Please wait a minute...
Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

Postal Subscription Code 80-984

2018 Impact Factor: 7.575

Protein Cell    2014, Vol. 5 Issue (6) : 420-444    https://doi.org/10.1007/s13238-014-0054-z      PMID: 24756565
REVIEW
Intercellular protein-protein interactions at synapses
Xiaofei Yang1,*(),Dongmei Hou1,2,3,Wei Jiang1,2,3,Chen Zhang2,3,*()
1. Key Laboratory of Cognitive Science, Laboratory of Membrane Ion Channels and Medicine, College of Biomedical Engineering, South-Central University for Nationalities, Wuhan 430074, China
2. State Key Laboratory of Biomembrane and Membrane Biotechnology, College of Life Sciences, Peking University, Beijing 100871, China
3. PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing 100871, China
 Download: PDF(348 KB)  
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Chemical synapses are asymmetric intercellular junctions through which neurons send nerve impulses to communicate with other neurons or excitable cells. The appropriate formation of synapses, both spatially and temporally, is essential for brain function and depends on the intercellular protein-protein interactions of cell adhesion molecules (CAMs) at synaptic clefts. The CAM proteins link pre- and post-synaptic sites, and play essential roles in promoting synapse formation and maturation, maintaining synapse number and type, accumulating neurotransmitter receptors and ion channels, controlling neuronal differentiation, and even regulating synaptic plasticity directly. Alteration of the interactions of CAMs leads to structural and functional impairments, which results in many neurological disorders, such as autism, Alzheimer’s disease and schizophrenia. Therefore, it is crucial to understand the functions of CAMs during development and in the mature neural system, as well as in the pathogenesis of some neurological disorders. Here, we review the function of the major classes of CAMs, and how dysfunction of CAMs relates to several neurological disorders.

Keywords synapse formation      cell-cell adhesion      synaptic plasticity      neurological disorders      protein-protein interaction      cell adhesion molecules     
Corresponding Author(s): Xiaofei Yang   
Issue Date: 25 June 2014
 Cite this article:   
Xiaofei Yang,Dongmei Hou,Wei Jiang, et al. Intercellular protein-protein interactions at synapses[J]. Protein Cell, 2014, 5(6): 420-444.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-014-0054-z
https://academic.hep.com.cn/pac/EN/Y2014/V5/I6/420
1 Aiga M, Levinson JN, Bamji SX (2011) N-cadherin and neuroligins cooperate to regulate synapse formation in hippocampal cultures. J Biol Chem286: 851-858
doi: 10.1074/jbc.M110.176305
2 Akert K, Streit P, Sandri C, Livingston R, Moor H (1972) Synapses as indicators of elevated and depressed activity. An electron microscopic analysis. Schweiz Arch Neurol Neurochir Psychiatr111: 227-236
3 Andreyeva A, Nieweg K, Horstmann K, Klapper S, Müller-Schiffmann A, Korth C, Gottmann K (2012) C-terminal fragment of N-cadherin accelerates synapse destabilization by amyloid-β. Brain135: 2140-2154
doi: 10.1093/brain/aws120
4 Ango F, di Cristo G, Higashiyama H, Bennett V, Wu P, Huang ZJ (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell119: 257-272
doi: 10.1016/j.cell.2004.10.004
5 Ango F, Wu C, Van der Want JJ, Wu P, Schachner M, Huang ZJ (2008) Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biol6: e103
doi: 10.1371/journal.pbio.0060103
6 Antion MD, Christie LA, Bond AM, Dalva MB, Contractor A (2010) Ephrin-B3 regulates glutamate receptor signaling at hippocampal synapses. Mol Cell Neurosci45: 378-388
doi: 10.1016/j.mcn.2010.07.011
7 Aoto J, Ting P, Maghsoodi B, Xu N, Henkemeyer M, Chen L (2007) Post-synaptic ephrinB3 promotes shaft glutamatergic synapse formation. J Neurosci27: 7508-7519
doi: 10.1523/JNEUROSCI.0705-07.2007
8 Aoto J, Martinelli DC, Malenka RC, Tabuchi K, Südhof TC (2013) Pre-synaptic neurexin-3 alternative splicing trans-synaptically controls post-synaptic AMPA receptor trafficking. Cell154: 75-88
doi: 10.1016/j.cell.2013.05.060
9 Ara? D, Boucard AA, Ozkan E, Strop P, Newell E, Südhof TC, Brunger AT (2007) Structures of neuroligin-1 and the neuroligin-1/neurexin-1 beta complex reveal specific protein-protein and protein-Ca2+interactions. Neuron56: 992-1003
doi: 10.1016/j.neuron.2007.12.002
10 Armstrong JN, Saganich MJ, Xu NJ, Henkemeyer M, Heinemann SF, Contractor A (2006) B-ephrin reverse signaling is required for NMDA-independent long-term potentiation of mossy fibers in the hippocampus. J Neurosci26: 3474-3481
doi: 10.1523/JNEUROSCI.4338-05.2006
11 Asada-Utsugi M, Uemura K, Noda Y, Kuzuya A, Maesako M, Ando K, Kubota M, Watanabe K, Takahashi M, Kihara T, Shimohama S, Takahashi R, Berezovska O, Kinoshita A (2011) N-cadherin enhances APP dimerization at the extracellular domain and modulates Aβ production. J Neurochem119: 354-363
doi: 10.1111/j.1471-4159.2011.07364.x
12 Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B, Reichardt LF (2003) Role of beta-catenin in synaptic vesicle localization and pre-synaptic assembly. Neuron40: 719-731
doi: 10.1016/S0896-6273(03)00718-9
13 Barbeau D, Liang JJ, Robitalille Y, Quirion R, Srivastava LK (1995) Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc Natl Acad Sci USA92: 2785-2789
doi: 10.1073/pnas.92.7.2785
14 Barrow SL, Constable JR, Clark E, El-Sabeawy F, McAllister AK, Washbourne P (2009) Neuroligin1: a cell adhesion molecule that recruits PSD-95 and NMDA receptors by distinct mechanisms during synaptogenesis. Neural Dev4: 17
doi: 10.1186/1749-8104-4-17
15 Bateman A, Jouet M, MacFarlane J, Du JS, Kenwrick S, Chothia C (1996) Outline structure of the human L1 cell adhesion molecule and the sites where mutations cause neurological disorders. EMBO J15: 6050-6059
16 Baudouin S, Scheiffele P (2010) SnapShot: Neuroligin-neurexin complexes. Cell141(908): 908
doi: 10.1016/j.cell.2010.05.024
17 Bayés A, van de Lagemaat LN, Collins MO, Croning MD, Whittle IR, Choudhary JS, Grant SG (2011) Characterization of the proteome, diseases and evolution of the human post-synaptic density. Nat Neurosci14: 19-21
doi: 10.1038/nn.2719
18 Benson DL, Tanaka H (1998) N-cadherin redistribution during synaptogenesis in hippocampal neurons. J Neurosci18: 6892-6904
19 Berninghausen O, Rahman MA, Silva JP, Davletov B, Hopkins C, Ushkaryov YA (2007) Neurexin Ibeta and neuroligin are localized on opposite membranes in mature central synapses. J Neurochem103: 1855-1863
doi: 10.1111/j.1471-4159.2007.04918.x
20 Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Südhof TC (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science297: 1525-1531
doi: 10.1126/science.1072356
21 Blair IP, Chetcuti AF, Badenhop RF, Scimone A, Moses MJ, Adams LJ, Craddock N, Green E, Kirov G, Owen MJ, Kwok JB, Donald JA, Mitchell PB, Schofield PR (2006) Positional cloning, association analysis and expression studies provide convergent evidence that the cadherin gene FAT contains a bipolar disorder susceptibility allele. Mol Psychiatry11: 372-383
doi: 10.1038/sj.mp.4001784
22 Bloom FE, Aghajanian GK (1966) Cytochemistry of synapses: selective staining for electron microscopy. Science154: 1575-1577
doi: 10.1126/science.154.3756.1575
23 Borg JP, L?pez-Figueroa MO, de Taddèo-Borg M, Kroon DE, Turner RS, Watson SJ, Margolis B (1999) Molecular analysis of the X11-mLin-2/CASK complex in brain. J Neurosci19: 1307-1316
24 Bot N, Schweizer C, Ben Halima S, Fraering PC (2011) Processing of the synaptic cell adhesion molecule neurexin-3beta by Alzheimer disease alpha- and gamma-secretases. J Biol Chem286: 2762-2773
doi: 10.1074/jbc.M110.142521
25 Boucard AA, Chubykin AA, Comoletti D, Taylor P, Südhof TC (2005) A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron48: 229-236
doi: 10.1016/j.neuron.2005.08.026
26 Bourgin C, Murai KK, Richter M, Pasquale EB (2007) The EphA4 receptor regulates dendritic spine remodeling by affecting beta1-integrin signaling pathways. J Cell Biol178: 1295-1307
doi: 10.1083/jcb.200610139
