Synaptic cell adhesion

Cold Spring Harbor Perspectives in Biology

Volumn 4, Issue 4, 2012, Pages

  Missler, Markus ^a   Südhof, Thomas C ^b   Biederer, Thomas ^c  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; LIGAND;

ARTICLE; CELL ADHESION; HUMAN; PHYSIOLOGY; SIGNAL TRANSDUCTION; SYNAPSE;

CADHERINS; CELL ADHESION; HUMANS; LIGANDS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84863915107     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a005694     Document Type: Article

References (146)

1. Akins MR, Biederer T. 2006. Cell-cell interactions in synaptogenesis. Curr Opin Neurobiol 16: 83-89.
2. 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. Cell 119: 257-272.
3. Ango F, Wu C, Van derWant 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 Biol 6: e103.
4. Aoto J, Ting P, Maghsoodi B, Xu N, Henkemeyer M, Chen L. 2007. Postsynaptic EphrinB3 promotes shaft glutamatergic synapse formation. J Neurosci 27: 7508-7519.
5. Araç D, Boucard AA, Özkan E, Strop P, Newell E, Südhof TC, Brunger AT. 2007. Structures of Neuroligin-1 and the Neuroligin-1/Neurexin-1b complex reveal specific protein- protein and protein-Ca2+ interactions. Neuron 56: 992-1003.
6. Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B, Reichardt LF. 2003. Role of b-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40: 719-731.
7. Banovic D, Khorramshahi O, Owald D, Wichmann C, Riedt T, Fouquet W, Tian R, Sigrist SJ, Aberle H. 2010. Drosophila neuroligin 1 promotes growth and postsynaptic differentiation at glutamatergic neuromuscular junctions. Neuron 66: 724-738.
8. Benson DL, Tanaka H. 1998. N-Cadherin redistribution during synaptogenesis in hippocampal neurons. J Neurosci 18: 6892-6904.
9. Biederer T. 2006. Bioinformatic characterization of the SynCAM family of immunoglobulin-like domain-containing adhesion molecules. Genomics 87: 139-150.
10. Biederer T, Südhof TC. 2001. CASK and protein 4. 1 support F-actin nucleation on neurexins. J Biol Chem 276: 47869-47876.
11. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Südhof TC. 2002. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297: 1525-1531.
12. 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 α and b-neurexins. Neuron 48: 229-236.
13. Bourgeron T. 2009. A synaptic trek to autism. Curr Opin Neurobiol 19: 231-234.
14. Bourgin C, Murai KK, Richter M, Pasquale EB. 2007. The EphA4 receptor regulates dendritic spine remodeling by affecting b1-integrin signaling pathways. J Cell Biol 178: 1295-1307.
15. 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 Neurosci 30: 9984-9989.
16. Budreck EC, Scheiffele P. 2007. Neuroligin-3 is a neuronal adhesion protein at GABAergic and glutamatergic synapses. Eur J Neurosci 26: 1738-1748.
17. Chagnon MJ, Uetani N, Tremblay ML. 2004. Functional significance of the LAR receptor protein tyrosine phosphatase family in development and diseases. Biochem Cell Biol 82: 664-675.
18. Chan CS, Weeber EJ, Zong L, Fuchs E, Sweatt JD, Davis RL. 2006. β1-integrins are required for hippocampal AMPA receptor-dependent synaptic transmission, synaptic plasticity, and working memory. J Neurosci 26: 223-232.
19. Chavis P, Westbrook G. 2001. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411: 317-321.
20. Chen F, Venugopal V, Murray B, Rudenko G. 2011. The structure of neurexin 1a reveals features promoting a role as synaptic organizer. Structure 19: 779-789.
21. Cheng SB, Amici SA, Ren XQ, McKay SB, Treuil MW, Lindstrom JM, Rao J, Anand R. 2009. Presynaptic targeting of a4b2 nicotinic acetylcholine receptors is regulated by neurexin-1b. J Biol Chem 284: 23251-23259.
