molecules explain long-term potentiation? Nature Neurosci. 2, 597–604 (1999).
  CAS PubMed Google Scholar
• Montanaro, F. et al. Laminin and α-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway. J. Neurosci. 18, 1250–1260 (1998).
  CAS PubMed PubMed Central Google Scholar
• Noakes, P. G., Gautam, M., Mudd, J., Sanes, J. R. & Merlie, J. P. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2. Nature 374, 258–262 (1995).
  CAS PubMed Google Scholar
• Patton, B. L. et al. Properly formed but improperly localized synaptic specializations in the absence of laminin α4. Nature Neurosci. 4, 597–604 (2001).
  CAS PubMed Google Scholar
• Marangi, P. A., Wieland, S. T. & Fuhrer, C. Laminin-1 redistributes postsynaptic proteins and requires rapsyn, tyrosine phosphorylation, and Src and Fyn to stably cluster acetylcholine receptors. J. Cell Biol. 157, 883–895 (2002).
  CAS PubMed PubMed Central Google Scholar
• Knight, D., Tolley, L. K., Kim, D. K., Lavidis, N. A. & Noakes, P. G. Functional analysis of neurotransmission at β2-laminin deficient terminals. J. Physiol. (Lond.) 546, 789–800 (2003).
  CAS Google Scholar
• Indyk, J. A., Chen, Z. L., Tsirka, S. E. & Strickland, S. Laminin chain expression suggests that laminin-10 is a major isoform in the mouse hippocampus and is degraded by the tissue plasminogen activator/plasmin protease cascade during excitotoxic injury. Neuroscience 116, 359–371 (2003).
  CAS PubMed Google Scholar
• Nayeem, N. et al. A potential role for the plasmin(ogen) system in the posttranslational cleavage of the neural cell adhesion molecule L1. J. Cell Sci. 112, 4739–4749 (1999).
  CAS PubMed Google Scholar
• Pinkstaff, J. K., Detterich, J., Lynch, G. & Gall, C. Integrin subunit gene expression is regionally differentiated in adult brain. J. Neurosci. 19, 1541–1556 (1999).
  CAS PubMed PubMed Central Google Scholar
• Schuster, T. et al. Immunoelectron microscopic localization of the neural recognition molecules L1, NCAM, and its isoform NCAM180, the NCAM-associated polysialic acid, β1 integrin and the extracellular matrix molecule tenascin-R in synapses of the adult rat hippocampus. J. Neurobiol. 49, 142–158 (2001).
  CAS PubMed Google Scholar
• Xiao, P., Bahr, B. A., Staubli, U., Vanderklish, P. W. & Lynch, G. Evidence that matrix recognition contributes to stabilization but not induction of LTP. Neuroreport 2, 461–464 (1991).
  CAS PubMed Google Scholar
• Staubli, U., Chun, D. & Lynch, G. Time-dependent reversal of long-term potentiation by an integrin antagonist. J. Neurosci. 18, 3460–3469 (1998).
  CAS PubMed PubMed Central Google Scholar
• Chun, D., Gall, C. M., Bi, X. & Lynch, G. Evidence that integrins contribute to multiple stages in the consolidation of long term potentiation in rat hippocampus. Neuroscience 105, 815–829 (2001).
  CAS PubMed Google Scholar
• Kramar, E. A., Bernard, J. A., Gall, C. M. & Lynch, G. α3 integrin receptors contribute to the consolidation of long-term potentiation. Neuroscience 110, 29–39 (2002).
  CAS PubMed Google Scholar
• Caviness, V. S. Jr & Rakic, P. Mechanisms of cortical development: a view from mutations in mice. Annu. Rev. Neurosci. 1, 297–326 (1978).
  PubMed Google Scholar
• Miao, G. G. et al. Isolation of an allele of reeler by insertional mutagenesis. Proc. Natl Acad. Sci. USA 91, 11050–11054 (1994).
  CAS PubMed PubMed Central Google Scholar
• Tissir, F. & Goffinet, A. M. Reelin and brain development. Nature Rev. Neurosci. 4, 496–505 (2003).