27 Bouzioukh F, Wilkinson GA, Adelmann G, Frotscher M, Stein V, Klein R (2007) Tyrosine phosphorylation sites in ephrinB2 are required for hippocampal long-term potentiation but not long-term depression. J Neurosci7: 1279-1288
28 Bozdagi O, Wang XB, Nikitczuk JS, Anderson TR, Bloss EB, Radice GL, Zhou Q, Benson DL, Huntley GW (2010) Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J Neurosci30: 9984-9989
doi: 10.1523/JNEUROSCI.1223-10.2010
29 Brigidi GS, Bamji SX (2011) Cadherin-catenin adhesion complexes at the synapse. Curr Opin Neurobiol21: 208-214
doi: 10.1016/j.conb.2010.12.004
30 Broeke JH, Roelandse M, Luteijn MJ, Boiko T, Matus A, Toonen RF, Verhage M (2010) Munc18 and Munc13 regulate early neurite outgrowth. Biol Cell102: 479-488
doi: 10.1042/BC20100036
31 Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi HM (2007) Forecasting the global burden of Alzheimer’s disease. Alzheimers Dement3: 186-191
doi: 10.1016/j.jalz.2007.04.381
32 Bukalo O, Dityatev A (2012) Synaptic cell adhesion molecules. Adv Exp Med Biol970: 97-128
doi: 10.1007/978-3-7091-0932-8_5
33 Bukalo O, Fentrop N, Lee AY, Salmen B, Law JW, Wotjak CT, Schweizer M, Dityatev A, Schachner M (2004) Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus. J Neurosci24: 1565-1577
doi: 10.1523/JNEUROSCI.3298-03.2004
34 Buttiglione M, Revest JM, Rougon G, Faivre-Sarrailh C (1996) F3 neuronal adhesion molecule controls outgrowth and fasciculation of cerebellar granule cell neurites: a cell-type-specific effect mediated by the Ig-like domains. Mol Cell Neurosci8: 53-69
doi: 10.1006/mcne.1996.0043
35 Butz S, Okamoto M, Südhof TC (1998) A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell94: 773-782
doi: 10.1016/S0092-8674(00)81736-5
36 Carrasquillo MM, Zou F, Pankratz VS, Wilcox SL, Ma L, Walker LP, Younkin SG, Younkin CS, Younkin LH, Bisceglio GD, Ertekin-Taner N, Crook JE, Dickson DW, Petersen RC, Graff-Radford NR, Younkin SG (2009) Genetic variation in PCDH11X is associated with susceptibility to late-onset Alzheimer’s disease. Nat Genet41: 192-198
doi: 10.1038/ng.305
37 Chagnon MJ, Uetani N, Tremblay ML (2004) Functional significance of the LAR receptor protein tyrosine phosphatase family in development and diseases. Biochem Cell Biol82: 664-675
doi: 10.1139/o04-120
38 Chan SA, Polo-Parada L, Landmesser LT, Smith C (2005) Adrenal chromaffin cells exhibit impaired granule trafficking in NCAM knockout mice. J Neurophysiol94: 1037-1047
doi: 10.1152/jn.01213.2004
39 Chang S, Rathjen FG, Raper JA (1987) Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J Cell Biol104: 355-662
doi: 10.1083/jcb.104.2.355
40 Chapman NH, Estes A, Munson J, Bernier R, Webb SJ, Rothstein JH, Minshew NJ, Dawson G, Schellenberg GD, Wijsman EM (2011) Genome-scan for IQ discrepancy in autism: evidence for loci on chromosomes 10 and 16. Hum Genet129: 59-70
doi: 10.1007/s00439-010-0899-z
41 Chattopadhyaya B, Baho E, Huang ZJ, Schachner M, Di Cristo G (2013) Neural cell adhesion molecule-mediated Fyn activation promotes GABAergic synapse maturation in postnatal mouse cortex. J Neurosci33: 5957-5968
doi: 10.1523/JNEUROSCI.1306-12.2013
42 Chavis P, Westbrook G (2001) Integrins mediate functional pre- and post-synaptic maturation at a hippocampal synapse. Nature411: 317-321
doi: 10.1038/35077101
43 Chen BM, Grinnell AD (1995) Integrins and modulation of transmitter release from motor nerve terminals by stretch. Science269: 1578-1580
doi: 10.1126/science.7667637
44 Chen X, Liu H, Shim AH, Focia PJ, He X (2008) Structural basis for synaptic adhesion mediated by neuroligin-neurexin interactions. Nat Struct Mol Biol15: 50-56
doi: 10.1038/nsmb1350
45 Chen F, Venugopal V, Murray B, Rudenko G (2011) The structure of neurexin 1α reveals features promoting a role as synaptic organizer. Structure19: 779-789
doi: 10.1016/j.str.2011.03.012
46 Chen Y, Fu AK, Ip NY (2012) Eph receptors at synapses: implications in neurodegenerative diseases. Cell Signal24: 606-611
doi: 10.1016/j.cellsig.2011.11.016
47 Cheng D, Hoogenraad CC, Rush J, Ramm E, Schlager MA, Duong DM, Xu P, Wijayawardana SR, Hanfelt J, Nakagawa T, Sheng M, Peng J (2006) Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol Cell Proteomics5: 1158-1170
doi: 10.1074/mcp.D500009-MCP200
48 Chih B, Afridi SK, Clark L, Scheiffele P (2004) Disorder-associated mutations lead to functional inactivation of neuroligins : 1471-1477
doi: 10.1093/hmg/ddh158
49 Chih B, Engelman H, Scheiffele P (2005) Control of excitatory and inhibitory synapse formation by neuroligins. Science307: 1324-1328
doi: 10.1126/science.1107470
50 Chih B, Gollan L, Scheiffele P (2006) Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron51: 171-178
doi: 10.1016/j.neuron.2006.06.005
51 Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell120: 421-433
doi: 10.1016/j.cell.2004.12.020
52 Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR, Südhof TC (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron54: 919-931
doi: 10.1016/j.neuron.2007.05.029
53 Cingolani LA, Thalhammer A, Yu LM, Catalano M, Ramos T, Colicos MA, Goda Y (2008) Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron58: 749-762
doi: 10.1016/j.neuron.2008.04.011
54 Cissé M, Halabisky B, Harris J, Devidze N, Dubal DB, Sun B, Orr A, Lotz G, Kim DH, Hamto P, Ho K, Yu GQ, Mucke L (2011) Reversing EphB2 depletion rescues cognitive functions in Alzheimer model. Nature469: 47-52
doi: 10.1038/nature09635
55 Clifford MA, Kanwal JK, Dzakpasu R, Donoghue MJ (2011) EphA4 expression promotes network activity and spine maturation in cortical neuronal cultures. Neural Dev6: 21
doi: 10.1186/1749-8104-6-21
56 Collins MO, Husi H, Yu L, Brandon JM, Anderson CN, Blackstock WP, Choudhary JS, Grant SG (2006) Molecular characterization and comparison of the components and multiprotein complexes in the post-synaptic proteome. J Neurochem97: 16-23
doi: 10.1111/j.1471-4159.2005.03507.x
57 Comoletti D, De Jaco A, Jennings LL, Flynn RE, Gaietta G, Tsigelny I, Ellisman MH, Taylor P (2004) The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing. J Neurosci24: 4889-4893
doi: 10.1523/JNEUROSCI.0468-04.2004
58 Comoletti D, Flynn RE, Boucard AA, Demeler B, Schirf V, Shi J, Jennings LL, Newlin HR, Südhof TC, Taylor P (2006) Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for beta-neurexins. Biochemistry45: 12816-12827
doi: 10.1021/bi0614131
59 Conrad AJ, Scheibel AB (1987) Schizophrenia and the hippocampus: the embryological hypothesis extended. Schizophr Bull13: 577-587
doi: 10.1093/schbul/13.4.577
60 Contractor A, Rogers C, Maron C, Henkemeyer M, Swanson GT, Heinemann SF (2002) Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science296: 1864-1869
doi: 10.1126/science.1069081
61 Cotman CW, Taylor D (1972) Isolation and structural studies on synaptic complexes from rat brain. J Cell Biol55: 696-711
doi: 10.1083/jcb.55.3.696
62 Cottrell CE, Bir N, Varga E, Alvarez CE, Bouyain S, Zernzach R, Thrush DL, Evans J, Trimarchi M, Butter EM, Cunningham D, Gastier-Foster JM, McBride KL, Herman GE (2011) Contactin 4 as an autism susceptibility locus. Autism Res4: 189-199
doi: 10.1002/aur.184
63 Craig AM, Kang Y (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol17: 43-52
doi: 10.1016/j.conb.2007.01.011
64 Daar IO (2012) Non-SH2/PDZ reverse signaling by ephrins. Semin Cell Dev Biol23: 65-74
doi: 10.1016/j.semcdb.2011.10.012
65 Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: signalling functions at the synapse. Nat Rev Neurosci8: 206-220
doi: 10.1038/nrn2075
66 Davy A, Soriano P (2005) Ephrin signaling in vivo: look both ways. Dev Dyn232: 1-10
doi: 10.1002/dvdy.20200
67 De Angelis E, MacFarlane J, Du JS, Yeo G, Hicks R, Rathjen FG, Kenwrick S, Brümmendorf T (1999) Pathological missense mutations of neural cell adhesion molecule L1 affect homophilic and heterophilic binding activities. EMBO J18: 4744-4753
doi: 10.1093/emboj/18.17.4744
68 De Strooper B (2003) Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron38: 9-12
doi: 10.1016/S0896-6273(03)00205-8
