Cell adhesion and synaptogenesis

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Author:
CHEN Gong(Department of Biology,The Huck Institutes of Life Sciences,The Pennsylvania State University,University Park,PA 16802,USA)
WU Xia(Department of Biology,The Huck Institutes of Life Sciences,The Pennsylvania State University,University Park,PA 16802,USA)
Sebnem Tuncdemir(Department of Biology,The Huck Institutes of Life Sciences,The Pennsylvania State University,University Park,PA 16802,USA)
Journal Title:
ACTA PHYSIOLOGICA SINICA
Issue:
Volume 59, Issue 06, 2007
DOI:
Key Word:
synaptogenesis;cell adhesion;synapse assembly

Abstract´╝Ü Synapses are inter-neuronal connections that are fundamental working units in neural networks.How synapses are molecularly constructed is a fascinating question,which attracted scientists'attention for many decades.Neuromuscular junction,a field pioneered by Te-Pei FENG and many others,has been an excellent model for studying synaptogenesis and paved the way for our understanding of the synapse formation in the central nervous system.Recent studies shed new light on the molecular mechanisms of central synapse formation by discovering a group of cell adhesion molecules exerting potent synaptogenic effects.This review will focus on those cell adhesion molecules which can induce central synapse formation when expressed in non-neuronal cells.

  • [1]Hall ZW.Sanes JR.Synaptic structure and development:the neuromuscular junction Cell 1993;72(Suppl):99-121.
  • [2]Dan Y.Lo Y.Poo MM.Plasticity of developing neuromuscular synapses.Prog Brain Res 1995;105:211-215.
  • [3]Sanes JR,Lichtman JW.Development of the vertebrate neuromuscular junction.Annu Rev Neurosci 1999;22:389-442.
  • [4]GarnerCC.2haiRG,GundelfingerED,Ziv NE.Molecular mechanisms of CNS synaptogenesis.Trends Neurosci 2002;25(5):243-251.
  • [5]Waites CL,Craig AM,Garner CC.Mechanisms of vertebrate synaptogenesis.Annu Rev Neurosci 2005;28:251-274.
  • [6]Sheng M.Molecular organization of the postsynaptic specialization.Proc Natl Acad Sci USA 2001;98(13):7058-7061.
  • [7]Cline HT.Dendritic arbor development and synaptogenesis.Curr Opin Neurobiol 2001;11(1):118-126.
  • [8]Scannevin RH,Huganir RL.Postsynaptic organization and regulation of excitatory synapses.Nat Rev Neurosci 2000;1(2):133-141
  • [9]Friedman HV,Bresler T,Garner CC,Ziv NE.Assembly of new individual excitatory synapses:time course and temporal order of synaptic molecule recruitment.Neuron 2000:27(1):57-69.
  • [10]Zhai RG.Vardinon-Friedman H,Cases-Langhoff C,Becker B,Gundeifinger ED,Ziv NE,Garner CC.Assembling the presynaptic active zone:a characterization of an active one precursor vesicle.Neuron 2001:29(1):131-143.
  • [11]Ahmari SE,Buchanan J,Smith SJ.Assembly of presynaptic active zones from cytoplasmic transport packets.Nat Neurosci 2000;3(5):445-451.
  • [12]Krueger SR,Kolar A,Fitzsimonds RM.The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons.Neuron 2003;40(5):945-957.
  • [13]Washbourne P.Bennett JE,McAllister AK.Rapid recruitment of NMDA receptor transport packets to nascent synapses.Nat Neurosci 2002;5(8):751-759.
  • [14]ziv NE.Garner CC.Cellular and molecular mechanisms of presynaptic assembly.Nat Rev Neurosci 2004;5(5):385-399.
  • [15]Deng L,Yao J,Fang C,Dong N,Luscher B,Chen G.Sequential postsynaptic maturation governs the temporal order of GABAergic and glutamatergic synaptogenesis in rat embryonic cultures.J Neurosci 2007;27:10860-10869.
  • [16]Ben-Ari Y,Khalilov I,Represa A.Gozlan H.Interneurons set the tune of developing networks.Trends Neurosci 2004;27(7):422-427.
  • [17]Dong N,Qi J,Chen G.Molecular reconstitution of functional GABAergic synapses with expression of neuroligin-2 and GABAAreceptors.Mol Cell Neurosci 2007;35(1):14-23.
