Neuroligins Determine Synapse Maturation and Function

Neuron

Volumn 51, Issue 6, 2006, Pages 741-754

  Varoqueaux, Frédérique ^a   Aramuni, Gayane ^b   Rawson, Randi L ^a   Mohrmann, Ralf ^c,d   Missler, Markus ^b,e,f   Gottmann, Kurt ^a,c,g   Zhang, Weiqi ^b   Südhof, Thomas C ^e   Brose, Nils ^a,e  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f OTTO VON GUERICKE UNIVERSITY   (Germany)

^g HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

MOLNEURO; SIGNALING

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; BETA DYSTROGLYCAN; CALBINDIN; CELL ADHESION MOLECULE; GEPHYRIN; GLYCINE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUREXIN; NEUROLIGIN; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTISM; CELL ADHESION; CONTROLLED STUDY; DELETION MUTANT; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; NERVE CELL NETWORK; NEWBORN; NONHUMAN; NORTHERN BLOTTING; PATCH CLAMP; PRIORITY JOURNAL; RAT; RESPIRATION CENTER; RESPIRATORY FAILURE; SYNAPTOGENESIS; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN; BRAIN STEM; CELLS, CULTURED; GENE EXPRESSION; IN SITU HYBRIDIZATION; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; NEURONS; PHENOTYPE; RESPIRATORY INSUFFICIENCY; RNA, MESSENGER; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS; SYNAPSES;

EID: 33748531328     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.09.003     Document Type: Article

References (51)