69 de Wit J, Sylwestrak E, O’Sullivan ML, Otto S, Tiglio K, Savas JN, Yates JR3rd, Comoletti D, Taylor P, Ghosh A (2009) LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron64: 799-806
doi: 10.1016/j.neuron.2009.12.019
70 Deininger K, Eder M, Kramer ER, Zieglg?nsberger W, Dodt HU, Dornmair K, Colicelli J, Klein R (2008) The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proc Natl Acad Sci USA105: 12539-12544
doi: 10.1073/pnas.0801174105
71 Di Luca M, Baker M, Corradetti R, Kettenmann H, Mendlewicz J, Olesen J, Ragan I, Westphal M (2011) Consensus document on European brain research. Eur J Neurosci33: 768-818
doi: 10.1111/j.1460-9568.2010.07596.x
72 Dickinson BA, Jo J, Seok H, Son GH, Whitcomb DJ, Davies CH, Sheng M, Collingridge GL, Cho K (2009) A novel mechanism of hippocampal LTD involving muscarinic receptor-triggered interactions between AMPARs, GRIP and liprin-alpha. Mol Brain2: 18
doi: 10.1186/1756-6606-2-18
73 Dityatev A, Dityateva G, Schachner M (2000) Synaptic strength as a function of post- versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron26: 207-217
doi: 10.1016/S0896-6273(00)81151-4
74 Dosemeci A, Tao-Cheng JH, Vinade L, Jaffe H (2006) Preparation of post-synaptic density fraction from hippocampal slices and proteomic analysis. Biochem Biophys Res Commun339: 687-694
doi: 10.1016/j.bbrc.2005.11.069
75 Dunah AW, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, Simonetta A, Liu G, Sheng M (2005) LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci8: 458-467
76 Egea J, Klein R (2007) Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol17: 230-238
doi: 10.1016/j.tcb.2007.03.004
77 Fannon AM, Colman DR (1996) A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron17: 423-434
doi: 10.1016/S0896-6273(00)80175-0
78 Fantin M, van der Kooij MA, Grosse J, Krummenacher C, Sandi C (2013) A key role for nectin-1 in the ventral hippocampus in contextual fear memory. PLoS One8: e56897
doi: 10.1371/journal.pone.0056897
79 Feng J, Schroer R, Yan J, Song W, Yang C, Bockholt A, Cook EH Jr, Skinner C, Schwartz CE, Sommer SS (2006) High frequency of neurexin 1beta signal peptide structural variants in patients with autism. Neurosci Lett409: 10-13
doi: 10.1016/j.neulet.2006.08.017
80 Fernandez T, Morgan T, Davis N, Klin A, Morris A, Farhi A, Lifton RP, State MW (2004) Disruption of contactin 4 (CNTN4) results in developmental delay and other features of 3p deletion syndrome. Am J Hum Genet74: 1286-1293
doi: 10.1086/421474
81 Fernández E, Collins MO, Uren RT, Kopanitsa MV, Komiyama NH, Croning MD, Zografos L, Armstrong JD, Choudhary JS, Grant SG (2009) Targeted tandem affinity purification of PSD-95 recovers core post-synaptic complexes and schizophrenia susceptibility proteins. Mol Syst Biol5: 269
doi: 10.1038/msb.2009.27
82 Filosa A, Paix?o S, Honsek SD, Carmona MA, Becker L, Feddersen B, Gaitanos L, Rudhard Y, Schoepfer R, Klopstock T, Kullander K, Rose CR, Pasquale EB, Klein R (2009) Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat Neurosci12: 1285-1292
doi: 10.1038/nn.2394
83 Fischer G, Künemund V, Schachner M (1986) Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1. J Neurosci6: 605-612
84 Fogel AI, Akins MR, Krupp AJ, Stagi M, Stein V, Biederer T (2007) SynCAMs organize synapses through heterophilic adhesion. J Neurosci27: 12516-12530
doi: 10.1523/JNEUROSCI.2739-07.2007
85 Fogel AI, Stagi M, Perez de Arce K, Biederer T (2011) Lateral assembly of the immunoglobulin protein SynCAM 1 controls its adhesive function and instructs synapse formation. EMBO J30: 4728-4738
doi: 10.1038/emboj.2011.336
86 Fu WY, Chen Y, Sahin M, Zhao XS, Shi L, Bikoff JB, Lai KO, Yung WH, Fu AK, Greenberg ME, Ip NY (2007) Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat Neurosci10: 67-76
doi: 10.1038/nn1811
87 Fu AK, HungK W, FuW Y, Shen C, Chen Y, Xia J, Lai KO, Ip NY (2011) APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nat Neurosci14: 181-189
doi: 10.1038/nn.2715
88 Giagtzoglou N, Ly CV, Bellen HJ (2009) Cell adhesion, the backbone of the synapse: “vertebrate” and “invertebrate” perspectives. Cold Spring Harb Perspect Biol1: a003079
doi: 10.1101/cshperspect.a003079
89 Gil OD, Zhang L, Chen S, Ren YQ, Pimenta A, Zanazzi G, Hillman D, Levitt P, Salzer JL (2002) Complementary expression and heterophilic interactions between IgLON family members neurotrimin and LAMP. J Neurobiol51: 190-204
doi: 10.1002/neu.10050
90 Giza JI, Jung Y, Jeffrey RA, Neugebauer NM, Picciotto MR, Biederer T (2013) The synaptic adhesion molecule SynCAM 1 contributes to cocaine effects on synapse structure and psychostimulant behavior. Neuropsychopharmacology38: 628-638
doi: 10.1038/npp.2012.226
91 Gokce O, Südhof TC (2013) Membrane-tethered monomeric neurexin LNS-domain triggers synapse formation. J Neurosci33: 14617-14628
doi: 10.1523/JNEUROSCI.1232-13.2013
92 Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature183: 1592-1593
doi: 10.1038/1831592a0
93 Grunwald IC, Korte M, Wolfer D, Wilkinson GA, Unsicker K, Lipp HP, Bonhoeffer T, Klein R (2001) Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron32: 1027-1040
doi: 10.1016/S0896-6273(01)00550-5
94 Grunwald IC, Korte M, Adelmann G, Plueck A, Kullander K, Adams RH, Frotscher M, Bonhoeffer T, Klein R (2004) Hippocampal plasticity requires post-synaptic ephrinBs. Nat Neurosci7: 33-40
doi: 10.1038/nn1164
95 Guan H, Maness PF (2010) Perisomatic GABAergic innervation in prefrontal cortex is regulated by ankyrin interaction with the L1 cell adhesion molecule. Cereb Cortex20: 2684-2693
doi: 10.1093/cercor/bhq016
96 Guo H, Xun G, Peng Y, Xiang X, Xiong Z, Zhang L, He Y, Xu X, Liu Y, Lu L, Long Z, Pan Q, Hu Z, Zhao J, Xia K (2012) Disruption of Contactin 4 in two subjects with autism in Chinese population. Gene505: 201-205
doi: 10.1016/j.gene.2012.06.051
97 Hahn CG, Banerjee A, Macdonald ML, Cho DS, Kamins J, Nie Z, Borgmann-Winter KE, Grosser T, Pizarro A, Ciccimaro E, Arnold SE, Wang HY, Blair IA (2009) The post-synaptic density of human postmortem brain tissues: an experimental study paradigm for neuropsychiatric illnesses. PLoS One4: e5251
doi: 10.1371/journal.pone.0005251
98 Harburger DS, Calderwood DA (2009) Integrin signalling at a glance. J Cell Sci122: 159-163
doi: 10.1242/jcs.018093
99 Hashimoto T, Yamada M, Maekawa S, Nakashima T, Miyata S (2008) IgLON cell adhesion molecule Kilon is a crucial modulator for synapse number in hippocampal neurons. Brain Res1224: 1-11
doi: 10.1016/j.brainres.2008.05.069
100 Hashimoto T, Maekawa S, Miyata S (2009) IgLON cell adhesion molecules regulate synaptogenesis in hippocampal neurons. Cell Biochem Funct27: 496-498
doi: 10.1002/cbf.1600
101 Heine M, Thoumine O, Mondin M, Tessier B, Giannone G, Choquet D (2008) Activity-independent and subunit-specific recruitment of functional AMPA receptors at neurexin/neuroligin contacts. Proc Natl Acad Sci USA105: 20947-20952
doi: 10.1073/pnas.0804007106
102 Henderson JT, Georgiou J, Jia Z, Robertson J, Elowe S, Roder JC, Pawson T (2001) The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron32: 1041-1056
doi: 10.1016/S0896-6273(01)00553-0
103 Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM (2003) Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol163: 1313-1326
doi: 10.1083/jcb.200306033
104 Herron LR, Hill M, Davey F, Gunn-Moore FJ (2009) The intracellular interactions of the L1 family of cell adhesion molecules. Biochem J419: 519-531
doi: 10.1042/BJ20082284
105 Himanen JP (2012) Ectodomain structures of Eph receptors. Semin Cell Dev Biol23: 35-42
doi: 10.1016/j.semcdb.2011.10.025
106 Hirano S, Takeichi M (2012) Cadherins in brain morphogenesis and wiring. Physiol Rev92: 597-634
doi: 10.1152/physrev.00014.2011
107 Honda T, Sakisaka T, Yamada T, Kumazawa N, Hoshino T, Kajita M, Kayahara T, Ishizaki H, Tanaka-Okamoto M, Mizoguchi A, Manabe T, Miyoshi J, Takai Y (2006) Involvement of nectins in the formation of puncta adherentia junctions and the mossy fiber trajectory in the mouse hippocampus. Mol Cell Neurosci31: 315-325
doi: 10.1016/j.mcn.2005.10.002
108 Honer WG, Falkai P, Young C, Wang T, Xie J, Bonner J, Hu L, Boulianne GL, Luo Z, Trimble WS (1997) Cingulate cortex synaptic terminal proteins and neural cell adhesion molecule in schizophrenia. Neuroscience78: 99-110
