Calsyntenin-3 molecular architecture and interaction with neurexin 1α

Journal of Biological Chemistry

Volumn 289, Issue 50, 2014, Pages 34530-34542

  Lu, Zhuoyang ^b,c   Wang, Yun ^e   Chen, Fang ^e   Tong, Huimin ^b   Reddy, M V V V Sekhar ^a   Luo, Lin ^d   Seshadrinathan, Suchithra ^a   Zhang, Lei ^b   Holthauzen, Luis Marcelo F ^a   Craig, Ann Marie ^d   Ren, Gang ^b   Rudenko, Gabby ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c XI'AN JIAOTONG UNIVERSITY   (China)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; COMPLEX NETWORKS; COVALENT BONDS; MONOMERS; NUMBER THEORY; OLIGOMERS;

CELL-BASED ASSAYS; DIFFERENT MECHANISMS; EXTRACELLULAR DOMAINS; ITS ARCHITECTURE; MOLECULAR ARCHITECTURE; NANOMOLAR AFFINITY; RADIALLY SYMMETRIC; SYNAPTIC COMPLEX;

NETWORK ARCHITECTURE;

CALCIUM; CALSYNTENIN 3; MONOMER; NEUREXIN; NEUREXIN 1; NEUROLIGIN; NEUROLIGIN 2; PROTEIN; TETRAMER; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; CELL SURFACE RECEPTOR; CLSTN3 PROTEIN, HUMAN; MEMBRANE PROTEIN; NEUREXIN 1 PROTEIN, RAT; PROTEIN BINDING;

ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEARNING; MEMORY; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; POSTSYNAPTIC MEMBRANE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; AMINO ACID SEQUENCE; ANIMAL; BOVINE; CHEMICAL STRUCTURE; CHEMISTRY; EXTRACELLULAR SPACE; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RAT; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CATTLE; EXTRACELLULAR SPACE; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, CELL SURFACE; SYNAPSES;

EID: 84919338468     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.606806     Document Type: Article

References (48)