  CAS Google Scholar
• Ishida, A., Shimazaki, K., Terashima, T. & Kawai, N. An electrophysiological and immunohistochemical study of the hippocampus of the reeler mutant mouse. Brain Res. 662, 60–68 (1994).
  CAS PubMed Google Scholar
• Weeber, E. J. et al. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J. Biol. Chem. 277, 39944–39952 (2002). A combination of acute perturbation with analysis of mouse mutants deficient in Reln receptors uncovers some functions of Reln in synaptic plasticity.
  CAS PubMed Google Scholar
• Zhuo, M. et al. Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J. Neurosci. 20, 542–549 (2000).
  CAS PubMed PubMed Central Google Scholar
• Verhey, K. J. et al. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152, 959–970 (2001).
  CAS PubMed PubMed Central Google Scholar
• Rauvala, H. & Peng, H. B. HB-GAM (heparin-binding growth-associated molecule) and heparin-type glycans in the development and plasticity of neuron-target contacts. Prog. Neurobiol. 52, 127–144 (1997).
  CAS PubMed Google Scholar
• Amet, L. E. et al. Enhanced hippocampal long-term potentiation in mice lacking heparin-binding growth-associated molecule. Mol. Cell. Neurosci. 17, 1014–1024 (2001).
  CAS PubMed Google Scholar
• Pavlov, I. et al. Role of heparin-binding growth-associated molecule (HB-GAM) in hippocampal LTP and spatial learning revealed by studies on overexpressing and knockout mice. Mol. Cell. Neurosci. 20, 330–342 (2002).
  CAS PubMed Google Scholar
• Lauri, S. E. et al. Regulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (_N_-syndecan) in hippocampal long-term potentiation. J. Neurosci. 19, 1226–1235 (1999).
  CAS PubMed PubMed Central Google Scholar
• Kaksonen, M. et al. Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol. Cell. Neurosci. 21, 158–172 (2002).
  CAS PubMed Google Scholar
• Kinnunen, T. et al. Cortactin-Src kinase signaling pathway is involved in _N_-syndecan-dependent neurite outgrowth. J. Biol. Chem. 273, 10702–10708 (1998).
  CAS PubMed Google Scholar
• Naisbitt, S. et al. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23, 569–582 (1999).
  CAS PubMed Google Scholar
• Sheng, M. & Kim, M. J. Postsynaptic signaling and plasticity mechanisms. Science 298, 776–780 (2002).
  CAS PubMed Google Scholar
• Tsui, C. C. et al. Narp, a novel member of the pentraxin family, promotes neurite outgrowth and is dynamically regulated by neuronal activity. J. Neurosci. 16, 2463–2478 (1996).
  CAS PubMed PubMed Central Google Scholar
• O'Brien, R. J. et al. Synaptic clusterng of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23, 309–323 (1999). A novel mechanism for clustering of AMPA receptors by extracellularly secreted molecule is described.
  CAS PubMed Google Scholar
• O'Brien, R. J. et al. 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 (2002).
  CAS PubMed PubMed Central Google Scholar
• Mi, R. et al. Differing mechanisms for glutamate receptor aggregation on dendritic spines and shafts in cultured hippocampal neurons. J. Neurosci. 22, 7606–7616 (2002).
  CAS PubMed PubMed Central Google Scholar
• Hall, R. A. et al. Effects of heparin on the properties of solubilized and reconstituted rat brain AMPA receptors. Neurosci. Lett. 217, 179–183 (1996).
  CAS PubMed Google Scholar
• Sinnarajah, S. et al. Heparin modulates the single channel kinetics of reconstituted AMPA receptors from rat brain. Synapse 31, 203–209 (1999).
  CAS PubMed Google Scholar
• Faissner, A. & Schachner, M. in Neuroglia (eds Kettenmann, H. & Ransom, B. R.) 422–426 (Oxford Univ. Press, New York, 1995).
  Google Scholar
• Nakic, M., Mitrovic, N., Sperk, G. & Schachner, M. Kainic acid activates transient expression of tenascin-C in the adult rat hippocampus. J. Neurosci. Res. 44, 355–362 (1996).