doi: 10.1016/S0306-4522(96)00489-7
109 Horn KE, Xu B, Gobert D, Hamam BN, Thompson KM, Wu CL, Bouchard JF, Uetani N, Racine RJ, Tremblay ML, Ruthazer ES, Chapman CA, Kennedy TE (2012) Receptor protein tyrosine phosphatase sigma regulates synapse structure, function and plasticity. J Neurochem122: 147-161
doi: 10.1111/j.1471-4159.2012.07762.x
110 Hortsch M, Nagaraj K, Godenschwege TA (2009) The interaction between L1-type proteins and ankyrins-a master switch for L1-type CAM function. Cell Mol Biol Lett14: 57-69
doi: 10.2478/s11658-008-0035-4
111 Hoy JL, Constable JR, Vicini S, Fu Z, Washbourne P (2009) SynCAM1 recruits NMDA receptors via protein 4.1B. Mol Cell Neurosci42: 466-483
doi: 10.1016/j.mcn.2009.09.010
112 Hruska M, Dalva MB (2012) Ephrin regulation of synapse formation, function and plasticity. Mol Cell Neurosci50: 35-44
doi: 10.1016/j.mcn.2012.03.004
113 Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell110: 673-687
doi: 10.1016/S0092-8674(02)00971-6
114 Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Südhof TC (1995) Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell81: 435-443
doi: 10.1016/0092-8674(95)90396-8
115 Inoue E, Deguchi-Tawarada M, Togawa A, Matsui C, Arita K, Katahira-Tayama S, Sato T, Yamauchi E, Oda Y, Takai Y (2009) Synaptic activity prompts gamma-secretase-mediated cleavage of EphA4 and dendritic spine formation. J Cell Biol185: 551-564
doi: 10.1083/jcb.200809151
116 Jamain S, Radyushkin K, Hammerschmidt K, Granon S, Boretius S, Varoqueaux F, Ramanantsoa N, Gallego J, Ronnenberg A, Winter D, Frahm J, Fischer J, Bourgeron T, Ehrenreich H, Brose N (2008) Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci USA105: 1710-1715
doi: 10.1073/pnas.0711555105
117 Jedlicka P, Vnencak M, Krueger DD, Jungenitz T, Brose N, Schwarzacher SW (2013) Neuroligin-1 regulates excitatory synaptic transmission, LTP and EPSP-spike coupling in the dentate gyrus in vivo. Brain Struct Funct
doi: 10.1007/s00429-013-0636-1
118 Jensen PH, Soroka V, Thomsen NK, Ralets I, Berezin V, Bock E, Poulsen FM (1999) Structure and interactions of NCAM modules 1 and 2, basic elements in neural cell adhesion. Nat Struct Biol6: 486-493
doi: 10.1038/8292
119 Jüngling K, Eulenburg V, Moore R, Kemler R, Lessmann V, Gottmann K (2006) N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons. J Neurosci26: 6968-6978
doi: 10.1523/JNEUROSCI.1013-06.2006
120 Kayser MS, McClelland AC, Hughes EG, Dalva MB (2006) Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci26: 12152-12164
doi: 10.1523/JNEUROSCI.3072-06.2006
121 Kayser MS, Nolt MJ, Dalva MB (2008) EphB receptors couple dendritic filopodia motility to synapse formation. Neuron59: 56-69
doi: 10.1016/j.neuron.2008.05.007
122 Kim DY, Ingano LA, Kovacs DM (2002) Nectin-1alpha, an immunoglobulin-like receptor involved in the formation of synapses, is a substrate for presenilin/gamma-secretase-like cleavage. J Biol Chem277: 49976-49981
doi: 10.1074/jbc.M210179200
123 Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, Kim K, Kim H, Weinberg RJ, Kim E (2006) NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci9: 1294-1301
doi: 10.1038/nn1763
124 Kim J, Chang A, Dudak A, Federoff HJ, Lim ST (2011) Characterization of nectin processing mediated by presenilin-dependent γ-secretase. J Neurochem119: 945-956
doi: 10.1111/j.1471-4159.2011.07479.x
125 Kirov G, Gumus D, Chen W, Norton N, Georgieva L, Sari M, O’Donovan MC, Erdogan F, Owen MJ, Ropers HH, Ullmann R (2008) Comparative genome hybridization suggests a role for NRXN1 and APBA2 in schizophrenia. Hum Mol Genet17: 458-465
doi: 10.1093/hmg/ddm323
126 Klein R (2009) Bidirectional modulation of synaptic functions by Eph/ ephrin signaling. Nat Neurosci12: 15-20
doi: 10.1038/nn.2231
127 Ko J, Kim S, Chung HS, Kim K, Han K, Kim H, Jun H, Kaang BK, Kim E (2006) SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron50: 233-245
doi: 10.1016/j.neuron.2006.04.005
128 Ko J, Fuccillo MV, Malenka RC, Südhof TC (2009) LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron64: 791-798
doi: 10.1016/j.neuron.2009.12.012
129 Ko J, Soler-Llavina GJ, Fuccillo MV, Malenka RC, Südhof TC (2011) Neuroligins/LRRTMs prevent activity- and Ca2+/calmodulindependent synapse elimination in cultured neurons. J Cell Biol194: 323-334
doi: 10.1083/jcb.201101072
130 Kolkman MJ, Streijger F, Linkels M, Bloemen M, Heeren DJ, Hendriks WJ, Van der Zee CE (2004) Mice lacking leukocyte common antigen-related (LAR) protein tyrosine phosphatase domains demonstrate spatial learning impairment in the two-trial water maze and hyperactivity in multiple behavioural tests. Behav Brain Res154: 171-182
doi: 10.1016/j.bbr.2004.02.006
131 Kolkova K, Novitskaya V, Pedersen N, Berezin V, Bock E (2000) Neural cell adhesion molecule-stimulated neurite outgrowth depends on activation of protein kinase C and the Rasmitogen-activated protein kinase pathway. J Neurosci20: 2238-2246
132 Krushel LA, Sporns O, Cunningham BA, Crossin KL, Edelman GM (1995) Neural cell adhesion molecule (N-CAM) inhibits astrocyte proliferation after injury to different regions of the adult rat brain. Proc Natl Acad Sci USA92: 4323-4327
doi: 10.1073/pnas.92.10.4323
133 Kullander K, Klein R (2002) Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol3: 475-486
doi: 10.1038/nrm856
134 Kwon SK, Woo J, Kim SY, Kim H, Kim E (2010) Trans-synaptic adhesions between netrin-G ligand-3 (NGL-3) and receptor tyrosine phosphatases LAR, protein-tyrosine phosphatase delta (PTPdelta), and PTPsigma via specific domains regulate excitatory synapse formation. J Biol Chem285: 13966-13978
doi: 10.1074/jbc.M109.061127
135 Laumonnier F, Bonnet-Brilhault F, Gomot M, Blanc R, David A, Moizard MP, Raynaud M, Ronce N, Lemonnier E, Calvas P, Laudier B, Chelly J, Fryns JP, Ropers HH, Hamel BC, Andres C, Barthélémy C, Moraine C, Briault S (2004) X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am J Hum Genet74: 552-557
doi: 10.1086/382137
136 Laurén J, Airaksinen MS, Saarma M, Timmusk T (2003) A novel gene family encoding leucine-rich repeat transmembrane proteins differentially expressed in the nervous system. Genomics81: 411-421
doi: 10.1016/S0888-7543(03)00030-2
137 Law JW, Lee AY, Sun M, Nikonenko AG, Chung SK, Dityatev A, Schachner M, Morellini F (2003) Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J Neurosci23: 10419-10432
138 Lee HJ, Song JY, Kim JW, Jin SY, Hong MS, Park JK, Chung JH, Shibata H, Fukumaki Y (2005) Association study of polymorphisms in synaptic vesicle-associated genes, SYN2 and CPLX2, with schizophrenia. Behav Brain Funct1: 15
doi: 10.1186/1744-9081-1-15
139 Levinson JN, Chéry N, Huang K, Wong TP, Gerrow K, Kang R, Prange O, Wang YT, El-Husseini A (2005) Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD- 95 and neurexin-1beta in neuroligin-induced synaptic specificity. J Biol Chem280: 17312-17319
doi: 10.1074/jbc.M413812200
140 Lim ST, Lim KC, Giuliano RE, Federoff HJ (2008) (). Temporal and spatial localization of nectin-1 and l-afadin during synaptogenesis in hippocampal neurons. J Comp Neurol507: 1228-1244
doi: 10.1002/cne.21608
141 Lindner J, Rathjen FG, Schachner M (1983) L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature305: 427-430
doi: 10.1038/305427a0
142 Linhoff MW, Laurén J, Cassidy RM, Dobie FA, Takahashi H, Nygaard HB, Airaksinen MS, Strittmatter SM, Craig AM (2009) An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron61: 734-749
doi: 10.1016/j.neuron.2009.01.017
143 Lisé MF, El-Husseini A (2006) The neuroligin and neurexin families: from structure to function at the synapse. Cell Mol Life Sci63: 1833-1849
doi: 10.1007/s00018-006-6061-3
144 Litterst C, Georgakopoulos A, Shioi J, Ghersi E, Wisniewski T, Wang R, Ludwig A, Robakis NK (2007) Ligand binding and calcium influx induce distinct ectodomain/gamma-secretase-processing pathways of EphB2 receptor. J Biol Chem282: 16155-16163
doi: 10.1074/jbc.M611449200