1. Siddiqui, T. J., and Craig, A. M. (2011) Synaptic organizing complexes. Curr. Opin. Neurobiol. 21, 132-143
2. Missler, M., Südhof, T. C., and Biederer, T. (2012) Synaptic cell adhesion. Cold Spring Harb. Perspect. Biol. 4, a005694
3. Pettem, K. L., Yokomaku, D., Luo, L., Linhoff, M. W., Prasad, T., Connor, S. A., Siddiqui, T. J., Kawabe, H., Chen, F., Zhang, L., Rudenko, G., Wang, Y. T., Brose, N., and Craig, A. M. (2013) The specific α-neurexin interactor calsyntenin-3 promotes excitatory and inhibitory synapse development. Neuron 80, 113-128
4. Um, J. W., Pramanik, G., Ko, J. S., Song, M. Y., Lee, D., Kim, H., Park, K. S., Südhof, T. C., Tabuchi, K., and Ko, J. (2014) Calsyntenins function as synaptogenic adhesion molecules in concert with neurexins. Cell Rep. 6, 1096-1109
5. Hintsch, G., Zurlinden, A., Meskenaite, V., Steuble, M., Fink-Widmer, K., Kinter, J., and Sonderegger, P. (2002) The calsyntenins: a family of postsynaptic membrane proteins with distinct neuronal expression patterns. Mol. Cell Neurosci. 21, 393-409
6. Papassotiropoulos, A., Stephan, D. A., Huentelman, M. J., Hoerndli, F. J., Craig, D. W., Pearson, J. V., Huynh, K. D., Brunner, F., Corneveaux, J., Osborne, D., Wollmer, M. A., Aerni, A., Coluccia, D., Hänggi, J., Mondadori, C. R., Buchmann, A., Reiman, E. M., Caselli, R. J., Henke, K., and de Quervain, D. J. (2006) Common Kibra alleles are associated with human memory performance. Science 314, 475-478
7. Ikeda, D. D., Duan, Y., Matsuki, M., Kunitomo, H., Hutter, H., Hedgecock, E. M., and Iino, Y. (2008) CASY-1, an ortholog of calsyntenins/alcadeins, is essential for learning in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 105, 5260-5265
8. Hoerndli, F. J., Walser, M., Fröhli, Hoier, E., de Quervain, D., Papassotiropoulos, A., and Hajnal, A. (2009) A conserved function of C. elegans CASY-1 calsyntenin in associative learning. PLoS One 4, e4880
9. Araki, Y., Tomita, S., Yamaguchi, H., Miyagi, N., Sumioka, A., Kirino, Y., and Suzuki, T. (2003) Novel cadherin-related membrane proteins, Alcadeins, enhance the X11-like protein-mediated stabilization of amyloid β-protein precursor metabolism. J. Biol. Chem. 278, 49448-49458
10. Vagnoni, A., Perkinton, M. S., Gray, E. H., Francis, P. T., Noble, W., and Miller, C. C. (2012) Calsyntenin-1 mediates axonal transport of the amyloid precursor protein and regulates Aβ production. Hum. Mol. Genet. 21, 2845-2854
11. Steuble, M., Diep, T. M., Schätzle, P., Ludwig, A., Tagaya, M., Kunz, B., and Sonderegger, P. (2012) Calsyntenin-1 shelters APP from proteolytic processing during anterograde axonal transport. Biol. Open 1, 761-774
12. Francks, C., Maegawa, S., Laurén, J., Abrahams, B. S., Velayos-Baeza, A., Medland, S. E., Colella, S., Groszer, M., McAuley, E. Z., Caffrey, T. M., Timmusk, T., Pruunsild, P., Koppel, I., Lind, P. A., Matsumoto-Itaba, N., Nicod, J., Xiong, L., Joober, R., Enard, W., Krinsky, B., Nanba, E., Richardson, A. J., Riley, B. P., Martin, N. G., Strittmatter, S. M., Möller, H. J., Rujescu, D., St Clair, D., Muglia, P., Roos, J. L., Fisher, S. E., Wade-Martins, R., Rouleau, G. A., Stein, J. F., Karayiorgou, M., Geschwind, D. H., Ragoussis, J., Kendler, K. S., Airaksinen, M. S., Oshimura, M., DeLisi, L. E., and Monaco, A. P. (2007) LRRTM1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia. Mol. Psychiatry 12, 1129-1139, 1057
13. Betancur, C., Sakurai, T., and Buxbaum, J. D. (2009) The emerging role of synaptic cell-adhesion pathways in the pathogenesis of autism spectrum disorders. Trends Neurosci. 32, 402-412
14. Béna, F., Bruno, D. L., Eriksson, M., van Ravenswaaij-Arts, C., Stark, Z., Dijkhuizen, T., Gerkes, E., Gimelli, S., Ganesamoorthy, D., Thuresson, A. C., Labalme, A., Till, M., Bilan, F., Pasquier, L., Kitzis, A., Dubourgm, C., Rossi, M., Bottani, A., Gagnebin, M., Sanlaville, D., Gilbert-Dussardier, B., Guipponi, M., van Haeringen, A., Kriek, M., Ruivenkamp, C., Antonarakis, S. E., Anderlid, B. M., Slater, H. R., and Schoumans, J. (2013) NRXN1 and comprehensive review of the literature. Am. J. Med. Genet. B Neuropsychiatr. Genet. 162B, 388-403
15. Südhof, T. C. (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911
16. Chen, F., Venugopal, V., Murray, B., and Rudenko, G. (2011) The structure of neurexin 1α reveals features promoting a role as synaptic organizer. Structure 19, 779-789
17. Miller, M. T., Mileni, M., Comoletti, D., Stevens, R. C., Harel, M., and Taylor, P. (2011) The crystal structure of the α-neurexin-1 extracellular region reveals a hinge point for mediating synaptic adhesion and function. Structure 19, 767-778
18. Treutlein, B., Gokce, O., Quake, S. R., and Südhof, T. C. (2014) Cartography of neurexin alternative splicing mapped by single-molecule long-read mRNA sequencing. Proc. Natl. Acad. Sci. U.S.A. 111, E1291-E1299
19. Rudenko, G., Nguyen, T., Chelliah, Y., Südhof, T. C., and Deisenhofer, J. (1999) The structure of the ligand-binding domain of neurexin Iβ: regulation of LNS domain function by alternative splicing. Cell 99, 93-101
