Structural basis for variant-specific neuroligin-binding by α-neurexin

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Tanaka, Hiroki ^a   Nogi, Terukazu ^a   Yasui, Norihisa ^a,b   Iwasaki, Kenji ^a   Takagi, Junichi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; NEUREXIN; NEUREXIN 1ALPHA; NEUREXIN 1BETA; NEUROLIGIN; UNCLASSIFIED DRUG; GLYCOPROTEIN; ISOPROTEIN; NERVE CELL ADHESION MOLECULE; NEUREXOPHILIN; NEUROLIGIN 1; NEUROPEPTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; MOLECULAR RECOGNITION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ECTODOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN VARIANT; SEQUENCE ALIGNMENT; AMINO ACID SEQUENCE; ANIMAL; CATTLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CELL ADHESION MOLECULES, NEURONAL; EXTRACELLULAR MATRIX; GLYCOPROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; SYNAPSES;

EID: 79955734152     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019411     Document Type: Article

References (51)

1. Craig AM, Kang Y, (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17: 43-52.
2. Dean C, Dresbach T, (2006) Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29: 21-29.
3. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, et al. (2003) Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6: 708-716.
4. 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.
5. Nam CI, Chen L, (2005) Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci U S A 102: 6137-6142.
6. 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.
7. Sudhof TC, (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455: 903-911.
8. Lise MF, El-Husseini A, (2006) The neuroligin and neurexin families: from structure to function at the synapse. Cell Mol Life Sci 63: 1833-1849.
9. Missler M, Sudhof TC, (1998) Neurexins: three genes and 1001 products. Trends Genet 14: 20-26.
10. Chih B, Gollan L, Scheiffele P, (2006) Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51: 171-178.
11. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, et al. (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54: 919-931.
12. Ko J, Zhang C, Arac D, Boucard AA, Brunger AT, et al. (2009) Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J 28: 3244-3255.
13. Ullrich B, Ushkaryov YA, Sudhof TC, (1995) Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron 14: 497-507.
14. Ushkaryov YA, Sudhof TC, (1993) Neurexin III alpha: extensive alternative splicing generates membrane-bound and soluble forms. Proc Natl Acad Sci U S A 90: 6410-6414.
15. Bellen HJ, Lu Y, Beckstead R, Bhat MA, (1998) Neurexin IV, caspr and paranodin-novel members of the neurexin family: encounters of axons and glia. Trends Neurosci 21: 444-449.
16. Nollet F, Kools P, van Roy F, (2000) Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 299: 551-572.
17. Richard M, Roepman R, Aartsen WM, van Rossum AG, den Hollander AI, et al. (2006) Towards understanding CRUMBS function in retinal dystrophies. Hum Mol Genet 15 Spec No 2: R235-R243.
18. Boucard AA, Chubykin AA, Comoletti D, Taylor P, Sudhof TC, (2005) A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 48: 229-236.
19. Kang Y, Zhang X, Dobie F, Wu H, Craig AM, (2008) Induction of GABAergic postsynaptic differentiation by alpha-neurexins. J Biol Chem 283: 2323-2334.
20. Geppert M, Khvotchev M, Krasnoperov V, Goda Y, Missler M, et al. (1998) Neurexin I alpha is a major alpha-latrotoxin receptor that cooperates in alpha-latrotoxin action. J Biol Chem 273: 1705-1710.
21. Missler M, Hammer RE, Sudhof TC, (1998) Neurexophilin binding to alpha-neurexins. A single LNS domain functions as an independently folding ligand-binding unit. J Biol Chem 273: 34716-34723.
22. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, et al. (2003) Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423: 939-948.
23. Koehnke J, Jin X, Trbovic N, Katsamba PS, Brasch J, et al. (2008) Crystal structures of beta-neurexin 1 and beta-neurexin 2 ectodomains and dynamics of splice insertion sequence 4. Structure 16: 410-421.