145 Little EB, Edelman GM, Cunningham BA (1998) Palmitoylation of the cytoplasmic domain of the neural cell adhesion molecule N-CAM serves as an anchor to cellular membranes. Cell Adhes Commun6: 415-430
doi: 10.3109/15419069809109150
146 Lodge AP, Howard MR, McNamee CJ, Moss DJ (2000) Colocalisation, heterophilic interactions and regulated expression of IgLON family proteins in the chick nervous system. Brain Res Mol Brain Res82: 84-94
doi: 10.1016/S0169-328X(00)00184-4
147 Loers G, Schachner M (2007) Recognition molecules and neural repair. J Neurochem101: 865-882
doi: 10.1111/j.1471-4159.2006.04409.x
148 Lyons F, Martin ML, Maguire C, Jackson A, Regan CM, Shelley RK (1988) The expression of an N-CAM serum fragment is positively correlated with severity of negative features in type II schizophrenia. Biol Psychiatry23: 769-775
doi: 10.1016/0006-3223(88)90065-0
149 Maguschak KA, Ressler KJ (2012) The dynamic role of beta-catenin in synaptic plasticity. Neuropharmacology62: 78-88
doi: 10.1016/j.neuropharm.2011.08.032
150 Mah W, Ko J, Nam J, Han K, Chung WS, Kim E (2010) Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation. J Neurosci30: 5559-5568
doi: 10.1523/JNEUROSCI.4839-09.2010
151 Majima T, Ogita H, Yamada T, Amano H, Togashi H, Sakisaka T, Tanaka-Okamoto M, Ishizaki H, Miyoshi J, Takai Y (2009) Involvement of afadin in the formation and remodeling of synapses in the hippocampus. Biochem Biophys Res Commun385: 539-544
doi: 10.1016/j.bbrc.2009.05.097
152 Malhotra JD, Tsiotra P, Karagogeos D, Hortsch M (1998) Cisactivation of L1-mediated ankyrin recruitment by TAG-1 homophilic cell adhesion. J Biol Chem273: 33354-33359
doi: 10.1074/jbc.273.50.33354
153 Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci10: 19-26
doi: 10.1038/nn1827
154 Margolis SS, Salogiannis J, Lipton DM, Mandel-Brehm C, Wills ZP, Mardinly AR, Hu L, Greer PL, Bikoff JB, Ho HY, Soskis MJ, Sahin M, Greenberg ME (2010) EphB-mediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation. Cell143: 442-455
doi: 10.1016/j.cell.2010.09.038
155 Matsui C, Inoue E, Kakita A, Arita K, Deguchi-Tawarada M, Togawa A, Yamada A, Takai Y, Takahashi H (2012) Involvement of the γ- secretase-mediated EphA4 signaling pathway in synaptic pathogenesis of Alzheimer’s disease. Brain Pathol22: 776-787
doi: 10.1111/j.1750-3639.2012.00587.x
156 McGeachie AB, Skrzypiec AE, Cingolani LA, Letellier M, Pawlak R, Goda Y (2012) β3 integrin is dispensable for conditioned fear and hebbian forms of plasticity in the hippocampus. Eur J Neurosci36: 2461-2469
doi: 10.1111/j.1460-9568.2012.08163.x
157 Mendez P, De Roo M, Poglia L, Klauser P, Muller D (2010) N-cadherin mediates plasticity-induced long-term spine stabilization. J Cell Biol189: 589-600
doi: 10.1083/jcb.201003007
158 Mercati O, Danckaert A, André-Leroux G, Bellinzoni M, Gouder L, Watanabe K, Shimoda Y, Grailhe R, De Chaumont F, Bourgeron T, Clo?z-Tayarani I (2013) Contactin 4, -5 and-6 differentially regulate neuritogenesis while they display identical PTPRG binding sites. Biol Open2: 324-334
doi: 10.1242/bio.20133343
159 Missler M, Fernandez-Chacon R, Südhof TC (1998) The making of neurexins. J Neurochem71: 1339-1347
doi: 10.1046/j.1471-4159.1998.71041339.x
160 Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K, Südhof TC (2003) Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature423: 939-948
doi: 10.1038/nature01755
161 Miyata S, Matsumoto N, Taguchi K, Akagi A, Iino T, Funatsu N, Maekawa S (2003) Biochemical and ultrastructural analyses of IgLON cell adhesion molecules, Kilon and OBCAM in the rat brain. Neuroscience117: 645-658
doi: 10.1016/S0306-4522(02)00873-4
162 Mizoguchi A, Nakanishi H, Kimura K, Matsubara K, Ozaki-Kuroda K, Katata T, Honda T, Kiyohara Y, Heo K, Higashi M, Tsutsumi T, Sonoda S, Ide C, Takai Y (2002) Nectin: an adhesion molecule involved in formation of synapses. J Cell Biol156: 555-565
doi: 10.1083/jcb.200103113
163 Moos M, Tacke R, Scherer H, Teplow D, Früh K, Schachner M (1988) Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature334: 701-703
doi: 10.1038/334701a0
164 Morellini F, Lepsveridze E, K?hler B, Dityatev A, Schachner M (2007) Reduced reactivity to novelty, impaired social behavior, and enhanced basal synaptic excitatory activity in perforant path projections to the dentate gyrus in young adult mice deficient in the neural cell adhesion molecule CHL1. Mol Cell Neurosci34: 121-136
doi: 10.1016/j.mcn.2006.10.006
165 Morrow EM, Yoo SY, Flavell SW, Kim TK, Lin Y, Hill RS, Mukaddes NM, Balkhy S, Gascon G, Hashmi A, Al-Saad S, Ware J, Joseph RM, Greenblatt R, Gleason D, Ertelt JA, Apse KA, Bodell A, Partlow JN, Barry B, Yao H, Markianos K, Ferland RJ, Greenberg ME, Walsh CA (2008) Identifying autism loci and genes by tracing recent shared ancestry. Science321: 218-223
doi: 10.1126/science.1157657
166 Mortillo S, Elste A, Ge Y, Patil SB, Hsiao K, Huntley GW, Davis RL, Benson DL (2012) Compensatory redistribution of neuroligins and N-cadherin following deletion of synaptic β 1-integrin. J Comp Neurol520: 2041-2052
doi: 10.1002/cne.23027
167 Mukherjee K, Sharma M, Urlaub H, Bourenkov GP, Jahn R, Südhof TC, Wahl MC (2008) CASK Functions as a Mg2+-independent neurexin kinase. Cell133: 328-339
doi: 10.1016/j.cell.2008.02.036
168 Muller D, Wang C, Skibo G, Toni N, Cremer H, Calaora V, Rougon G, Kiss JZ (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron17: 413-422
doi: 10.1016/S0896-6273(00)80174-9
169 Murai KK, Misner D, Ranscht B (2002) Contactin supports synaptic plasticity associated with hippocampal long-term depression but not potentiation. Curr Biol12: 181-190
doi: 10.1016/S0960-9822(02)00680-2
170 Murai KK, Nguyen LN, Koolpe M, McLennan R, Krull CE, Pasquale EB (2003) Targeting the EphA4 receptor in the nervous system with biologically active peptides. Mol Cell Neurosci24: 1000-1011
doi: 10.1016/j.mcn.2003.08.006
171 Nam CI, Chen L (2005) Post-synaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci USA102: 6137-6142
doi: 10.1073/pnas.0502038102
172 Newschaffer CJ, Croen LA, Daniels J, Giarelli E, Grether JK, Levy SE, Mandell DS, Miller LA, Pinto-Martin J, Reaven J, Reynolds AM, Rice CE, Schendel D, Windham GC (2007) The epidemiology of autism spectrum disorders. Annu Rev Public Health28: 235-258
doi: 10.1146/annurev.publhealth.28.021406.144007
173 Nguyen T, Südhof TC (1997) Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J Biol Chem272: 26032-26039
doi: 10.1074/jbc.272.41.26032
174 Nikonenko AG, Sun M, Lepsveridze E, Apostolova I, Petrova I, Irintchev A, Dityatev A, Schachner M(2006) Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1-deficient mice. Eur J Neurosci23: 1839-1852
doi: 10.1111/j.1460-9568.2006.04710.x
175 Ning L, Tian L, Smirnov S, Vihinen H, Llano O, Vick K, Davis RL, Rivera C, Gahmberg CG (2013) Interactions between ICAM-5 and β1 integrins regulate neuronal synapse formation. J Cell Sci126: 77-89
doi: 10.1242/jcs.106674
176 Nuriya M, Huganir RL (2006) Regulation of AMPA receptor trafficking by N-cadherin. J Neurochem97: 652-661
doi: 10.1111/j.1471-4159.2006.03740.x
177 Okuda T, Yu LM, Cingolani LA, Kemler R, Goda Y (2007) beta-Catenin regulates excitatory post-synaptic strength at hippocampal synapses. Proc Natl Acad Sci USA104: 13479-13484
doi: 10.1073/pnas.0702334104
178 Ongür D, Drevets WC, Price JL (1998) Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci USA95: 13290-13295
doi: 10.1073/pnas.95.22.13290
179 Pagnamenta AT, Khan H, Walker S, Gerrelli D, Wing K, Bonaglia MC, Giorda R, Berney T, Mani E, Molteni M, Pinto D, Le Couteur A, Hallmayer J, Sutcliffe JS, Szatmari P, Paterson AD, Scherer SW, Vieland VJ, Monaco AP (2011) Rare familial 16q21 microdeletions under a linkage peak implicate cadherin 8 (CDH8) in susceptibility to autism and learning disability. J Med Genet48: 48-54
doi: 10.1136/jmg.2010.079426
180 Pedrosa E, Shah A, Tenore C, Capogna M, Villa C, Guo X, Zheng D, Lachman HM (2010) β-catenin promoter ChIP-chip reveals potential schizophrenia and bipolar disorder gene network. J Neurogenet24: 182-193
doi: 10.3109/01677063.2010.495182