22. Chih B, Engelman H, Scheiffele P. 2005. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307: 1324-1328.
23. Chih B, Gollan L, Scheiffele P. 2006. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51: 171-178.
24. Chiu SL, Chen CM, Cline HT. 2008. Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 58: 708-719.
25. Choi YB, Li HL, Kassabov SR, Jin I, Puthanveettil SV, Karl KA, Lu Y, Kim JH, Bailey CH, Kandel ER. 2011. Neurexinneuroligin transsynaptic interaction mediates learningrelated synaptic remodeling and long-term facilitation in aplysia. Neuron 70: 468-481.
26. 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. Neuron 54: 919-931.
27. Cooper MW, Smith SJ. 1992. A real-time analysis of growth cone-target cell interactions during the formation of stable contacts between hippocampal neurons in culture. J Neurobiol 23: 814-828.
28. Dahlhaus R, Hines RM, Eadie BD, Kannangara TS, Hines DJ, Brown CE, Christie BR, El-Husseini A. 2010. Overexpression of the cell adhesion protein neuroligin-1 induces learning deficits and impairs synaptic plasticity by altering the ratio of excitation to inhibition in the hippocampus. Hippocampus 20: 305-322.
29. Dalva MB, Takasu MA, Lin MZ, Shamah SM, Hu L, Gale NW, Greenberg ME. 2000. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103: 945-956.
30. deWit J, Sylwestrak E, O'Sullivan ML, Otto S, Tiglio K, Savas JN, Yates JR III, Comoletti D, Taylor P, Ghosh A. 2009. LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 64: 799-806.
31. Dityatev A, Bukalo O, Schachner M. 2008. Modulation of synaptic transmission and plasticity by cell adhesion and repulsion molecules. Neuron Glia Biol 4: 197-209.
32. 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 Neurosci 8: 458-467.
33. Elia LP, Yamamoto M, Zang K, Reichardt LF. 2006. p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51: 43-56.
34. Etherton MR, Blaiss CA, Powell CM, Südhof TC. 2009. Mouse neurexin-1a deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc Natl Acad Sci 42: 7998-8003.
35. Fogel AI, Akins MR, Krupp AJ, Stagi M, Stein V, Biederer T. 2007. SynCAMs organize synapses through heterophilic adhesion. J Neurosci 27: 12516-12530.
36. Fogel AI, Li Y, Giza J, Wang Q, Lam TT, Modis Y, Biederer T. 2010. N-glycosylation at the SynCAM immunoglobulin interface modulates synaptic adhesion. J Biol Chem 285: 34864-34874.
37. Formstone CJ. 2010. 7TM-Cadherins: Developmental roles and future challenges. Adv Exp Med Biol 706: 14-36.
38. Gibson JR, Huber KM, Südhof TC. 2009. Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking, but not from somatostatin- positive interneurons. J Neurosci 29: 13883-13897.
39. Graf ER, Zhang X, Jin S-X, Linhoff MW, Craig AM. 2004. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119: 1013-1026.
40. Gray EG. 1959. Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study. J Anat 93: 420-433.
41. Gray EG, Whittaker VP. 1962. The isolation of nerve endings from brain: An electron-microscopic study of cell fragments derived by homogenization and centrifugation. J Anat 96: 79-88.
42. Haklai-Topper L, Soutschek J, Sabanay H, Scheel J, Hobert O, Peles E. 2011. The neurexin superfamily of Caenorhabditis elegans. Gene Expr Patterns 11: 144-150.
43. Hata Y, Butz S, Südhof TC. 1996. CASK: A novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neuro sci 16: 2488-2494.
44. Hata K, Polo-Parada L, Landmesser LT. 2007. Selective targeting of different neural cell adhesion molecule isoforms during motoneuron myotube synapse formation in culture and the switch from an immature tomature form of synaptic vesicle cycling. J Neurosci 27: 14481-14493.
45. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM. 2003. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163: 1313-1326.
46. Hines RM, Wu L, Hines DJ, Steenland H, Mansour S, Dahlhaus R, Singaraja RR, Cao X, Sammler E, Hormuzdi SG, et al. 2008. Synaptic imbalance, stereotypies, and impaired social interactions in mice with altered neuroligin 2 expression. J Neurosci 28: 6055-6067.
47. Hintsch G, Zurlinden A, Meskenaite V, Steuble M, Fink-Widmer K, Kinter J, Sonderegger P. 2002. The calsyntenins- a family of postsynaptic membrane proteins with distinct neuronal expression patterns. Mol Cell Neurosci 21: 393-409.