  CAS PubMed Google Scholar
• Nakic, M., Manahan-Vaughan, D., Reymann, K. G. & Schachner, M. Long-term potentiation in vivo increases rat hippocampal tenascin-C expression. J. Neurobiol. 37, 393–404 (1998).
  CAS PubMed Google Scholar
• Strekalova, T. et al. Fibronectin domains of extracellular matrix molecule tenascin-C modulate hippocampal learning and synaptic plasticity. Mol. Cell. Neurosci. 21, 173–187 (2002). A combined cell biological, electrophysiological and behavioural study on a distinct domain of TN-C in synaptic plasticity.
  CAS PubMed Google Scholar
• Dorries, U. et al. Distinct effects of recombinant tenascin-C domains on neuronal cell adhesion, growth cone guidance, and neuronal polarity. J. Neurosci. Res. 43, 420–438 (1996).
  CAS PubMed Google Scholar
• Srinivasan, J., Schachner, M. & Catterall, W. A. Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc. Natl Acad. Sci. USA 95, 15753–15757 (1998). References 79–81 highlight the interactions between ion channels and ECM molecules.
  CAS PubMed PubMed Central Google Scholar
• Weber, P. et al. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J. Neurosci. 19, 4245–4262 (1999).
  CAS PubMed PubMed Central Google Scholar
• Xiao, Z. C. et al. Tenascin-R is a functional modulator of sodium channel β-subunits. J. Biol. Chem. 274, 26511–26517 (1999).
  CAS PubMed Google Scholar
• Bruckner, G. et al. Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J. Comp. Neurol. 428, 616–629 (2000).
  CAS PubMed Google Scholar
• Saghatelyan, A. K. et al. Reduced perisomatic inhibition, increased excitatory transmission and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol. Cell. Neurosci. 17, 226–240 (2001).
  CAS PubMed Google Scholar
• Schachner, M. & Martini, R. Glycans and the modulation of neural-recognition molecule function. Trends Neurosci. 18, 183–191 (1995).
  CAS PubMed Google Scholar
• Yamamoto, S. et al. Mice deficient in nervous system-specific carbohydrate epitope HNK-1 exhibit impaired synaptic plasticity and spatial learning. J. Biol. Chem. 277, 27227–27231 (2002).
  CAS PubMed Google Scholar
• Senn, C. et al. Mice deficient for the HNK-1 sulfotransferase show alterations in synaptic efficacy and spatial learning and memory. Mol. Cell. Neurosci. 20, 712–729 (2002).
  CAS PubMed Google Scholar
• Nikonenko, A., Schmidt, S., Skibo, G., Bruckner, G. & Schachner, M. Tenascin-R-deficient mice show structural alterations of symmetric perisomatic synapses in the CA1 region of the hippocampus. J. Comp. Neurol. 456, 338–349 (2003).
  CAS PubMed Google Scholar
• Saghatelyan, A. K. et al. Recognition molecule associated carbohydrate inhibits postsynaptic GABAB receptors: a mechanism for homeostatic regulation of GABA release in perisomatic synapses. Mol. Cell. Neurosci. (in the press).
• Niederost, B. P., Zimmermann, D. R., Schwab, M. E. & Bandtlow, C. E. Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J. Neurosci. 19, 8979–8989 (1999).
  CAS PubMed PubMed Central Google Scholar
• Bradbury, E. J. et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636–640 (2002).
  CAS PubMed Google Scholar
• Pizzorusso, T. et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248–1251 (2002). The importance of CSPGs in regulating synaptic plasticity in the visual cortex in vivo is elegantly demonstrated in this paper.
  CAS PubMed Google Scholar
• Brakebusch, C. et al. Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol. Cell. Biol. 22, 7417–7427 (2002). This study shows that injection of brevican antibody and genetic ablation of brevican lead to abolishment of LTP.