181 Peng J, Kim MJ, Cheng D, Duong DM, Gygi SP, Sheng M (2004) Semiquantitative proteomic analysis of rat forebrain post-synaptic density fractions by mass spectrometry. J Biol Chem279: 21003-21011
doi: 10.1074/jbc.M400103200
182 Peng YR, Hou ZH, Yu X (2013) The kinase activity of EphA4 mediates homeostatic scaling-down of synaptic strength via activation of Cdk5. Neuropharmacology65: 232-243
doi: 10.1016/j.neuropharm.2012.10.012
183 Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, Huganir RL (2003) Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron37: 263-274
doi: 10.1016/S0896-6273(02)01168-6
184 Perrin FE, Rathjen FG, Stoeckli ET (2001) Distinct subpopulations of sensory afferents require F11 or axonin-1 for growth to their target layers within the spinal cord of the chick. Neuron30: 707-723
doi: 10.1016/S0896-6273(01)00315-4
185 Pfenninger KH (1971) The cytochemistry of synaptic densities. II. Proteinaceous components and mechanism of synaptic connectivity. J Ultrastruct Res35: 451-475
doi: 10.1016/S0022-5320(71)80005-9
186 Pimenta AF, Reinoso BS, Levitt P (1996) Expression of the mRNAs encoding the limbic system-associated membrane protein (LAMP): II. Fetal rat brain. J Comp Neurol375: 289-302
doi: 10.1002/(SICI)1096-9861(19961111)375:2<289::AID-CNE8>3.0.CO;2-Z
187 Pinkstaff JK, Lynch G, Gall CM (1998) Localization and seizureregulation of integrin beta 1 mRNA in adult rat brain. Brain Res Mol Brain Res55: 265-276
doi: 10.1016/S0169-328X(98)00007-2
188 Plioplys AV, Hemmens SE, Regan CM (1990) Expression of a neural cell adhesion molecule serum fragment is depressed in autism. J Neuropsychiatry Clin Neurosci2: 413-417
189 Polo-Parada L, Bose CM, Landmesser LT (2001) Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions. Neuron32: 815-828
doi: 10.1016/S0896-6273(01)00521-9
190 Polo-Parada L, Plattner F, Bose C, Landmesser LT (2005) NCAM 180 acting via a conserved C-terminal domain and MLCK is essential for effective transmission with repetitive stimulation. Neuron46: 917-931
doi: 10.1016/j.neuron.2005.05.018
191 Poltorak M, Frye MA, Wright R, Hemperly JJ, George MS, Pazzaglia PJ, Jerrels SA, Post RM, Freed WJ (1996) Increased neural cell adhesion molecule in the CSF of patients with mood disorder. J Neurochem66: 1532-1538
doi: 10.1046/j.1471-4159.1996.66041532.x
192 Pozo K, Cingolani LA, Bassani S, Laurent F, Passafaro M, Goda Y (2012) β3 integrin interacts directly with GluA2 AMPA receptor subunit and regulates AMPA receptor expression in hippocampal neurons. Proc Natl Acad Sci USA109: 1323-1328
doi: 10.1073/pnas.1113736109
193 Pulido R, Serra-Pagès C, Tang M, Streuli M (1995) The LAR/PTP delta/PTP sigma subfamily of transmembrane protein-tyrosinephosphatases: multiple human LAR, PTP delta, and PTP sigma isoforms are expressed in a tissue-specific manner and associate with the LAR-interacting protein LIP.1. Proc Natl Acad Sci USA92: 11686-11690
doi: 10.1073/pnas.92.25.11686
194 Puzzo D, Bizzoca A, Privitera L, Furnari D, Giunta S, Girolamo F, Pinto M, Gennarini G, Palmeri A (2013) F3/Contactin promotes hippocampal neurogenesis, synaptic plasticity, and memory in adult mice. Hippocampus23: 1367-1382
doi: 10.1002/hipo.22186
195 Rafuse VF, Polo-Parada L, Landmesser LT (2000) Structural and functional alterations of neuromuscular junctions in NCAMdeficient mice. J Neurosci20: 6529-6539
196 Ramser EM, Wolters G, Dityateva G, Dityatev A, Schachner M, Tilling T (2010) The 14-3-3ζ protein binds to the cell adhesion molecule L1, promotes L1 phosphorylation by CKII and influences L1-dependent neurite outgrowth. PLoS One5: e13462
doi: 10.1371/journal.pone.0013462
197 Reissner C, Runkel F, Missler M (2013) Neurexins. Genome Biol14: 213-227
doi: 10.1186/gb-2013-14-9-213
198 Ren Q, Bennett V (1998) Palmitoylation of neurofascin at a site in the membrane-spanning domain highly conserved among the L1 family of cell adhesion molecules. J Neurochem70: 1839-1849
doi: 10.1046/j.1471-4159.1998.70051839.x
199 Rentzos M, Michalopoulou M, Nikolaou C, Cambouri C, Rombos A, Dimitrakopoulos A, Vassilopoulos D (2005) The role of soluble intercellular adhesion molecules in neurodegenerative disorders. J Neurol Sci228: 129-135
doi: 10.1016/j.jns.2004.11.001
200 Resnick M, Segall A, GR G, Lupowitz Z, Zisapel N (2008) Alternative splicing of neurexins: a role for neuronal polypyrimidine tract binding protein. Neurosci Lett439: 235-240
doi: 10.1016/j.neulet.2008.05.034
201 Reyes AA, Small SJ, Akeson R (1991) At least 27 alternatively spliced forms of the neural cell adhesion molecule mRNA are expressed during rat heart development. Mol Cell Biol11: 1654-1661
202 Richter M, Murai KK, Bourgin C, Pak DT, Pasquale EB (2007) The EphA4 receptor regulates neuronal morphology through SPARmediated inactivation of Rap GTPases. J Neurosci27: 14205-14215
doi: 10.1523/JNEUROSCI.2746-07.2007
203 Rikitake Y, Mandai K, Takai Y (2012) The role of nectins in different types of cell-cell adhesion. J Cell Sci125: 3713-3722
doi: 10.1242/jcs.099572
204 Robbins EM, Krupp AJ, Perez de Arce K, Ghosh AK, Fogel AI, Boucard A, Südhof TC, Stein V, Biederer T (2010) SynCAM 1 adhesion dynamically regulates synapse number and impacts plasticity and learning. Neuron68: 894-906
doi: 10.1016/j.neuron.2010.11.003
205 Rujescu D, Ingason A, Cichon S, Pietil?inen OP, Barnes MR, Toulopoulou T, Picchioni M, Vassos E, Ettinger U, Bramon E, Murray R, Ruggeri M, Tosato S, Bonetto C, Steinberg S, Sigurdsson E, Sigmundsson T, Petursson H, Gylfason A, Olason PI, Hardarsson G, Jonsdottir GA, Gustafsson O, Fossdal R, Giegling I, M?ller HJ, Hartmann AM, Hoffmann P, Crombie C, Fraser G, Walker N, Lonnqvist J, Suvisaari J, Tuulio-Henriksson A, Djurovic S, Melle I, Andreassen OA, Hansen T, Werge T, Kiemeney LA, Franke B, Veltman J, Buizer-Voskamp JE, InvestigatorsGROUP, Sabatti C, Ophoff RA, Rietschel M, N?then MM, Stefansson K, Peltonen L, St Clair D, Stefansson H, Collier DA (2009) Disruption of the neurexin 1 gene is associated with schizophrenia. Hum Mol Genet18: 988-996
206 Saghatelyan AK, Nikonenko AG, Sun M, Rolf B, Putthoff P, Kutsche M, Bartsch U, Dityatev A, Schachner M (2004) Reduced GABAergic transmission and number of hippocampal perisomatic inhibitory synapses in juvenile mice deficient in the neural cell adhesion molecule L1. Mol Cell Neurosci26: 191-203
doi: 10.1016/j.mcn.2004.01.008
207 Saglietti L, Dequidt C, Kamieniarz K, Rousset MC, Valnegri P, Thoumine O, Beretta F, Fagni L, Choquet D, Sala C, Sheng M, Passafaro M (2007) Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron54: 461-477
doi: 10.1016/j.neuron.2007.04.012
208 Sakisaka T, Ikeda W, Ogita H, Fujita N, Takai Y (2007) The roles of nectins in cell adhesions: cooperation with other cell adhesion molecules and growth factor receptors. Curr Opin Cell Biol19: 593-602
doi: 10.1016/j.ceb.2007.09.007
209 Sakurai K, Toyoshima M, Ueda H, Matsubara K, Takeda Y, Karagogeos D, Shimoda Y, Watanabe K (2009) Contribution of the neural cell recognition molecule NB-3 to synapse formation between parallel fibers and Purkinje cells in mouse. Dev Neurobiol69: 811-824
doi: 10.1002/dneu.20742
210 Sakurai K, Toyoshima M, Takeda Y, Shimoda Y, Watanabe K (2010) Synaptic formation in subsets of glutamatergic terminals in the mouse hippocampal formation is affected by a deficiency in the neural cell recognition molecule NB-3. Neurosci Lett473: 102-106
doi: 10.1016/j.neulet.2010.02.027
211 Sanders SJ, Ercan-Sencicek AG, Hus V, Luo R, Murtha MT, Moreno-De-Luca D, Chu SH, Moreau MP, Gupta AR, Thomson SA, Mason CE, Bilguvar K, Celestino-Soper PB, Choi M, Crawford EL, Davis L, Wright NR, Dhodapkar RM, DiCola M, DiLullo NM, Fernandez TV, Fielding-Singh V, Fishman DO, Frahm S, Garagaloyan R, Goh GS, Kammela S, Klei L, Lowe JK, Lund SC, McGrew AD, Meyer KA, Moffat WJ, Murdoch JD, O’Roak BJ, Ober GT, Pottenger RS, Raubeson MJ, Song Y, Wang Q, Yaspan BL, Yu TW, Yurkiewicz IR, Beaudet AL, Cantor RM, Curland M, Grice DE, Günel M, Lifton RP, Mane SM, Martin DM, Shaw CA, Sheldon M, Tischfield JA, Walsh CA, Morrow EM, Ledbetter DH, Fombonne E, Lord C, Martin CL, Brooks AI, Sutcliffe JS, Cook EH Jr, Geschwind D, Roeder K, Devlin B, State MW (2011) Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism. Neuron70: 863-885