48. Hoon M, Soykan T, Falkenburger B, Hammer M, Patrizi A, Schmidt KF, Sassoe-Pognetto M, Löwel S, Moser T, Taschenberger H, et al. 2011. Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina. Proc Natl Acad Sci 108: 3053-3058.
49. Huang Z, Shimazu K, Woo NH, Zang K, Muller U, Lu B, Reichardt LF. 2006. Distinct roles of the b1-class integrins at the developing and the mature hippocampal excitatory synapse. J Neurosci 26: 11208-11219.
50. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Südhof TC. 1995. Neuroligin 1: A splice site-specific ligand for b-neurexins. Cell 81: 435-443.
51. Ichtchenko K, Nguyen T, Südhof TC. 1996. Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 271: 2676-2682.
52. Irie M, Hata Y, Takeuchi M, Ichtchenko K, Toyoda A, Hirao K, Takai Y, Rosahl TW, Südhof TC. 1997. Binding of neuroligins to PSD-95. Science 277: 1511-1515.
53. Jamain S, Radyushkin K, Hammerschmidt K, Granon S, Boretius S, Varoqueaux F, Ramanantsoa N, Gallego J, Ronnenberg A, Winter D, et al. 2008. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci 105: 1710-1715.
54. 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 Neurosci 26: 6968-6978.
55. Kakunaga S, Ikeda W, Itoh S, Deguchi-Tawarada M, Ohtsuka T, Mizoguchi A, Takai Y. 2005. Nectin-like molecule- 1/TSLL1/SynCAM3: A neural tissue-specific immunoglobulin- like cell-cell adhesion molecule localizing at non-junctional contact sites of presynaptic nerve terminals, axons and glia cell processes. J Cell Sci 118: 1267-1277.
56. Kattenstroth G, Tantalaki E, Südhof TC, Gottmann K, Missler M. 2004. Postsynaptic N-methyl-D-aspartate receptor function requires αneurexins. Proc Natl Acad Sci 101: 2607-2612.
57. Kaufmann N, DeProto J, Ranjan R, Wan H, Van Vactor D. 2002. Drosophila liprin-a and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34: 27-38.
58. Kayser MS, McClelland AC, Hughes EG, Dalva MB. 2006. Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci 26: 12152-12164.
59. 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 Neurosci 9: 1294-1301.
60. Knott GW, Quairiaux C, Genoud C, Welker E. 2002. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34: 265-273.
61. 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. Neuron 50: 233-245.
62. Ko J, Zhang C, Araç D, Boucard AA, Brunger AT, Südhof TC. 2009a. Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J 28: 3244-3255.
63. Ko J, Fuccillo MV, Malenka RC, Südhof TC. 2009b. LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 64: 791-798.
64. 2+/calmodulin-dependent synapse elimination in cultured neurons. J Cell Biol 194: 323-334.
65. Koch SM, Ullian EM. 2010. Neuronal pentraxins mediate silent synapse conversion in the developing visual system. J Neurosci 30: 5404-5414.
66. Lai KO, Ip NY. 2009. Synapse development and plasticity: Roles of ephrin/Eph receptor signaling. Curr Opin Neurobiol 19: 275-283.
67. 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. Genomics 81: 411-421.
68. Li J, Ashley J, Budnik V, Bhat MA. 2007. Crucial role of Drosophila neurexin in proper active zone apposition to postsynaptic densities, synaptic growth, and synaptic transmission. Neuron 55: 741-755.
69. Lim BK, Matsuda N, Poo MM. 2008. Ephrin-B reverse signaling promotes structural and functional synaptic maturation in vivo. Nat Neurosci 11: 160-169.
70. Lin JC, Ho WH, Gurney A, Rosenthal A. 2003. The netrin- G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons. Nat Neurosci 6: 1270-1276.
71. Linhoff MW, Lauren 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. Neuron 61: 734-749.
72. Lucic V, Yang T, Schweikert G, Forster F, Baumeister W. 2005. Morphological characterization of molecular complexes present in the synaptic cleft. Structure 13: 423-434.
73. Luikart BW, Nef S, Virmani T, Lush ME, Liu Y, Kavalali ET, Parada LF. 2005. TrkB has a cell-autonomous role in the establishment of hippocampal Schaffer collateral synapses. J Neurosci 25: 3774-3786.