24. Koehnke J, Katsamba PS, Ahlsen G, Bahna F, Vendome J, et al. (2010) Splice form dependence of beta-neurexin/neuroligin binding interactions. Neuron 67: 61-74.
25. Shen KC, Kuczynska DA, Wu IJ, Murray BH, Sheckler LR, et al. (2008) Regulation of neurexin 1beta tertiary structure and ligand binding through alternative splicing. Structure 16: 422-431.
26. Rudenko G, Nguyen T, Chelliah Y, Sudhof TC, Deisenhofer J, (1999) The structure of the ligand-binding domain of neurexin Ibeta: regulation of LNS domain function by alternative splicing. Cell 99: 93-101.
27. Arac D, Boucard AA, Ozkan E, Strop P, Newell E, et al. (2007) Structures of neuroligin-1 and the neuroligin-1/neurexin-1 beta complex reveal specific protein-protein and protein-Ca2+ interactions. Neuron 56: 992-1003.
28. 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.
29. Fabrichny IP, Leone P, Sulzenbacher G, Comoletti D, Miller MT, et al. (2007) Structural analysis of the synaptic protein neuroligin and its beta-neurexin complex: determinants for folding and cell adhesion. Neuron 56: 979-991.
30. Sheckler LR, Henry L, Sugita S, Sudhof TC, Rudenko G, (2006) Crystal structure of the second LNS/LG domain from neurexin 1alpha: Ca2+ binding and the effects of alternative splicing. J Biol Chem 281: 22896-22905.
31. 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 U S A 105: 15124-15129.
32. Harding MM, (2001) Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr 57: 401-411.
33. Stetefeld J, Alexandrescu AT, Maciejewski MW, Jenny M, Rathgeb-Szabo K, et al. (2004) Modulation of agrin function by alternative splicing and Ca2+ binding. Structure 12: 503-515.
34. Hoffman RC, Jennings LL, Tsigelny I, Comoletti D, Flynn RE, et al. (2004) Structural characterization of recombinant soluble rat neuroligin 1: mapping of secondary structure and glycosylation by mass spectrometry. Biochemistry 43: 1496-1506.
35. Comoletti D, Miller MT, Jeffries CM, Wilson J, Demeler B, et al. (2010) The macromolecular architecture of extracellular domain of alphaNRXN1: domain organization, flexibility, and insights into trans-synaptic disposition. Structure 18: 1044-1053.
36. Hata Y, Butz S, Sudhof TC, (1996) CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 16: 2488-2494.
37. Ichtchenko K, Nguyen T, Sudhof TC, (1996) Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 271: 2676-2682.
38. Leahy DJ, Dann CE 3rd, Longo P, Perman B, Ramyar KX, (2000) A mammalian expression vector for expression and purification of secreted proteins for structural studies. Protein Expr Purif 20: 500-506.
39. Stanley P, (1989) Chinese hamster ovary cell mutants with multiple glycosylation defects for production of glycoproteins with minimal carbohydrate heterogeneity. Mol Cell Biol 9: 377-383.
40. Otwinowski Z, Minor W, (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods Enzymol 276: 307-326.
41. Vagin A, Teplyakov A, (1997) MOLREP: an Automated Program for Molecular Replacement. J Appl Cryst 30: 1022-1025.
42. Collaborative Computational Project N (1994) Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Cryst D50: 760-763.
43. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
44. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
45. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
46. Lee B, Richards FM, (1971) The interpretation of protein structures: estimation of static accessibility. J Mol Biol 55: 379-400.
47. Krissinel E, Henrick K, (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60: 2256-2268.
48. DeLano WL, (2002) The PyMOL Molecular Graphics System San Carlos, CA, USA. DeLano Scientific.
49. Ludtke SJ, Baldwin PR, Chiu W, (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
50. Goddard TD, Huang CC, Ferrin TE, (2007) Visualizing density maps with UCSF Chimera. J Struct Biol 157: 281-287.
51. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.