  CAS PubMed PubMed Central Google Scholar
• Miura, R., Ethell, I. M. & Yamaguchi, Y. Carbohydrate-protein interactions between HNK-1-reactive sulfoglucuronyl glycolipids and the proteoglycan lectin domain mediate neuronal cell adhesion and neurite outgrowth. J. Neurochem. 76, 413–424 (2001).
  CAS PubMed Google Scholar
• Zhou, X. H. et al. Neurocan is dispensable for brain development. Mol. Cell. Biol. 21, 5970–5978 (2001).
  CAS PubMed PubMed Central Google Scholar
• Ngezahayo, A., Schachner, M. & Artola A. Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus. J. Neurosci. 20, 2451–2458 (2000). A patch-clamp study that provides a framework for evaluation of depolarization thresholds for induction of LTP and LTD.
  CAS PubMed PubMed Central Google Scholar
• Fagiolini, M. & Hensch, T. K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404, 183–186 (2000).
  CAS PubMed Google Scholar
• Rusakov, D. A. & Kullmann, D. M. Geometric and viscous components of the tortuosity of the extracellular space in the brain. Proc. Natl Acad. Sci. USA 95, 8975–8980 (1998).
  CAS PubMed PubMed Central Google Scholar
• Tian, M. et al. Laminin-α2 chain-like antigens in CNS dendritic spines. Brain Res. 764, 28–38 (1997).
  CAS PubMed Google Scholar
• Pappas, G. D., Kriho, V. & Pesold, C. Reelin in the extracellular matrix and dendritic spines of the cortex and hippocampus: a comparison between wild type and heterozygous reeler mice by immunoelectron microscopy. J. Neurocytol. 30, 413–425 (2001).
  CAS PubMed Google Scholar
• Wan, H. I. et al. Highwire regulates synaptic growth in Drosophila. Neuron 26, 313–329 (2000).
  CAS PubMed Google Scholar
• Sytnyk, V. et al. NCAM promotes accumulation of trans-Golgi network organelles at sites of neuron-to-neuron contacts. J. Cell Biol. 159, 649–661 (2002).
  CAS PubMed PubMed Central Google Scholar
• Son, Y. J. et al. The synaptic vesicle protein SV2 is complexed with an α5-containing laminin on the nerve terminal surface. J. Biol. Chem. 275, 451–460 (2000).
  CAS PubMed Google Scholar
• Brown, E. J. Integrin-associated proteins. Curr. Opin. Cell Biol. 14, 603–607 (2002).
  CAS PubMed Google Scholar
• Chavis, P. & Westbrook, G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411, 317–321 (2001).
  CAS PubMed Google Scholar
• Beattie, E. C. et al. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nature Neurosci. 3, 1291–1300 (2000).
  CAS PubMed Google Scholar
• Passafaro, M., Piech, V. & Sheng, M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nature Neurosci. 4, 917–926 (2001).
  CAS PubMed Google Scholar
• Skeberdis, V. A., Lan, J., Zheng, X., Zukin, R. S. & Bennett, M. V. Insulin promotes rapid delivery of N-methyl-D-aspartate receptors to the cell surface by exocytosis. Proc. Natl Acad. Sci. USA 98, 3561–3566 (2001).
  CAS PubMed PubMed Central Google Scholar
• Wan, Q. et al. Recruitment of functional GABAA receptors to postsynaptic domains by insulin. Nature 388, 686–690 (1997).
  CAS PubMed Google Scholar
• Zhu, J., Qin, Y., Zhao, M., Van Aelst, L. & Malinow, R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110, 443–455 (2002). The study provides strong evidence for the involvement of small GTPases in receptor trafficking during LTP and LTD.
  CAS PubMed Google Scholar
• Sin, W. C., Haas, K., Ruthazer, E. S. & Cline, H. T. Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419, 475–480 (2002).
  CAS PubMed Google Scholar
• Ivins, J. K., Yurchenco, P. D. & Lander, A. D. Regulation of neurite outgrowth by integrin activation. J. Neurosci. 20, 6551–6560 (2000).
  CAS PubMed PubMed Central Google Scholar
• Bass, M. D. & Humphries, M. J. Cytoplasmic interactions of syndecan-4 orchestrate adhesion receptor and growth factor receptor signalling. Biochem. J. 368, 1–15 (2002).