74. Lyckman AW, Horng S, Leamey CA, Tropea D, Watakabe A, VanWart A, McCurry C, Yamamori T, Sur M. 2008. Gene expression patterns in visual cortex during the critical period: Synaptic stabilization and reversal by visual deprivation. Proc Natl Acad Sci 105: 9409-9414.
75. Matsuda K, Yuzaki M. 2011. Cbln family proteins promote synapse formation by regulating distinct neurexin signaling pathways in various brain regions. Eur J Neurosci 33: 1447-1461.
76. Mendez P, De Roo M, Poglia L, Klauser P, Muller D. 2010. N-cadherin mediates plasticity-induced long-term spine stabilization. J Cell Biol 189: 589-600.
77. Miller MT, Mileni M, Comoletti D, Stevens RC, Harel M, Taylor P. 2011. The crystal structure of the αneurexin-1 extracellular region reveals a hinge point for mediating synaptic adhesion and function. Structure 19: 767-778.
78. Missler M, Südhof TC. 1998. Neurexophilins form a conserved family of neuropeptide-like glycoproteins. J Neurosci 18: 3630-3638.
79. 2+ channels to synaptic vesicle exocytosis. Nature 423: 939-948.
80. Mizoguchi A, Nakanishi H, Kimura K, Matsubara K, Ozaki-Kuroda K, Katata T, Honda T, Kiyohara Y, Heo K, Higashi M, et al. 2002. Nectin: An adhesion molecule involved in formation of synapses. J Cell Biol 156: 555-565.
81. Muller D, Wang C, Skibo G, Toni N, Cremer H, Calaora V, Rougon G, Kiss JZ. 1996. PSαNCAM is required for activity-induced synaptic plasticity. Neuron 17: 413-422.
82. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 6: 153-160.
83. Nakashiba T, Nishimura S, Ikeda T, Itohara S. 2002. Complementary expression and neurite outgrowth activity of netrin-G subfamily members. Mech Dev 111: 47-60.
84. Nam CI, Chen L. 2005. Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci 102: 6137-6142.
85. Nam J, Mah W, Kim E. 2011. The SALM/Lrfn family of leucine-rich repeat-containing cell adhesion molecules. Semin Cell Dev Biol 22: 492-498.
86. Nozumi M, Togano T, Takahashi-Niki K, Lu J, Honda A, Taoka M, Shinkawa T, Koga H, Takeuchi K, Isobe T, Igarashi M. 2009. Identification of functional marker proteins in the mammalian growth cone. Proc Natl Acad Sci 106: 17211-17216.
87. O'Brien R, Xu D, Mi R, Tang X, Hopf C, Worley P. 2002. Synaptically targeted narp plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons. J Neurosci 22: 4487-4498.
88. Palade GE, Palay SL. 1954. Electron microscope observations of interneuronal and neuromuscular synapses. Anat Record 118: 335-336.
89. Phillips GR, Tanaka H, Frank M, Elste A, Fidler L, Benson DL, Colman DR. 2003. Aγ-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons. J Neurosci 23: 5096-5104.
90. Piechotta K, Dudanova I, Missler M. 2006. The resilient synapse: Insights from genetic interference of synaptic cell adhesion molecules. Cell Tissue Res 326: 617-642.
91. Pokutta S, Weis WI. 2007. Structure and mechanism of cadherins and catenins in cell-cell contacts. Annu Rev Cell Dev Biol 23: 237-261.
92. Polo-Parada L, Bose CM, Plattner F, Landmesser LT. 2004. Distinct roles of different neural cell adhesion molecule (NCAM) isoforms in synaptic maturation revealed by analysis of NCAM 180 kDa isoform-deficient mice. J Neurosci 24: 1852-1864.
93. Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Zhang M, Paarmann I, Fuchs C, Harvey K, et al. 2009. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63: 628-642.
94. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM. 2002. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109: 205-216.
95. Rees RP, Bunge MB, Bunge RP. 1976. Morphological changes in the neuritic growth cone and target neuron during synaptic junction development in culture. J Cell Biol 68: 240-263.
