Membrane-tethered monomeric neurexin LNS-domain triggers synapse formation

Journal of Neuroscience

Volumn 33, Issue 36, 2013, Pages 14617-14628

  Gokce, Ozgun ^a   Südhof, Thomas C ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; HYBRID PROTEIN; LENTIVIRUS VECTOR; MESSENGER RNA; NEUREXIN; NEUROLIGIN 1; NEURON SPECIFIC NUCLEAR PROTEIN; PDZ PROTEIN; PROTEIN SERINE THREONINE KINASE; SYNAPSIN; SYNAPTOBREVIN 2; SYNAPTOTAGMIN I;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE EXPRESSION PROFILING; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MOUSE; MUTAGENESIS; NEWBORN; NONHUMAN; PDZ DOMAIN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC INHIBITION;

AMINO ACID SEQUENCE; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL MEMBRANE; CELLS, CULTURED; GUANYLATE KINASE; HIPPOCAMPUS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULES; NEURONS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SYNAPSES;

EID: 84883387704     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1232-13.2013     Document Type: Article

References (41)

1. 2+ interactions. Neuron 56:992-1003. CrossRef Medline
2. Biederer T, Südhof TC (2001) CASK and protein 4.1 support F-actin nucleation on neurexins. J Biol Chem 276:47869-47876. Medline
3. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Südhof TC (2002) SynCAM, a synaptic cell adhesion molecule that drives synapse assembly. Science 297:1525-1531. CrossRef Medline
4. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232. CrossRef Medline
5. Chen F, Venugopal V, Murray B, Rudenko G (2011) The structure of neurexin 1α reveals features promoting a role as synaptic organizer. Structure 19:779-789. CrossRef Medline
6. Chubykin AA, Liu X, Comoletti D, Tsigelny I, Taylor P, Südhof TC (2005) Dissection of synapse induction by neuroligins: effect of a neuroligin mutation associated with autism. J Biol Chem 280:22365-22374. CrossRef Medline
7. Cohen AR, Woods DF, Marfatia SM, Walther Z, Chishti AH, Anderson JM, Wood DF (1998) Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J Cell Biol 142:129-138. CrossRef Medline
8. de Wit J, Sylwestrak E, O'Sullivan ML, Otto S, Tiglio K, Savas JN, Yates JR 3rd, Comoletti D, Taylor P, Ghosh A (2009) LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 64:799-806. CrossRef Medline
9. Fabrichny IP, Leone P, Sulzenbacher G, Comoletti D, Miller MT, Taylor P, Bourne Y, Marchot P (2007) Structural analysis of the synaptic protein neuroligin and its beta-neurexin complex: determinants for folding and cell adhesion. Neuron 56:979-991. CrossRef Medline
10. Fairless R, Masius H, Rohlmann A, Heupel K, AhmadM, Reissner C, Dresbach T, Missler M (2008) Polarized targeting of neurexins to synapses is regulated by their C-terminal sequences. J Neurosci 28:12969-12981. CrossRef Medline
11. Fernández-Busnadiego R, Zuber B, Maurer UE, Cyrklaff M, Baumeister W, Lucic V (2010) Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J Cell Biol 188:145-156. CrossRef Medline
12. 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 J 30:4728-4738. CrossRef Medline
13. Hata Y, Butz S, Südhof TC (1996) CASK: A novel dlg/PSD95 homologue with an n-terminal CaM kinase domain identified by interaction with neurexins. J Neurosci 16:2488-2494. Medline
14. Hsueh YP, Yang FC, Kharazia V, Naisbitt S, Cohen AR, Weinberg RJ, Sheng M (1998) Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol 142:139-151. CrossRef Medline
15. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Südhof TC (1995) Neuroligin 1: a splice site-specific ligand for β-neurexins. Cell 81:435-443. CrossRef Medline