1. Alvarez V.A., Ridenour D.A., and Sabatini B.L. Retraction of synapses and dendritic spines induced by off-target effects of RNA interference. J. Neurosci. 26 (2006) 7820-7825
2. Augustin I., Betz A., Herrmann C., Jo T., and Brose N. Differential expression of two novel Munc13 proteins in rat brain. Biochem. J. 337 (1999) 363-371
3. Biederer T., and Südhof T.C. Mints as adaptors. Direct binding to neurexins and recruitment of munc18. J. Biol. Chem. 275 (2000) 39803-39806
4. Boucard A.A., Chubykin A.A., Comoletti D., Taylor P., and Südhof T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 48 (2005) 229-236
5. Chih B., Afridi S.K., Clark L., and Scheiffele P. Disorder-associated mutations lead to functional inactivation of neuroligins. Hum. Mol. Genet. 13 (2004) 1471-1477
6. Chih B., Engelman H., and Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307 (2005) 1324-1328
7. Chih B., Gollan L., and Scheiffele P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51 (2006) 171-178
8. Chubykin A.A., Liu X., Comoletti D., Tsigelny I., Taylor P., and Südhof T.C. Dissection of synapse induction by neuroligins: Effects of a neuroligin mutation associated with autism. J. Biol. Chem. 280 (2005) 22365-22374
9. Comoletti D., De Jaco A., Jennings L.L., Flynn R.E., Gaietta G., Tsigelny I., Ellisman M.H., and Taylor P. The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing. J. Neurosci. 24 (2004) 4889-4893
10. Dean C., Scholl F.G., Choih J., DeMaria S., Berger J., Isacoff E., and Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6 (2003) 708-716
11. Dresbach T., Neeb A., Meyer G., Gundelfinger E.D., and Brose N. Synaptic targeting of neuroligin is independent of neurexin and SAP90/PSD95 binding. Mol. Cell. Neurosci. 27 (2004) 227-235
12. Ehlers M.D. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6 (2003) 231-242
13. El-Husseini A., Schnell E., Dakoji S., Sweeney N., Zhou Q., Prange O., Gauthier-Campbell C., Aguilera-Moreno A., Nicoll R.A., and Bredt D.S. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108 (2002) 849-863
14. Fu Z., Washbourne P., Ortinski P., and Vicini S. Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors. J. Neurophysiol. 90 (2003) 3950-3957
15. Fukata Y., Tzingounis A.V., Trinidad J.C., Fukata M., Burlingame A.L., Nicoll R.A., and Bredt D.S. Molecular constituents of neuronal AMPA receptors. J. Cell Biol. 169 (2005) 399-404
16. Garner C.C., Zhai R.G., Gundelfinger E.D., and Ziv N.E. Molecular mechanisms of CNS synaptogenesis. Trends Neurosci. 25 (2002) 243-251
17. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., and Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119 (2004) 1013-1026
18. Hata Y., Butz S., and Südhof T.C. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16 (1996) 2488-2494
19. Herbert M.R. Large brains in autism: the challenge of pervasive abnormality. Neuroscientist 11 (2005) 417-440
20. Hirao K., Hata Y., Ide N., Takeuchi M., Irie M., Yao I., Deguchi M., Toyoda A., Südhof T.C., and Takai Y. A novel multiple PDZ domain-containing molecule interacting with N-methyl-D-aspartate receptors and neuronal cell adhesion proteins. J. Biol. Chem. 273 (1998) 21105-21110
21. Ichtchenko K., Hata Y., Nguyen T., Ullrich B., Missler M., Moomaw C., and Südhof T.C. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 81 (1995) 435-443
22. Ichtchenko K., Nguyen T., and Südhof T.C. Structures, alternative splicing, and neurexin binding of multiple neuroligins. J. Biol. Chem. 271 (1996) 2676-2682
23. Irie M., Hata Y., Takeuchi M., Ichtchenko K., Toyoda A., Hirao K., Takai Y., Rosahl T.W., and Südhof T.C. Binding of neuroligins to PSD-95. Science 277 (1997) 1511-1515
24. Jamain S., Quach H., Betancur C., Rastam M., Colineaux C., Gillberg I.C., Soderstrom H., Giros B., Leboyer M., Gillberg C., and Bourgeron T. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 34 (2003) 27-29
25. Kim E., and Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5 (2004) 771-781
26. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378 (1995) 85-88
27. Kornau H.C., Schenker L.T., Kennedy M.B., and Seeburg P.H. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269 (1995) 1737-1740
28. Laumonnier F., Bonnet-Brilhault F., Gomot M., Blanc R., David A., Moizard M.P., Raynaud M., Ronce N., Lemonnier E., Calvas P., et al. X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am. J. Hum. Genet. 74 (2004) 552-557
29. Levinson J.N., Chery N., Huang K., Wong T.P., Gerrow K., Kang R., Prange O., Wang Y.T., and 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. 280 (2005) 17312-17319
30. Li Z., and Sheng M. Some assembly required: the development of neuronal synapses. Nat. Rev. Mol. Cell Biol. 4 (2003) 833-841
31. McMahon H.T., Bolshakov V.Y., Janz R., Hammer R.E., Siegelbaum S.A., and Südhof T.C. Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc. Natl. Acad. Sci. USA 93 (1996) 4760-4764
32. Meyer G., Varoqueaux F., Neeb A., Oschlies M., and Brose N. The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 47 (2004) 724-733
33. 2+ channels to synaptic vesicle exocytosis. Nature 423 (2003) 939-948
34. Mohrmann R., Werner M., Hatt H., and Gottmann K. Target-specific factors regulate the formation of glutamatergic transmitter release sites in cultured neocortical neurons. J. Neurosci. 19 (1999) 10004-10013
35. Montgomery J.M., Zamorano P.L., and Garner C.C. MAGUKs in synapse assembly and function: an emerging view. Cell. Mol. Life Sci. 61 (2004) 911-929
36. Nam C.I., and Chen L. Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc. Natl. Acad. Sci. USA 102 (2005) 6137-6142
37. Polleux F., and Lauder J.M. Toward a developmental neurobiology of autism. Ment. Retard. Dev. Disabil. Res. Rev. 10 (2004) 303-317
38. Prange O., Wong T.P., Gerrow K., Wang Y.T., and El-Husseini A. A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc. Natl. Acad. Sci. USA 101 (2004) 13915-13920
39. A-mediated inhibition in the brainstem respiratory rhythm-generating network of the mouse. Eur. J. Neurosci. 12 (2000) 2975-2984
40. Scheiffele P. Cell-cell signaling during synapse formation in the CNS. Annu. Rev. Neurosci. 26 (2003) 485-508
41. Scheiffele P., Fan J., Choih J., Fetter R., and Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101 (2000) 657-669
42. Schnell E., Sizemore M., Karimzadegan S., Chen L., Bredt D.S., and Nicoll R.A. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. USA 99 (2002) 13902-13907
43. Serafini T. Finding a partner in a crowd: neuronal diversity and synaptogenesis. Cell 98 (1999) 133-136
44. Song J.Y., Ichtchenko K., Südhof T.C., and Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. USA 96 (1999) 1100-1105
45. Sperry R.W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50 (1963) 703-710
46. Talebizadeh Z., Lam D.Y., Theodoro M.F., Bittel D.C., Lushington G.H., and Butler M.G. Novel splice isoforms for NLGN3 and NLGN4 with possible implications in autism. J. Med. Genet. 43 (2006) e21
47. Tarsa L., and Goda Y. Synaptophysin regulates activity-dependent synapse formation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 99 (2002) 1012-1016
48. Turrigiano G.G., and Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5 (2004) 97-107
49. Varoqueaux F., Jamain S., and Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 83 (2004) 449-456
50. Yamagata M., Sanes J.R., and Weiner J.A. Synaptic adhesion molecules. Curr. Opin. Cell Biol. 15 (2003) 621-632
51. 2+ channels. J. Neurosci. 25 (2005) 4330-4342