doi: 10.1016/j.neuron.2011.05.002
212 Sanes JR, Yamagata M (2009) Many paths to synaptic specificity. Annu Rev Cell Dev Biol25: 161-195
doi: 10.1146/annurev.cellbio.24.110707.175402
213 Sara Y, Biederer T, Atasoy D, Chubykin A, Mozhayeva MG, Südhof TC, Kavalali ET(2005) Selective capabilityofSynCAMand neuroligin for functional synapse assembly. J Neurosci25: 260-270
doi: 10.1523/JNEUROSCI.3165-04.2005
214 Satoh K, Takeuchi M, Oda Y, Deguchi-Tawarada M, Sakamoto Y, Matsubara K, Nagasu T, Takai Y (2002) Identification of activityregulated proteins in the post-synaptic density fraction. Genes Cells7: 187-197
doi: 10.1046/j.1356-9597.2001.00505.x
215 Saura CA, Servián-Morilla E, Scholl FG (2011) Presenilin/γ-secretase regulates neurexin processing at synapses. PLoS One6: e19430
doi: 10.1371/journal.pone.0019430
216 Schaefer AW, Kamiguchi H, Wong EV, Beach CM, Landreth G, Lemmon V (1999) Activation of the MAPK signal cascade by the neural cell adhesion molecule L1 requires L1 internalization. J Biol Chem274: 37965-37973
doi: 10.1074/jbc.274.53.37965
217 Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell101: 657-669
doi: 10.1016/S0092-8674(00)80877-6
218 Seabold GK, Wang PY, Chang K, Wang CY, Wang YX, Petralia RS, Wenthold RJ (2008) The SALM family of adhesion-like molecules forms heteromeric and homomeric complexes. J Biol Chem283: 8395-8405
doi: 10.1074/jbc.M709456200
219 Seabold GK, Wang PY, Petralia RS, Chang K, Zhou A, McDermott MI, Wang YX, Milgram SL, Wenthold RJ (2012) Dileucine and PDZ-binding motifs mediate synaptic adhesion-like molecule 1 (SALM1) trafficking in hippocampal neurons.J Biol Chem287: 4470-4484
doi: 10.1074/jbc.M111.279661
220 Siddiqui TJ, Tari PK, Connor SA, Zhang P, Dobie FA, She K, Kawabe H, Wang YT, Brose N, Craig AM (2013) An LRRTM4-HSPG complex mediates excitatory synapse development on dentate gyrus granule cells. Neuron79: 680-695
doi: 10.1016/j.neuron.2013.06.029
221 Simón AM, de Maturana RL, Ricobaraza A, Escribano L, Schiapparelli L, Cuadrado-Tejedor M, Pérez-Mediavilla A, Avila J, Del Río J, Frechilla D (2009) Early changes in hippocampal Eph receptors precede the onset of memory decline in mouse models of Alzheimer’s disease. J Alzheimers Dis17: 773-786
222 Sindi IA, Tannenberg RK, Dodd PR (2014) A role for the neurexinneuroligin complex in Alzheimer’s disease. Neurobiol Aging35: 746-756
doi: 10.1016/j.neurobiolaging.2013.09.032
223 Sklar P, Smoller JW, Fan J, Ferreira MA, Perlis RH, Chambert K, Nimgaonkar VL, McQueen MB, Faraone SV, Kirby A, de Bakker PI, Ogdie MN, Thase ME, Sachs GS, Todd-Brown K, Gabriel SB, Sougnez C, Gates C, Blumenstiel B, Defelice M, Ardlie KG, Franklin J, Muir WJ, McGhee KA, MacIntyre DJ, McLean A, VanBeck M, McQuillin A, Bass NJ, Robinson M, Lawrence J, Anjorin A, Curtis D, Scolnick EM, Daly MJ, Blackwood DH, Gurling HM, Purcell SM (2008) Whole-genome association study of bipolar disorder. Mol Psychiatry13: 558-569
doi: 10.1038/sj.mp.4002151
224 Soler-Llavina GJ, Fuccillo MV, Ko J, Südhof TC, Malenka RC (2011) The neurexin ligands, neuroligins and leucine-rich repeat transmembrane proteins, perform convergent and divergent synaptic functions in vivo. Proc Natl Acad Sci USA108: 16502-16509
doi: 10.1073/pnas.1114028108
225 Soler-Llavina GJ, Arstikaitis P, Morishita W, Ahmad M, Südhof TC, Malenka RC (2013) Leucine-rich repeat transmembrane proteins are essential for maintenance of long-term potentiation. Neuron79: 439-446
doi: 10.1016/j.neuron.2013.06.007
226 Soronen P, Ollila HM, Antila M, Silander K, Palo OM, Kiesepp? T, L?nnqvist J, Peltonen L, Tuulio-Henriksson A, Partonen T, Paunio T (2010) Replication of GWAS of bipolar disorder: association of SNPs near CDH7 with bipolar disorder and visual processing. Mol Psychiatry15: 4-6
doi: 10.1038/mp.2009.86
227 Soto F, Watkins KL, Johnson RE, Schottler F, Kerschensteiner D (2013) NGL-2 regulates pathway-specific neurite growth and lamination, synapse formation, and signal transmission in the retina. J Neurosci33: 11949-11959
doi: 10.1523/JNEUROSCI.1521-13.2013
228 Stan A, Pielarski KN, Brigadski T, Wittenmayer N, Fedorchenko O, Gohla A, Lessmann V, Dresbach T, Gottmann K (2010) Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation. Proc Natl Acad Sci USA107: 11116-11121
doi: 10.1073/pnas.0914233107
229 Südhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature455: 903-911
doi: 10.1038/nature07456
230 Sytnyk V, Leshchyns’ka I, Nikonenko AG, Schachner M (2006) NCAM promotes assembly and activity-dependent remodeling of the post-synaptic signaling complex. J Cell Biol174: 1071-1085
doi: 10.1083/jcb.200604145
231 Tabuchi K, Südhof TC (2002) Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics79: 849-859
doi: 10.1006/geno.2002.6780
232 Tabuchi K, Blundell J, Etherton MR, Hammer RE, Liu X, Powell CM, Südhof TC (2007) A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science318: 71-76
doi: 10.1126/science.1146221
233 Takahashi H, Arstikaitis P, Prasad T, Bartlett TE, Wang YT, Murphy TH, Craig AM (2011) Post-synaptic TrkC and presynaptic PTPσ function as a bidirectional excitatory synaptic organizing complex. Neuron69: 287-303
doi: 10.1016/j.neuron.2010.12.024
234 Takahashi H, Katayama K, Sohya K, Miyamoto H, Prasad T, Matsumoto Y, Ota M, Yasuda H, Tsumoto T, Aruga J, Craig AM (2012) Selective control of inhibitory synapse development by Slitrk3-PTPδ trans-synaptic interaction. Nat Neurosci15: 389-398
doi: 10.1038/nn.3040
235 Takai Y, Irie K, Shimizu K, Sakisaka T, Ikeda W (2003) Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization. Cancer Sci94: 655-667
doi: 10.1111/j.1349-7006.2003.tb01499.x
236 Takeichi M (1988) The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development102: 639-655
237 Takeichi M (2007) The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci8: 11-20
doi: 10.1038/nrn2043
238 Tallafuss A, Constable JR, Washbourne P (2010) Organization ofcentral synapses by adhesion molecules. Eur J Neurosci32: 198-206
doi: 10.1111/j.1460-9568.2010.07340.x
239 Taylor AM, Wu J, Tai HC, Schuman EM (2013) Axonal translation of β-catenin regulates synaptic vesicle dynamics. J Neurosci33: 5584-5589
doi: 10.1523/JNEUROSCI.2944-12.2013
240 Thomas LA, Akins MR, Biederer T (2008) Expression and adhesion profiles of SynCAM molecules indicate distinct neuronal functions. J Comp Neurol510 : 47-67
doi: 10.1002/cne.21773
241 Tolias KF, Bikoff JB, Kane CG, Tolias CS, Hu L, Greenberg ME (2007) The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proc Natl Acad Sci USA104: 7265-7270
doi: 10.1073/pnas.0702044104
242 Tomasoni R, Repetto D, Morini R, Elia C, Gardoni F, Di Luca M, Turco E, Defilippi P, Matteoli M (2013) SNAP-25 regulates spine formation through post-synaptic binding to p140Cap. Nat Commun4: 2136
doi: 10.1038/ncomms3136
243 Trinidad JC, Thalhammer A, Specht CG, Lynn AJ, Baker PR, Schoepfer R, Burlingame AL (2008) Quantitative analysis of synaptic phosphorylation and protein expression. Mol Cell Proteomics7: 684-696
doi: 10.1074/mcp.M700170-MCP200
244 Tuvia S, Garver TD, Bennett V (1997) The phosphorylation state of the FIGQY tyrosine of neurofascin determines ankyrin-binding activity and patterns of cell segregation. Proc Natl Acad Sci USA94: 12957-12962
doi: 10.1073/pnas.94.24.12957
245 Uchida N, Honjo Y, Johnson KR, Wheelock MJ, Takeichi M (1996) The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J Cell Biol135: 767-779
doi: 10.1083/jcb.135.3.767
246 Uemura M, Nakao S, Suzuki ST, Takeichi M, Hirano S (2007) OLProtocadherin is essential for growth of striatal axons and thalamocortical projections. Nat Neurosci10: 1151-1159
doi: 10.1038/nn1960
247 Uetani N, Kato K, Ogura H, Mizuno K, Kawano K, Mikoshiba K, Yakura H, Asano M, Iwakura Y (2000) Impaired learning with enhanced hippocampal long-term potentiation in PTPdelta-deficient mice. EMBO J19: 2775-2785
doi: 10.1093/emboj/19.12.2775
248 Ullrich B, Ushkaryov YA, Südhof TC (1995) Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron14: 497-507