16. Ichtchenko K, Nguyen T, Südhof TC (1996) Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 271:2676-2682. CrossRef Medline
17. 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. CrossRef Medline
18. Ko J, Fuccillo MV, Malenka RC, Südhof TC (2009a) LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 64: 791-798. CrossRef Medline
19. Ko J, Zhang C, Arac D, Boucard AA, Brunger AT, Südhof TC (2009b) Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J 28:3244-3255. CrossRef Medline
20. 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. Neuron 61:734-749. CrossRef Medline
21. Manders EMM, Verbeek FJ, Alen JA (1993) Measurement of co-localization of objects in dual-color confocal images. J Microsc 169:375-382. CrossRef
22. Miller MT, Mileni M, Comoletti D, Stevens RC, Harel M, Taylor P (2011) The crystal structure of the α-neurexin-1 extracellular region reveals a hinge point for mediating synaptic adhesion and function. Structure 8:767-778. Medline
23. 2+ channels to synaptic vesicle exocytosis. Nature 423:939-948. CrossRef Medline
24. 2+-independent neurexin kinase. Cell 133:328-339. CrossRef Medline
25. Owald D, Khorramshahi O, Gupta VK, Banovic D, Depner H, Fouquet W, Wichmann C, Mertel S, Eimer S, Reynolds E, Holt M, Aberle H, Sigrist SJ (2012) Cooperation of Syd-1 with Neurexin synchronizes pre-with postsynaptic assembly. Nature Neuroscience 15:1219-1226. CrossRef Medline
26. Pang ZP, Cao P, Xu W, Südhof TC (2010a) Calmodulin controls synaptic strength via presynaptic activation of calmodulin kinase II. J Neurosci 30:4132-4142. CrossRef Medline
27. Pang ZP, XuW, CaoP, Südhof TC (2010b) Calmodulin suppresses synaptotagmin-2 transcription in cortical neurons. J Biol Chem 285:33930-33939. CrossRef Medline
28. Pang ZP, Yang N, Vierbuchen T, Ostermeier A, Fuentes DR, Yang TQ, Citri A, Sebastiano V, Marro S, Südhof TC, Wernig M (2011) Induction of human neuronal cells by defined transcription factors. Nature 476:220-223. Medline
29. Rowen L, Young J, Birditt B, Kaur A, Madan A, Philipps DL, Qin S, Minx P, Wilson RK, Hood L, Graveley BR (2002) Analysis of the human neurexin genes: alternative splicing and the generation of protein diversity. Genomics 79:587-597. CrossRef Medline
30. 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. CrossRef Medline
31. Shipman SL, Nicoll RA (2012) Dimerization of postsynaptic neuroligin drives synaptic assembly via transsynaptic clustering of neurexin. Proc Natl Acad Sci U S A U S A 109:19432-19437. CrossRef
32. 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. CrossRef Medline
33. Südhof TC (1990) The structure of the human synapsin I gene and protein. J Biol Chem 265:7849-7852. Medline
34. 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. CrossRef Medline
35. Tabuchi K, Südhof TC (2002) Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics 79:849-859. CrossRef Medline
36. 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 Neurosci 15:389-398. CrossRef Medline
37. Tanaka H, Nogi T, Yasui N, Iwasaki K, Takagi J (2011) Structural basis for variant-specific neuroligin-binding by α-neurexin. PLoS One 6:e19411. CrossRef Medline
38. Uemura T, Lee SJ, Yasumura M, Takeuchi T, Yoshida T, Ra M, Taguchi R, Sakimura K, Mishina M (2010) Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141:1068-1079. CrossRef Medline
39. Ushkaryov YA, Petrenko AG, Geppert M, Südhof TC (1992) Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science 257:50-56. CrossRef Medline
40. Ushkaryov YA, Hata Y, Ichtchenko K, Moomaw C, Afendis S, Slaughter CA, Südhof TC (1994) Conserved domain structure of ß-Neurexins. J Biol Chem 269:11987-11992. Medline
41. 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. CrossRef Medline