  • [18]Chen G,Trombley PQ,van den Pol AN.Excitatory actions of GABA in developing rat hypothalamic neurones.J Physiol 1996;494:451-464.
  • [19]Ben-Ari Y.Excitatory actions of GABA during development:the nature of the nurture.Nat Rev Neurosci 2002;3(9):728-739.
  • [20]Owens DF.Kriegstein AR.Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 2002;3(9):715-727.
  • [21]Shapiro L,Love J,Colman DR.Adhesion molecules in the nervous system:structural insights into function and diversity.Annu Rev Neurosci 2007;30:451-474.
  • [22]Tabuchi K,Sudhof TC.Structure and evolution of neurexin genes:insight into the mechanism of alternative splicing.Genomics 2002;79(6):849-859.
  • [23]Rudenko G,Nguyen T,Chelliah Y,Sudhof TC,Deisenhofer J.The structure of the ligand-binding domain of neurexin Ibeta:regulation of LNS domain function by alternative splicing.Cell 1999;99(1):93-101.
  • [24]Ichtchenko K,Hata Y,Nguyen T,Ullrich B,Missler M,Moomaw C.Sudhof TC.Neuroligin 1:a splice site-specific ligand for betaneurexins.Cell 1995;81(3):435-443.
  • [25]Ichtchenko K,Nguyen T,Sudhof TC.Structures,alternative splicing,and neurexin binding of multiple neuroligins.J Biol Chem 1996;271(5):2676-2682.
  • [26]Bolliger MF,Frei K,Winterhalter KH,Gloor SM.Identification of a novel neuroligin in humans which binds to PSD-95 and has a widespread expression.Biochem J 2001;356(Pt 2):581-588.
  • [27]Scholl FG,Scheiffele P.Making connections:cholinesterasedomain proteins in the CNS.Trends Neurosci 2003;26(11):618-624.
  • [28]Ullrich B,Ushkaryov YA,Sudhof TC.Cartography of neurexins:more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons.Neuron 1995;14(3):497-507.
  • [29]Graf ER,Zhang X,Jin SX,Linhoff MW,Craig AM.Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins.Cell 2004;119(7):1013-1026.
  • [30]Dean C,Scholl FG,Choih J,DeMaria S,Berger J,Isacoff E,Scheiffele P.Neurexin mediates the assembly of presynaptic terminals.Nat Neurosci 2003;6(7):708-716.
  • [31]Taniguchi H,Gollan L,Scholl FG,Mahadomrongkul V,Dobler E,Limthong N,Peck M,Aoki C,Scheiffele P.Silencing of neuroligin function by postsynaptic neurexins.J Neurosci 2007;27(11):2815-2824.
  • [32]Song JY.Ichtchenko K,Sudhof TC,Brose N.Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses.Proc Natl Acad Sci USA 1999;96(3):1100-1105.
  • [33]Varoqueaux F,Jamain S,Brose N.Neuroligin 2 is exclusively localized to inhibitory synapses.Eur J Cell Biol 2004;83(9):449-456.
  • [34]Gilbert M,Smith J,Roskams AJ,Auld VJ.Neuroligin 3 is a vertebrate gliotactin expressed in the olfactory ensheathing glia,a growth-promoting class of macroglia.Glia 2001;34(3):151-164
  • [35]Hata Y,Davletov B,Petrenko AG,Jahn R,Sudhof TC.Interaction of synaptotagmin with the cytoplasmic domains of neurexins.Neuron 1993;10(2):307-315.
  • [36]Hata Y,Butz S,Sudhof TC.CASK:a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins.J Neurosci 1996;16(8):2488-2494.
  • [37]Biederer T,Sudhof TC.Mints as adaptors.Direct binding to neurexins and recruitment of munc18.J Biol Chem 2000;275(51):39803-39806.
  • [38]Grootjans JJ,Reekmans G,Ceulemans H,David G.Synteninsyndecan binding requires syndecan-synteny and the co-operation of both PDZ domains of syntenin.J Biol Chem 2000:275(26):19933-19941.
  • [39]Irie M,Hata Y,Takeuchi M,Ichtchenko K,Toyoda A,Hirao K,Takai Y.Rosahl TW.Sudhof TC.Binding of neuroligins to PSD95.Science 1997:277(5331):1511-1515.
  • [40]Futai K,Kim MJ,Hashikawa T,Scheiffele P,Sheng M,Hayashi Y.Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin.Nat Neurosci 2007:10(2):186-195.