  CAS PubMed PubMed Central Google Scholar
• Damsky, C. H. & Ilic, D. Integrin signaling: it's where the action is. Curr. Opin. Cell Biol. 14, 594–602 (2002).
  CAS PubMed Google Scholar
• Ziv, N. E. & Smith, S. J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91–102 (1996).
  CAS PubMed Google Scholar
• Shupliakov, O. et al. Impaired recycling of synaptic vesicles after acute perturbation of thepresynaptic actin cytoskeleton. Proc. Natl Acad. Sci. USA 99, 14476–14481 (2002).
  CAS PubMed PubMed Central Google Scholar
• Chang, S. & de Camilli, P. Glutamate regulates actin-based motility in axonal filopodia. Nature Neurosci. 4, 787–793 (2001).
  CAS PubMed Google Scholar
• Tanaka, H. et al. Molecular modification of N-cadherin in response to synaptic activity. Neuron 25, 93–107 (2000).
  CAS PubMed Google Scholar
• Scheiffele, P., Fan, J., Choih, J., Fetter, R. & Serafini, T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101, 657–669 (2000).
  CAS PubMed Google Scholar
• Biederer, T. et al. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525–1531 (2002).
  CAS PubMed Google Scholar
• Contractor, A. et al. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296, 1864–1869 (2002).
  CAS PubMed Google Scholar
• Cole, G. J. & Glaser, L. A heparin-binding domain from N-CAM is involved in neural cell-substratum adhesion. J. Cell Biol. 102, 403–412 (1986).
  CAS PubMed Google Scholar
• Storms, S. D., Kim, A. C., Tran, B. H., Cole, G. J. & Murray, B. A. NCAM-mediated adhesion of transfected cells to agrin. Cell Adhes. Commun. 3, 497–509 (1996).
  CAS PubMed Google Scholar
• Kwan, C. P. et al. Probing fibroblast growth factor dimerization and role of heparin-like glycosaminoglycans in modulating dimerization and signaling. J. Biol. Chem. 276, 23421–23429 (2001).
  CAS PubMed Google Scholar
• Frame, M. C., Fincham, V. J., Carragher, N. O. & Wyke, J. A. v-Src's hold over actin and cell adhesions. Nature Rev. Mol. Cell Biol. 3, 233–245 (2002).
  CAS Google Scholar
• Fazeli, M. S., Breen, K., Errington, M. L. & Bliss, T. V. Increase in extracellular NCAM and amyloid precursor protein following induction of long-term potentiation in the dentate gyrus of anaesthetized rats. Neurosci. Lett. 169, 77–80 (1994).
  CAS PubMed Google Scholar
• Kalus, I., Schnegelsberg, B., Seidah, N. G., Kleene, R. & Schachner, M. The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1. J. Biol. Chem. 278, 10381–10388 (2003).
  CAS PubMed Google Scholar
• Wu, Y. P. et al. The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J. Cell Biol. 148, 1295–1304 (2000).
  CAS PubMed PubMed Central Google Scholar
• Baranes, D. et al. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21, 813–825 (1998).
  CAS PubMed Google Scholar
• Calabresi, P. et al. Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur. J. Neurosci. 12, 1002–1012 (2000).
  CAS PubMed Google Scholar
• Komai, S. et al. Neuropsin regulates an early phase of Schaffer-collateral long-term potentiation in the murine hippocampus. Eur. J. Neurosci. 12, 1479–1486 (2000).
  CAS PubMed Google Scholar
• Hirata, A. et al. Abnormalities of synapses and neurons in the hippocampus of neuropsin-deficient mice. Mol. Cell. Neurosci. 17, 600–610 (2001).
  CAS PubMed Google Scholar
• D'Arcangelo, G. et al. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719–723 (1995).
  CAS PubMed Google Scholar
• Shrive, A. K. et al. Three dimensional structure of human C-reactive protein. Nat. Struct. Biol. 3, 346–354 (1996).
  CAS PubMed Google Scholar