96. Reichardt LF. 2006. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361: 1545-1564.
97. Reissner C, Klose M, Fairless R, Missler M. 2008. Mutational analysis of the neurexin/neuroligin complex reveals essential and regulatory components. Proc Natl Acad Sci 105: 15124-15129.
98. Rex CS, Lin CY, Kramar EA, Chen LY, Gall CM, Lynch G. 2007. Brain-derived neurotrophic factor promotes longterm potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 27: 3017-3029.
99. Rico B, Xu BJ, Reichardt LF. 2002. TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat Neurosci 5: 225-233.
100. 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. Neuron 68: 894-906.
101. Rudenko G, Hohenester E, Muller YA. 2001. LG/LNS domains: Multiple functions-one business end? Trends Biochem Sci 26: 363-368.
102. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T. 2000. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101: 657-669.
103. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17: 5858-5867.
104. Seabold GK, Wang PY, Chang K, Wang CY, Wang YX, Petralia RS, Wenthold RJ. 2008. The SALM family of adhesionlike molecules forms heteromeric and homomeric complexes. J Biol Chem 283: 8395-8405.
105. Segura I, Essmann CL, Weinges S, Acker-Palmer A. 2007. Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat Neurosci 10: 301-310.
106. Shen K, Fetter RD, Bargmann CI. 2004. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 116: 869-881.
107. Shipman SL, Schnell E, Hirai T, Chen BS, Roche KW, Nicoll RA. 2011. Functional dependence of neuroligin on a new non-PDZ intracellular domain. Nat Neurosci 14: 718-726.
108. Siddiqui TJ, Pancaroglu R, Kang Y, Rooyakkers A, Craig AM. 2010. LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development. J Neurosci 30: 7495-7506.
109. Soler-Llavina GJ, Fuccillo MV, Ko J, Südhof TC, Malenka RC. 2011. The neurexin ligands, neuroligins and LRRTMs, perform convergent and divergent synaptic functions in vivo. Proc Natl Acad Sci 108: 16502-16509.
110. Song JY, Ichtchenko K, Südhof TC, Brose N. 1999. Neuroligin 1 is a postsynaptic cell adhesion molecule of excitatory synapses. Proc Natl Acad Sci 96: 1100-1105.
111. Stagi M, Fogel AI, Biederer T. 2010. SynCAM 1 participates in axo-dendritic contact assembly and shapes neuronal growth cones. Proc Natl Acad Sci 107: 7568-7573.
112. Südhof TC. 2008. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455: 903-911.
113. Sugita S, Saito F, Tang J, Satz J, Campbell K, Südhof TC. 2001. A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154: 435-445.
114. Sun M, Xing G, Yuan L, Gan G, Knight D, With SI, He C, Han J, Zeng X, Fang M, et al. 2011. Neuroligin 2 is required for synapse development and function at the Drosophila neuromuscular junction. J Neurosci 31: 687-699.
115. Sytnyk V, Leshchyns'ka I, Nikonenko AG, Schachner M. 2006. NCAMpromotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. J Cell Biol 174: 1071-1085.
116. Tabuchi K, Südhof TC. 2002. Structure and evolution of neurexin genes: Insight into the mechanism of alternative splicing. Genomics 79: 849-859.
117. 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. Science 318: 71-76.
118. Takahashi H, Arstikaitis P, Prasad T, Bartlett TE, Wang YT, Murphy TH, Craig AM. 2011. Postsynaptic TrkC and presynaptic PTPs function as a bidirectional excitatory synaptic organizing complex. Neuron 69: 287-303.
119. Thomas LA, Akins MR, Biederer T. 2008. Expression and adhesion profiles of SynCAMmolecules indicate distinct neuronal functions. J Comp Neurol 510: 47-67.
120. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M. 2002. Cadherin regulates dendritic spine morphogenesis. Neuron 35: 77-89.
121. Togashi H, Miyoshi J, Honda T, Sakisaka T, Takai Y, Takeichi M. 2006. Interneurite affinity is regulated by heterophilic nectin interactions in concert with the cadherin machinery. J Cell Biol 174: 141-151.
122. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D. 1999. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402: 421-425.
123. 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 Biol 135: 767-779.
124. Uemura T, Lee SJ, Yasumura M, Takeuchi T, Yoshida T, Ra M, Taguchi R, Sakimura K Mishina M. 2010. Trans-synaptic interaction of GluRD2 and neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141: 1068-1079.