  • [41]Sumita K,Sato Y,Iida J,Kawata A.,Hamano M,Hirabayashi S,Ohno K,Peles E,Hata Y.Synaptic scaffolding molecule(SSCAM)membrane-associated guanylate kinase with inverted organization(MAGI)-2 is associated with cell adhesion molecules at inhibitory synapses in rat hippocampal neurons.J Neurochem 2007;100(1):154-166.
  • [42]Scheiffele P,Fan J,Choih J,Fetter R,Serafini T.Neuroligin expressed in nonneuronal ceils triggers presynaptic development in contacting axons.Cell 2000;101(6):657-669.
  • [43]Fu Z,Washbourne P,Ortinski P.Vicini S.Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors.J Neurophysiol 2003;90(6):3950-3957.
  • [44]Sara Y,Biederer T,Atasoy D,Chubykin A,Mozhayeva MG,Sudhof TC,Kayalali ET.Selective capability of SynCAM and neuroligin for functional synapse assembly.J Neurosci 2005;25(1):260-270.
  • [45]Levinson JN,Chery N,Huang K,Wong TP,Gerrow K,Kang R,Prange O.Wang YT,El-Husseini A.Neuroligins mediate excitatory and inhibitory synapse formation:involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity.J Biol Chem 2005;280(17):17312-17319.
  • [46]Chih B,Engelman H,Scheiffele P.Control of excitatory and inhibitory synapse formation by neuroligins.Science 2005;307(5713):1324-1328.
  • [47]Gerrow K,Romorini S,Nabi SM,Colicos MA,Sala C,ElHusseini A.A preformed complex of postsynaptic proteins is involved in excitatory synapse development Neuron 2006;49(4):547-562.
  • [48]Prange O,Wong TP,Gerrow K,Wang YT,El-Husseini A.A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin.Proc Natl Acad Sci USA 2004;101(38):13915-13920.
  • [49]Chih B,Gollan L,Scheiffele P.Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex.Neuron 2006;51(2):171-178.
  • [50]Boucard AA,Chubykin AA,Comoletti D,Taylor P,Sudhof TC.A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha-and beta-neurexins.Neuron 2005;48(2):229-236.
  • [51]Nam CI.Chen L.Postsynaptic assembly induced by neurexinneuroligin interaction and neurotransmitter.Proc Natl Acad Sci USA 2005:102(17):6137-6142.
  • [52]Varoqueaux F,Aramuni G,Rawson RL,Mohrmann R,Missler M,Gottmann K Zhang W,Sudhof TC,Brose N.Neuroligins determine synapse maturation and function Neuron 2006:51(6):741-754.
  • [53]Chubykin AA,Atasoy D,Etherton MR,Brose N,Kavalali ET,Gibson JR,Sudhof TC.Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin2.Neuron 2007:54(6):919-931.
  • [54]Biederer T.Bioinformatic characterization of the SynCAM family of immunoglobulin-like domain-containing adhesion molecules.Genomics 2006;87(1):139-150.
  • [55]Biederer T,Sara Y,Mozhayeva M,Atasoy D,Liu X,Kavalali ET,Sudhof TC.SynCAM,a synaptic adhesion molecule that drives synapse assembly.Science 2002:297(5586):1525-1531.
  • [56]Kuramochi M,Fukuhara H,Nobukuni T,Kanbe T,Maruyama T,Ghosh HP.Pletcher M,Isomura M.Onizuka M,Kitamura T,Sekiya T,Reeves RH.Murakami Y.TSLCl is a tumor-suppressor gene in human non-small-cell lung cancer.Nat Genet 2001;27(4):427-430.
  • [57]Fujita E,Kouroku Y,Ozeki S,Tanabe Y,Toyama Y,Maekawa M,Kojima N,Senoo H,Toshimori K,Momoi T.Oligo-asthenoteratozoospermia in mice lacking RA175/TSLC1/SynCAM/IGSF4A,a cell adhesion molecule in the immunoglobulin superfamily.Mol Cell Biol 2006:26(2):718-726.
  • [58]Shingai T,Ikeda W,Kakunaga S,Morimoto K,Takekuni K,Itoh S,Satoh K,Takeuchi M,Imai T,Monden M,Takai Y.Implications of nectin-like molecule-2/IGSF4/RA175/SgIGSF/TSLC1/SynCAMl in cell-cell adhesion and transmembrane protein localization in epithelial cells.J Biol Chem 2003;278(37):35421-35427.