doi: 10.1016/0896-6273(95)90306-2
249 van Daalen E, Kemner C, Verbeek NE, van der Zwaag B, Dijkhuizen T, Rump P, Houben R, van’t Slot R, de Jonge MV, Staal WG, Beemer FA, Vorstman JA, Burbach JP, van Amstel HK, Hochstenbach R, Brilstra EH, Poot M (2011) Social Responsiveness Scale-aided analysis of the clinical impact of copy number variations in autism : 315-323
doi: 10.1007/s10048-011-0297-2
250 Varoqueaux F, Jamain S, Brose N (2004) Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol83: 449-456
doi: 10.1078/0171-9335-00410
251 Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K, Zhang W, Südhof TC, Brose N (2006) Neuroligins determine synapse maturation and function. Neuron51: 741-754
doi: 10.1016/j.neuron.2006.09.003
252 Vawter MP (2000) Dysregulation of the neural cell adhesion molecule and neuropsychiatric disorders. Eur J Pharmacol405: 385-395
doi: 10.1016/S0014-2999(00)00568-9
253 Vawter MP, Cannon-Spoor HE, Hemperly JJ, Hyde TM, VanderPutten DM, Kleinman JE, Freed WJ (1998a) Abnormal expression of cell recognition molecules in schizophrenia. Exp Neurol149: 424-432
doi: 10.1006/exnr.1997.6721
254 Vawter MP, Hemperly JJ, Hyde TM, Bachus SE, VanderPutten DM, Howard AL, Cannon-Spoor HE, McCoy MT, Webster MJ, Kleinman JE, Freed WJ (1998b) VASE-containing N-CAM isoforms are increased in the hippocampus in bipolar disorder but not schizophrenia. Exp Neurol154: 1-11
doi: 10.1006/exnr.1998.6889
255 Vawter MP, Howard AL, Hyde TM, Kleinman JE, Freed WJ (1999) Alterations of hippocampal secreted N-CAM in bipolar disorder and synaptophysin in schizophrenia. Mol Psychiatry4: 467-475
doi: 10.1038/sj.mp.4000547
256 Voikar V, Kulesskaya N, Laakso T, Lauren J, Strittmatter SM, Airaksinen MS (2013) LRRTM1-deficient mice show a rare phenotype of avoiding small enclosures-a tentative mouse model for claustrophobia-like behaviour. Behav Brain Res238: 69-78
doi: 10.1016/j.bbr.2012.10.013
257 Vrijenhoek T, Buizer-Voskamp JE, van der Stelt I, Strengman E, Genetic Risk and Outcome in Psychosis (GROUP) Consortium, Sabatti C, Geurts van Kessel A, Brunner HG, Ophoff RA, Veltman JA (2008) Recurrent CNVs disrupt three candidate genes in schizophrenia patients. Am J Hum Genet83: 504-510
doi: 10.1016/j.ajhg.2008.09.011
258 Wang J, Luo ZG (2008) The role of Wnt/beta-catenin signaling in post-synaptic differentiation. Commun Integr Biol1: 158-160
doi: 10.4161/cib.1.2.7099
259 Wang CY, Chang K, Petralia RS, Wang YX, Seabold GK, Wenthold RJ (2006) A novel family of adhesion-like molecules that interacts with the NMDA receptor. J Neurosci26: 2174-2183
doi: 10.1523/JNEUROSCI.3799-05.2006
260 Wang PY, Seabold GK, Wenthold RJ (2008) Synaptic adhesion-like molecules (SALMs) promote neurite outgrowth. Mol Cell Neurosci39: 83-94
doi: 10.1016/j.mcn.2008.05.019
261 Wang K, Zhang H, Ma D, Bucan M, Glessner JT, Abrahams BS, Salyakina D, Imielinski M, Bradfield JP, Sleiman PM, Kim CE, Hou C, Frackelton E, Chiavacci R, Takahashi N, Sakurai T, Rappaport E, Lajonchere CM, Munson J, Estes A, Korvatska O, Piven J, Sonnenblick LI, Alvarez Retuerto AI, Herman EI, Dong H, Hutman T, Sigman M, Ozonoff S, Klin A, Owley T, Sweeney JA, Brune CW, Cantor RM, Bernier R, Gilbert JR, Cuccaro ML, McMahon WM, Miller J, State MW, Wassink TH, Coon H, Levy SE, Schultz RT, Nurnberger JI, Haines JL, Sutcliffe JS, Cook EH, Minshew NJ, Buxbaum JD, Dawson G, Grant SF, Geschwind DH, Pericak-Vance MA, Schellenberg GD, Hakonarson H (2009) Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature459: 528-533
doi: 10.1038/nature07999
262 Willemsen MH, Fernandez BA, Bacino CA, Gerkes E, de Brouwer AP, Pfundt R, Sikkema-Raddatz B, Scherer SW, Marshall CR, Potocki L, van Bokhoven H, Kleefstra T (2010) Identification of ANKRD11 and ZNF778 as candidate genes for autism and variable cognitive impairment in the novel 16q24.3 microdeletion syndrome. Eur J Hum Genet18: 429-435
doi: 10.1038/ejhg.2009.192
263 Williams ME, de Wit J, Ghosh A (2010) Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron68: 9-18
doi: 10.1016/j.neuron.2010.09.007
264 Woo J, Kwon SK, Choi S, Kim S, Lee JR, Dunah AW, Sheng M, Kim E (2009) Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat Neurosci12: 428-437
doi: 10.1038/nn.2279
265 Wyszynski M, Kim E, Dunah AW, Passafaro M, Valtschanoff JG, Serra-Pagès C, Streuli M, Weinberg RJ, Sheng M (2002) Interaction between GRIP and Liprin-α/SYD2 Is Required for AMPA Receptor Targeting. Neuron34: 39-52
doi: 10.1016/S0896-6273(02)00640-2
266 Xu NJ, Henkemeyer M (2012) Ephrin reverse signaling in axon guidance and synaptogenesis. Semin Cell Dev Biol23: 58-64
doi: 10.1016/j.semcdb.2011.10.024
267 Xu J, Litterst C, Georgakopoulos A, Zaganas I, Robakis NK (2009) Peptide EphB2/CTF2 generated by the gamma-secretase processing of EphB2 receptor promotes tyrosine phosphorylation and cell surface localization of N-methyl-D-aspartate receptors. J Biol Chem284: 27220-27228
doi: 10.1074/jbc.M109.048728
268 Yamada A, Irie K, Deguchi-Tawarada M, Ohtsuka T, Takai Y (2003) Nectin-dependent localization of synaptic scaffolding molecule (S-SCAM) at the puncta adherentia junctions formed between the mossy fiber terminals and the dendrites of pyramidal cells in the CA3 area of the mouse hippocampus. Genes Cells8: 985-994
doi: 10.1046/j.1356-9597.2003.00690.x
269 Yamada M, Hashimoto T, Hayashi N, Higuchi M, Murakami A, Nakashima T, Maekawa S, Miyata S (2007) Synaptic adhesion molecule OBCAM., synaptogenesis and dynamic internalization. Brain Res1165: 5-14
doi: 10.1016/j.brainres.2007.04.062
270 Yan J, Noltner K, Feng J, Li W, Schroer R, Skinner C, Zeng W, Schwartz CE, Sommer SS (2008) Neurexin 1alpha structural variants associated with autism. Neurosci Lett438: 368-370
doi: 10.1016/j.neulet.2008.04.074
271 Yim YS, Kwon Y, Nam J, Yoon HI, Lee K, Kim DG, Kim E, Kim CH, Ko J (2013) Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases. Proc Natl Acad Sci USA110: 4057-4062
doi: 10.1073/pnas.1209881110
272 Zhang C, Milunsky JM, Newton S, Ko J, Zhao G, Maher TA, Tager-Flusberg H, Bolliger MF, Carter AS, Boucard AA, Powell CM, Südhof TC (2009) A neuroligin-4 missense mutation associated with autism impairs neuroligin-4 folding and endoplasmic reticulum export. J Neurosci29: 10843-10854
doi: 10.1523/JNEUROSCI.1248-09.2009
273 Zhao L, Ma QL, Calon F, Harris-White ME, Yang F, Lim GP, Morihara T, Ubeda OJ, Ambegaokar S, Hansen JE, Weisbart RH, Teter B, Frautschy SA, Cole GM (2006) Role of p21-activated kinase pathway defects in the cognitive deficits of Alzheimer disease. Nat Neurosci9: 234-242
doi: 10.1038/nn1630
274 Zhou L, Jones EV, Murai KK (2012) EphA signaling promotes actinbased dendritic spine remodeling through slingshot phosphatase. J Biol Chem287: 9346-9359
doi: 10.1074/jbc.M111.302802
[1] Vsevolod V. Gurevich, Eugenia V. Gurevich, Vladimir N. Uversky. Arrestins: structural disorder creates rich functionality[J]. Protein Cell, 2018, 9(12): 986-1003.
[2] Zhi-Ping Liu, Luonan Chen. Proteome-wide prediction of protein-protein interactions from high-throughput data[J]. Prot Cell, 2012, 3(7): 508-520.
[3] Nuoyan zheng, Xiahe Huang, Bojiao Yin, Dan Wang, Qi Xie. An effective system for detecting protein-protein interaction based on in vivo cleavage by PPV NIa protease[J]. Prot Cell, 2012, 3(12): 921-928.
[4] Jing Pu, Cheol Woong Ha, Shuyan Zhang, Jong Pil Jung, Won-Ki Huh, Pingsheng Liu. Interactomic study on interaction between lipid droplets and mitochondria[J]. Prot Cell, 2011, 2(6): 487-496.
[5] Chao Xu, Jinrong Min. Structure and function of WD40 domain proteins[J]. Prot Cell, 2011, 2(3): 202-214.
[6] Sunil K. Verma, Trivadi S. Ganesan, Uday Kishore, Peter J. Parker. The tumor suppressor RASSF1A is a novel effector of small G protein Rap1A[J]. Prot Cell, 2011, 2(3): 237-249.
[7] Zheng Zhou, Jun-Ming Liao, Peng Zhang, Jun-Bao Fan, Jie Chen, Yi Liang. Parkinson disease drug screening based on the interaction between D2 dopamine receptor and beta-arrestin 2 detected by capillary zone electrophoresis[J]. Prot Cell, 2011, 2(11): 899-905.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed