Structural insights into the exquisite selectivity of neurexin/neuroligin synaptic interactions

EMBO Journal

Volumn 29, Issue 14, 2010, Pages 2461-2471

  Leone, Philippe ^a   Comoletti, Davide ^b   Ferracci, Géraldine ^a   Conrod, Sandrine ^a   Garcia, Simon U ^b   Taylor, Palmer ^b   Bourne, Yves ^a   Marchot, Pascale ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b San Diego   (United States)

Author keywords

autism spectrum disorders; cholinesterase like domain; conformational rearrangement; synaptic adhesion; hydrolase fold

Indexed keywords

CALCIUM ION; MUTANT PROTEIN; NEUREXIN; NEUREXIN 1BETA; NEUROLIGIN; NEUROLIGIN 1; NEUROLIGIN 2; NEUROLIGIN 4; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; IONIC STRENGTH; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; SYNAPTIC TRANSMISSION;

EID: 77954886772     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.123     Document Type: Article

References (65)

1. 2+ interactions. Neuron 56: 992-1003
2. Bolliger MF, Frei K, Winterhalter KH, Gloor SM (2001) Identification of a novel neuroligin in humans which binds to PSD-95 and has a widespread expression. Biochem J 356: 581-588
3. Bolliger MF, Pei J, Maxeiner S, Boucard AA, Grishin NV, Südhof TC (2008) Unusually rapid evolution of Neuroligin-4 in mice. Proc Natl Acad Sci USA 105: 6421-6426
4. 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 a-and b-neurexins. Neuron 48: 229-236
5. Budreck EC, Scheiffele P (2007) Neuroligin-3 is a neuronal adhesion protein at GABAergic and glutamatergic synapses. Eur J Neurosci 26: 1738-1748
6. Chen X, Liu H, Shim AH, Focia PJ, He X (2008) Structural basis for synaptic adhesion mediated by neuroligin-neurexin interactions. Nat Struct Mol Biol 15: 50-56
7. Chesler M, Kaila K (1992) Modulation of pH by neuronal activity. Trends Neurosci 15: 396-402
8. Chih B, Gollan L, Scheiffele P (2006) Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51: 171-178
9. 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
10. Cline H (2005) Synaptogenesis: a balancing act between excitation and inhibition. Curr Biol 15: R203-R205
11. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763
12. 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 Neurosci 24: 4889-4893
13. Comoletti D, Flynn R, Jennings LL, Chubykin A, Matsumura T, Hasegawa H, Südhof TC, Taylor P (2003) Characterization of the interaction of a recombinant soluble neuroligin-1 with neurexin-1b. J Biol Chem 278: 50497-50505
14. 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 b-neurexins. Biochemistry 45: 12816-12827
15. Comoletti D, Grishaev A, Whitten AE, Tsigelny I, Taylor P, Trewhella J (2007) Synaptic arrangement of the neuroligin/b-neurexin complex revealed by X-ray and neutron scattering. Structure 15: 693-705
16. Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: signalling functions at the synapse. Nat Rev Neurosci 8: 206-220
17. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132
18. 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 b-neurexin complex: determinants for folding and cell adhesion. Neuron 56: 979-991
19. Feng J, Schroer R, Yan J, Song W, Yang C, Bockholt A, Cook Jr EH, Skinner C, Schwartz CE, Sommer SS (2006) High frequency of neurexin 1b signal peptide structural variants in patients with autism. Neurosci Lett 409: 10-13
20. Fu Z, Washbourne P, Ortinski P, Vicini S (2003) Functional excitatory synapses in HEK293 cells expressing neuroligin and gluta-mate receptors. J Neurophysiol 90: 3950-3957
21. Gerrow K, El-Husseini A (2006) Cell adhesion molecules at the synapse. Front Biosci 11: 2400-2419
22. Glessner JT, Wang K, Cai G, Korvatska O, Kim CE, Wood S, Zhang H, Estes A, Brune CW, Bradfield JP, Imielinski M, Frackelton EC, Reichert J, Crawford EL, Munson J, Sleiman PM, Chiavacci R, Annaiah K, Thomas K, Hou C et al (2009) Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature 459: 569-573
23. Graf ER, Kang Y, Hauner AM, Craig AM (2006) Structure function and splice site analysis of the synaptogenic activity of the neurexin-1b LNS domain. J Neurosci 26: 4256-4265
24. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119: 1013-1026
25. Ichtchenko K, Nguyen T, Südhof TC (1996) Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 271: 2676-2682
26. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, Gillberg IC, Soderstrom H, Giros B, Leboyer M, Gillberg C, Bourgeron T, Paris Autism Research International Sibpair Study (2003) Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 34: 27-29
27. 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 USA 105: 1710-1715
28. Kang Y, Zhang X, Dobie F, Wu H, Craig AM (2008) Induction of GABAergic postsynaptic differentiation by a-neurexins. J Biol Chem 283: 2323-2334