  • [59]Fukami T,Satoh H.Williams YN,Masuda M,Fukuhara H,Maruyama T,Yageta M,Kuramochi M,Takamoto S,Murakami Y.Isolation of the mouse Tsll1 and Tsll2 genes,orthologues of the human TSLCI-like genes 1and2(TSLL1 and TSLL2).Gene 2003:323:11-18.
  • [60]Kakunaga S,Ikeda W,Itoh S,Deguchi-Tawarada M,Ohtsuka T,Mizoguchi A.Takai Y.Nectin-like molecule-1/TSLL1/SynCAM3:a neural tissue-specific immunoglobulin-like cellcell adhesion molecule localizing at non-junctional contact sites of presynaptic nerve terminals,axons and gila cell processes.J Cell Sci 2005:118(Pt 6):1267-1277.
  • [61]Spiegel I,Adamsky K,Eshed Y,Milo R,Sabanay H,Sarig-Nadir O.Horresh I,Scherer SS,Rasband MN,Peles E.A central role for Nec14(SynCAM4) in Schwann cell-axon interaction and myelination.Nat Neurosci 2007:10(7):861-869.
  • [62]Flanagan JG,Vanderhaeghen P.The ephrins and Eph receptors in neural development.Anuu Rev Neurosci 1998:21:309-345.
  • [63]Kullander K,Klein R.Mechanisms and functions of Eph and ephrin signalling.Nat Rev Mol Cell Biol 2002;3(7):475-486.
  • [64]Himanen JP,Chumley MJ,Lackmann M,Li C,Barton WA,Jeffrey PD,Vearing C,Geleick D,Feldheim DA,Boyd AW,Henkemeyer M.Nikolov DB.Repelling class discrimination:ephrin-A5 binds to and activates EphB2 receptor signaling.Nat Neurosci 2004:7(5):501-509.
  • [65]Calo L,Cinque C,Patane M,Schillaci D,Battaglia G,Melchiorri D,Nicoletti F,Bruno V.Interaction between ephrins/Eph receptors and excitatory amino acid receptors:possible relevance in the regulation of synaptic plasticity and in the pathophysiology of neuronal degeneration.J Neurochem 2006;98(1):1-10.
  • [66]Sahin M,Greer PL,Lin MZ,Poucher H,Eberhart J,Schmidt S,Wright TM,Shamah SM,O'Connell S,Cowan CW,Hu L,Goldberg JL,Debant A,Corfas G,Krull CE,Greenberg ME.Eph-dependent tyrosine phosphorylation of ephexinl modulates growth cone collapse.Neuron 2005;46(2):191-204.
  • [67]Holland SJ,Peles E,Pawson T,Schlessinger J.Cell-contactdependent signalling in axon growth and guidance:Eph receptor tyrosine kinases and receptor protein tyrosine phosphatase beta.Curt Opin Neurobiol 1998;8(1):117-127.
  • [68]Miao H,Strebhardt K,Pasquale EB,Shen TL,Guan JL,Wang B.Inhibition of integrin-mediated cell adhesion but not directional cell migration requires catalytic activity of EphB3 receptor tyrosine kinase.Role of Rho family small GTPases.J Biol Chem 2005:280(2):923-932.
  • [69]Contractor A,Rogers C,Maron C,Henkemeyer M,Swanson GT,Heinemann SF.Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP.Science 2002;296(5574):1864-1869.
  • [70]Torres R,Firestein BL,Dong H,Staudinger J,Olson EN,Huganir RL,Bredt DS,Gale NW,Yancopoulos GD.PDZ proteins bind,cluster,and synaptically colocalize with Eph receptors and their ephrin ligands.Neuron 1998;21(6):1453-1463.
  • [71]Liebl DJ.Morris CJ.Henkemeyer M,Parada LF.mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system.J Neurosci Res 2003:71(1):7-22.
  • [72]Dalva MB,Takasu MA,Ljn MZ,Shamah SM,Hu L,Gale NW,Greenberg ME.EphB receptors interact with NMDA receptors and regulate excitatory synapse formation.Cell 2000;103(6):945-956
  • [73]Takasu MA,Dalva MB,Zigmond RE,Greenberg ME.Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors.Science 2002;295(5554):491-495.