20. 2+ binding and the effects of alternative splicing. J. Biol. Chem. 281, 22896-22905
21. Graf, E. R., Kang, Y., Hauner, A. M., and Craig, A. M. (2006) Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 β LNS domain. J. Neurosci. 26, 4256-4265
22. Siddiqui, T. J., Pancaroglu, R., Kang, Y., Rooyakkers, A., and Craig, A. M. (2010) LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development. J. Neurosci. 30, 7495-7506
23. 2+-interactions. Neuron 56, 992-1003
24. Fabrichny, I. P., Leone, P., Sulzenbacher, G., Comoletti, D., Miller, M. T., Taylor, P., Bourne, Y., and Marchot, P. (2007) Structural analysis of the synaptic protein neuroligin and its β-neurexin complex: determinants for folding and cell adhesion. Neuron 56, 979-991
25. Chen, X., Liu, H., Shim, A. H., Focia, P. J., and He, X. (2008) Structural basis for synaptic adhesion mediated by neuroligin-neurexin interactions. Nat. Struct. Mol. Biol. 15, 50-56
26. Shen, K. C., Kuczynska, D. A., Wu, I. J., Murray, B. H., Sheckler, L. R., and Rudenko, G. (2008) Regulation of neurexin 1beta tertiary structure and ligand binding through alternative splicing. Structure 16, 422-431
27. Zhang, L., Song, J., Newhouse, Y., Zhang, S., Weisgraber, K. H., and Ren, G. (2010) An optimized negative-staining protocol of electron microscopy for apoE4.POPC lipoprotein. J. Lipid Res. 51, 1228-1236
28. Rames, M., Yu, Y., and Ren, G. (2014) Optimized negative staining: a high-throughput protocol for examining small and asymmetric protein structure by electron microscopy. J. Vis. Exp. 90, e51087
29. Grigorieff, N. (2007) FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 157, 117-125
30. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., and Leith, A. (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199
31. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97
32. Kremer, J. R., Mastronarde, D. N., and McIntosh, J. R. (1996) Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76
33. Fernández, J. J., Li, S., and Crowther, R. A. (2006) CTF determination and correction in electron cryotomography. Ultramicroscopy 106, 587-596
34. Zhang, L., and Ren, G. (2012) IPET and FETR: experimental approach for studying molecular structure dynamics by cryo-electron tomography of a single-molecule structure. PLoS One 7, e30249
35. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
36. Patel, S. D., Ciatto, C., Chen, C. P., Bahna, F., Rajebhosale, M., Arkus, N., Schieren, I., Jessell, T. M., Honig, B., Price, S. R., and Shapiro, L. (2006) Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124, 1255-1268
37. Kang, Y., Zhang, X., Dobie, F., Wu, H., and Craig, A. M. (2008) Induction of GABAergic postsynaptic differentiation by α-neurexins. J. Biol. Chem. 283, 2323-2334
38. Ko, J., Fuccillo, M. V., Malenka, R. C., and Südhof, T. C. (2009) LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 64, 791-798
39. Boucard, A. A., Ko, J., and Südhof, T. C. (2012) High affinity neurexin binding to cell adhesion G-protein-coupled receptor CIRL1/latrophilin-1 produces an intercellular adhesion complex. J. Biol. Chem. 287, 9399-9413
40. Poulopoulos, A., Soykan, T., Tuffy, L. P., Hammer, M., Varoqueaux, F., and Brose, N. (2012) Homodimerization and isoform-specific heterodimerization of neuroligins. Biochem. J. 446, 321-330
41. Ko, J., Zhang, C., Arac, D., Boucard, A. A., Brunger, A. T., and Südhof, T. C. (2009) Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J. 28, 3244-3255
42. Shipman, S. L., and Nicoll, R. A. (2012) Dimerization of postsynaptic neuroligin drives synaptic assembly via transsynaptic clustering of neurexin. Proc. Natl. Acad. Sci. U.S.A. 109, 19432-19437
43. Dean, C., Scholl, F. G., Choih, J., DeMaria, S., Berger, J., Isacoff, E., and Scheiffele, P. (2003) Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6, 708-716
44. Makagiansar, I. T., Nguyen, P. D., Ikesue, A., Kuczera, K., Dentler, W., Urbauer, J. L., Galeva, N., Alterman, M., and Siahaan, T. J. (2002) Disulfide bond formation promotes the cis- and trans-dimerization of the E-cadherin-derived first repeat. J. Biol. Chem. 277, 16002-16010
45. Schreiner, D., and Weiner, J. A. (2010) Combinatorial homophilic interaction between γ-protocadherin multimers greatly expands the molecular diversity of cell adhesion. Proc. Natl. Acad. Sci. U.S.A. 107, 14893-14898
46. Grimm, S., Hoehn, A., Davies, K. J., and Grune, T. (2011) Protein oxidative modifications in the ageing brain: consequence for the onset of neurodegenerative disease. Free Radic. Res. 45, 73-88
47. Lee, S. J., Uemura, T., Yoshida, T., and Mishina, M. (2012) GluRδ2 assembles four neurexins into trans-synaptic triad to trigger synapse formation. J. Neurosci. 32, 4688-4701
48. Shapiro, L., and Weis, W. I. (2009) Structure and biochemistry of cadherins and catenins. Cold Spring Harb. Perspect. Biol. 1, a003053