125. 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. Neuron 14: 497-507.
126. Ushkaryov YA, Südhof TC. 1993. Neurexin IIIa: Extensive alternative splicing generates membrane-bound and soluble forms. Proc Natl Acad Sci 90: 6410-6414.
127. Ushkaryov YA, Petrenko AG, Geppert M, Südhof TC. 1992. Neurexins: Synaptic cell surface proteins related to the α latrotoxin receptor and laminin. Science 257: 50-56.
128. Ushkaryov YA, Hata Y, Ichtchenko K, Moomaw C, Afendis S, Slaughter CA, Südhof TC. 1994. Conserved domainstructure of b-neurexins. Unusual cleaved signal sequences in receptor-like neuronal cell-surface proteins. J Biol Chem 269: 11987-11992.
129. Varoqueaux F, Jamain S, Brose N. 2004. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 83: 449-456.
130. 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. Neuron 51: 741-754.
131. Wang XZ, Weiner JA, Levi S, Craig AM, Bradley A, Sanes JR. 2002. γ-protocadherins are required for survival of spinal interneurons. Neuron 36: 843-854.
132. 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 Neurosci 26: 2174-2183.
133. Weiner JA, Wang X, Tapia JC, Sanes JR. 2005. γ-protocadherins are required for synaptic development in the spinal cord. Proc Natl Acad Sci 102: 8-14.
134. Woo RS, Li XM, Tao Y, Carpenter-Hyland E, Huang YZ, Weber J, Neiswender H, Dong XP, Wu J, Gassmann M, et al. 2007. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54: 599-610.
135. Woo J, Kwon SK, Kim E. 2009. The NGL family of leucinerich repeat-containing synaptic adhesion molecules. Mol Cell Neurosci 42: 1-10.
136. Yamagata M, Sanes JR. 2008. Dscam and Sidekick proteins direct laminαspecific synaptic connections in vertebrate retina. Nature 451: 465-469.
137. Yamagata M, Weiner JA, Sanes JR. 2002. Sidekicks: Synaptic adhesion molecules that promote laminαspecific connectivity in the retina. Cell 110: 649-660.
138. Zelano J, Berg A, Thams S, Hailer NP, Cullheim S. 2009. Syn- CAM 1 expression correlates with restoration of central synapses on spinal motoneurons after two different models of peripheral nerve injury. J Comp Neurol 517: 670-682.
139. Zhang W, Rohlmann A, Sargsyan V, Aramuni G, Hammer RE, Südhof TC, Missler M. 2005a. Extracellular domains of αneurexins participate in regulating synaptic transmission by selectively affecting N- and P/Q-type Ca2+ channels. J Neurosci 25: 4330-4342.
140. Zhang Q, Wang J, Fan S, Wang L, Cao L, Tang K, Peng C, Li Z, Li W, Gan K, et al. 2005b. Expression and functional characterization of LRRC4, a novel brain-specific member of the LRR superfamily. FEBS Lett 579: 3674-3682.
141. Zhang Q, Rajan I, Savelieva KV, Wang CY, Vogel P, Kelly M, Xu N, Hasson B, Jarman W, Lanthorn TH. 2008. Netrin-G2 and netrin-G2 ligand are both required for normal auditory responsiveness. Genes Brain Behav 7: 385-392.
142. Zhang C, Atasoy D, Araç D, Yang X, Fucillo MV, Robison AJ, Ko J, Brunger AT, Südhof TC. 2010. Neurexins physically and functionally interact with GABA(A) receptors. Neuron 66: 403-416.
143. Zhen M, Jin Y. 1999. The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401: 371-375.
144. Zoghbi HY. 2003. Postnatal neurodevelopmental disorders: Meeting at the synapse? Science 302: 826-830.
145. Zuber B, Nikonenko I, Klauser P, Muller D, Dubochet J. 2005. The mammalian central nervous synaptic cleft contains a high density of periodically organized complexes. Proc Natl Acad Sci 102: 19192-19197.
146. Zuko A, Bouyain S, van der Zwaag B, Burbach JP. 2011. Contactins: Structural aspects in relation to developmental functions in brain disease. Adv Protein Chem Struct Biol 84: 143-180.