  • [74]Kayser MS,McClelland AC,Hughes EG,Dalva MB.Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors.J Neurosci 2006;26(47):12152-12164.
  • [75]Henkemeyer M,Itkis OS,Ngo M,Hickmott PW,Ethell IM.Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus.J Cell Biol 2003:163(6):1313-1326.
  • [76]Nakashiba T.Ikeda T,Nishimura S,Tashiro K,Honjo T,Culotti JG,Itohara S.Netrin-G1:a novel glycosyl phosphatidylinositollinked mammalian netrin that is functionally divergent from classical netrins.J Neurosci 2000:20(17):6540-6550.
  • [77]Nakashiba T,Nishimura S,Ikeda T,Itohara S.Complementary expression and neurite outgrowth activity of netrin-G subfamily members.Mech Dev 2002:111(1-2):47-60.
  • [78]Lin JC,Ho WH,Gurney A,Rosenthal A.The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons.Nat Neurosci 2003;6(12):1270-1276.
  • [79]Kim S,Burette A,Chung HS,Kwon SK,Woo J,Lee HW,Kim K,Kim H,Weinberg RJ,Kim E.NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formafion.Nat Neurosci 2006:9(10):1294-1301.
  • [80]Nishimura-Akiyoshi S,Niimi K,Nakashiba T,Itohara S.Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments.Proc Natl Acad Sci USA 2007;104(37):14801-14806.
  • [81]Brummendorf T,Kenwrick S,Rathjen FG.Neural cell recognition molecule L1:from cell biology to human hereditary brain malformations.Curr Opin Neurobiol 1998;8(1):87-97.
  • [82]Davis JQ,Bennett V.Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules.J Biol Chem 1994;269(44):27163-27166.
  • [83]Cheng L,Itoh K,Lemmon V.L1-mediated branching is regulated by two ezrin-radixin-moesin(ERM)-binding sites,the RSLE region and a novel juxtamembrane ERM-binding region J Neurosci 2005;25(2):395-403.
  • [84]Wood PM.Schachner M,Bunge RP.Inhibition of Schwann cell myelination in vitro by antibody to the L1 adhesion molecule.J Neurosci 1990:10(11):3635-3645.
  • [85]Nishimura K,Yoshihara F,Tojima T,Ooashi N,Yoon W,Mikoshiba K.Bennett V,Kamiguchi H.L1-dependent neuritogenesis involves ankyrinB that mediates L1-CAM coupling with retrograde actin flow.J Cell Biol 2003;163(5):1077-1088.
  • [86]Cohen NR,Taylor JS,Scott LB,Guillery RW,Soriano P,Furley AJ.Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1.Curr Biol 1998;8(1):26-33.
  • [87]Kamiguchi H,Lemmon V.Recycling of the cell adhesion mole-cule L1 in axonal growth cones.J Neurosci 2000;20(10):3676-3686.
  • [88]Burden-Gulley SM,Payne HR,Lemmon V.Growth cones are actively influenced by substrate-bound adhesion molecules.J Neurosci 1995;15(6):4370-4381.
  • [89]Rose SP.Cell-adhesion molecules,glucocolticoids and long-termmemory formation.Trends Neurosci 1995;18(11):502-506.
  • [90]Matsumoto-Miyai K,Ninomiya A,Yamasaki H,Tamura H,Nakamura Y.Shiosaka S.NMDA-dependent proteolysis of presynaptic adhesion molecule L1 in the hippocampus by neuropsin.J Neurosci 2003:23(21):7727-7736.
  • [91]Panayi M.Gokhale D,Mansour S.Elles R.Prenatal diagnosis in a family with X-linked hydrocephalus.Prenat Diagn 2005;25(10):930-933.
  • [92]Fransen E.Van Camp G,Vits L.Willems PJ.L1-associated diseases:clinical geneticists divide,molecular geneticists unite.Hum Mol Genet 1997;6(10):1625-1632.
  • [93]Ango F,di Cristo G,Higashiyama H,Bennett V,Wu P,Huang ZJ.Ankyrin-based subcellular gradient of neurofascin,an immunoglobulin family protein,directs GABAergic innervation at purkinje axon initial segment.Cell 2004;119(2):257-272.
  • [94]Triana-Baltzer GB,Liu Z,Berg DK.Pre-and postsynaptic actions of L1-CAM in nicotinic pathways.Mol Cell Neurosci 2006;33(2):214-226.
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