29. Kim HG, Kishikawa S, Higgins AW, Seong IS, Donovan DJ, Shen Y, Lally E, Weiss LA, Najm J, Kutsche K, Descartes M, Holt L, Braddock S, Troxell R, Kaplan L, Volkmar F, Klin A, Tsatsanis K, Harris DJ, Noens I et al (2008) Disruption of neurexin 1 associated with autism spectrum disorder. Am J Hum Genet 82: 199-207
30. Kleywegt GJ (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr D Biol Crystallogr 52: 842-857
31. Koehnke J, Jin X, Trbovic N, Katsamba PS, Brasch J, Ahlsen G, Scheiffele P, Honig B, Palmer AG, Shapiro L (2008) Crystal structures of b-neurexin 1 and b-neurexin 2 ectodomains and dynamics of splice insertion sequence 4. Structure 16: 410-421
32. Krishtal OA, Osipchuk YV, Shelest TN, Smirnoff SV (1987) Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices. Brain Res 436: 352-356
33. 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 Genet 74: 552-557
34. Leslie AGW (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB. Newsletter on Protein Crystallography, No. 26
35. Levinson JN, El-Husseini A (2005) Building excitatory and inhibitory synapses: balancing neuroligin partnerships. Neuron 48: 171-174
36. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 39: 192-195
37. 2+ channels to synaptic vesicle exocytosis. Nature 423: 939-948
38. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macro-molecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255
39. Nam CI, Chen L (2005) Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci USA 102: 6137-6142
40. Nguyen T, Südhof TC (1997) Binding properties of neuroligin 1 and neurexin 1b reveal function as heterophilic cell adhesion molecules. J Biol Chem 272: 26032-26039
41. Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62: 439-450
42. Philibert RA, Winfield SL, Sandhu HK, Martin BM, Ginns EI (2000) The structure and expression of the human neuroligin-3 gene. Gene 246: 303-310
43. Potterton E, McNicholas S, Krissinel E, Cowtan K, Noble M (2002) The CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 58: 1955-1957
44. 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 USA 105: 15124-15129
45. 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
46. Rudenko G, Nguyen T, Chelliah Y, Südhof TC, Deisenhofer J (1999) The structure of the ligand-binding domain of neurexin Ib: regulation of LNS domain function by alternative splicing. Cell 99: 93-101
47. 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
48. 2+ binding and the effects of alternative splicing. J Biol Chem 281: 22896-22905
49. Shen KC, Kuczynska DA, Wu IJ, Murray BH, Sheckler LR, Rudenko G (2008) Regulation of neurexin 1b tertiary structure and ligand binding through alternative splicing. Structure 16: 422-431
50. Sitia R, Braakman I (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426: 891-894
51. Song JY, Ichtchenko K, Südhof TC, Brose N (1999) Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci USA 96: 1100-1105
52. Südhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455: 903-911
53. 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
54. Tabuchi K, Südhof TC (2002) Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics 79: 849-859
55. Talebizadeh Z, Lam DY, Theodoro MF, Bittel DC, Lushington GH, Butler MG (2006) Novel splice isoforms for NLGN3 and NLGN4 with possible implications in autism. J Med Genet 43: e21
56. The Autism Genome Project Consortium (2007) Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 39: 319-328
57. Ushkaryov YA, Petrenko AG, Geppert M, Südhof TC (1992) Neurexins: synaptic cell surface proteins related to the a-latrotox-in receptor and laminin. Science 257: 50-56
58. Vagin A, Teplyakov A (1997) MOLREP: an automated program for molecular replacement. J Appl Cryst 30: 1022-1025
59. 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
60. Varoqueaux F, Jamain S, Brose N (2004) Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 83: 449-456
61. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M (1997) A proton-gated cation channel involved in acid-sensing. Nature 386: 173-177
62. Wemmie JA, Chen J, Askwith CC, Hruska-Hageman AM, Price MP, Nolan BC, Yoder PG, Lamani E, Hoshi T, Freeman Jr JH, Welsh MJ (2002) The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34: 463-477
63. Yan J, Noltner K, Feng J, Li W, Schroer R, Skinner C, Zeng W, Schwartz CE, Sommer SS (2008) Neurexin 1a structural variants associated with autism. Neurosci Lett 438: 368-370
64. Yan J, Oliveira G, Coutinho A, Yang C, Feng J, Katz C, Sram J, Bockholt A, Jones IR, Craddock N, Cook EH, Vicente A, Sommer SS (2005) Analysis of the neuroligin 3 and 4 genes in autism and other neuropsychiatric patients. Mol Psychiatry 10: 329-332
65. 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 reti-culum export. J Neurosci 29: 10843-10854