Crystal Structure of an Engineered LRRTM2 Synaptic Adhesion Molecule and a Model for Neurexin Binding

Biochemistry

Volumn 55, Issue 6, 2016, Pages 914-926

  Paatero, Anja ^a   Rosti, Katja ^a   Shkumatov, Alexander V ^c   Sele, Celeste ^a   Brunello, Cecilia ^b   Kysenius, Kai ^b   Singha, Prosanta ^a   Jokinen, Ville ^d   Huttunen, Henri ^b   Kajander, Tommi ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d AALTO UNIVERSITY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING SITES; BINS; BRAIN; CELL ADHESION; CELL CULTURE; LIGANDS; MOLECULES; NEURONS; PROTEINS;

ADHESION MOLECULES; GLUTAMATERGIC SYNAPSE; HEPARAN SULFATE PROTEOGLYCANS; LEUCINE-RICH REPEATS; MOLECULAR MECHANISM; PROTEIN ENGINEERING; SEQUENCE CONSERVATION; WILD-TYPE PROTEINS;

CRYSTAL STRUCTURE;

CALCIUM; LEUCINE RICH REPEAT TRANSMEMBRANE NEURONAL 2; NERVE CELL ADHESION MOLECULE; NEUREXIN; NEUREXIN BETA 1; UNCLASSIFIED DRUG; LRRTM2 PROTEIN, MOUSE; NERVE PROTEIN; NRXN1 PROTEIN, HUMAN; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CELL ADHESION; CELL CULTURE; CELL SURFACE; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; HUMAN; IN VITRO STUDY; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RAT; SEQUENCE ALIGNMENT; SYNAPSE; THERMOSTABILITY; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DROSOPHILA; GENETICS; HEK293 CELL LINE; INSECT; METABOLISM; MOLECULAR GENETICS; NERVE CELL; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELLS, CULTURED; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA; HEK293 CELLS; HUMANS; INSECTS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULES; NEURONS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; SYNAPSES;

EID: 84958793738     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00971     Document Type: Article

References (46)

1. Sudhof, T. C. (2008) Neuroligins and neurexins link synaptic function to cognitive disease Nature 455, 903-911 10.1038/nature07456
2. Woo, J., Kwon, S. K., and Kim, E. (2009) The NGL family of leucine-rich repeat-containing synaptic adhesion molecules Mol. Cell. Neurosci. 42, 1-10 10.1016/j.mcn.2009.05.008
3. de Wit, J. and Ghosh, A. (2014) Control of neural circuit formation by leucine-rich repeat proteins Trends Neurosci. 37, 539-550 10.1016/j.tins.2014.07.004
4. Ko, J. (2012) The leucine-rich repeat superfamily of synaptic adhesion molecules: LRRTMs and slitrks Mol. Cells 34, 335-340 10.1007/s10059-012-0113-3
5. Lauren, J., Airaksinen, M. S., Saarma, M., and Timmusk, T. (2003) A novel gene family encoding leucine-rich repeat transmembrane proteins differentially expressed in the nervous system Genomics 81, 411-421 10.1016/S0888-7543(03)00030-2
6. Linhoff, M. W., Lauren, J., Cassidy, R. M., Dobie, F. A., Takahashi, H., Nygaard, H. B., Airaksinen, M. S., Strittmatter, S. M., and Craig, A. M. (2009) An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers Neuron 61, 734-749 10.1016/j.neuron.2009.01.017
7. de Wit, J., Sylwestrak, E., ÓSullivan, M. L., Otto, S., Tiglio, K., Savas, J. N., Yates, J. R., 3rd, Comoletti, D., Taylor, P., and Ghosh, A. (2009) LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation Neuron 64, 799-806 10.1016/j.neuron.2009.12.019
8. Ko, J., Fuccillo, M. V., Malenka, R. C., and Sudhof, T. C. (2009) LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation Neuron 64, 791-798 10.1016/j.neuron.2009.12.012
9. de Wit, J., ÓSullivan, M. L., Savas, J. N., Condomitti, G., Caccese, M. C., Vennekens, K. M., Yates, J. R., 3rd, and Ghosh, A. (2013) Unbiased discovery of glypican as a receptor for LRRTM4 in regulating excitatory synapse development Neuron 79, 696-711 10.1016/j.neuron.2013.06.049
10. Siddiqui, T. J., Tari, P. K., Connor, S. A., Zhang, P., Dobie, F. A., She, K., Kawabe, H., Wang, Y. T., Brose, N., and Craig, A. M. (2013) An LRRTM4-HSPG complex mediates excitatory synapse development on dentate gyrus granule cells Neuron 79, 680-695 10.1016/j.neuron.2013.06.029
11. Treutlein, B., Gokce, O., Quake, S. R., and Sudhof, T. C. (2014) Cartography of neurexin alternative splicing mapped by single-molecule long-read mRNA sequencing Proc. Natl. Acad. Sci. U. S. A. 111, E1291-9 10.1073/pnas.1403244111
12. Reissner, C., Runkel, F., and Missler, M. (2013) Neurexins Genome Biol. 14, 213 10.1186/gb-2013-14-9-213
13. Schreiner, D., Nguyen, T. M., Russo, G., Heber, S., Patrignani, A., Ahrne, E., and Scheiffele, P. (2014) Targeted combinatorial alternative splicing generates brain region-specific repertoires of neurexins Neuron 84, 386-398 10.1016/j.neuron.2014.09.011
14. 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 10.1523/JNEUROSCI.0470-10.2010
15. Tanaka, H., Miyazaki, N., Matoba, K., Nogi, T., Iwasaki, K., and Takagi, J. (2012) Higher-order architecture of cell adhesion mediated by polymorphic synaptic adhesion molecules neurexin and neuroligin Cell Rep. 2, 101-110 10.1016/j.celrep.2012.06.009
16. Reissner, C., Klose, M., Fairless, R., and 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 10.1073/pnas.0801639105
17. Koehnke, J., Jin, X., Trbovic, N., Katsamba, P. S., Brasch, J., Ahlsen, G., Scheiffele, P., Honig, B., Palmer, A. G., 3rd, and Shapiro, L. (2008) Crystal structures of beta-neurexin 1 and beta-neurexin 2 ectodomains and dynamics of splice insertion sequence 4 Structure 16, 410-421 10.1016/j.str.2007.12.024
18. Arac, D., Boucard, A. A., Ozkan, E., Strop, P., Newell, E., Sudhof, T. C., and Brunger, A. T. (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 10.1016/j.neuron.2007.12.002
19. 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 beta-neurexin complex: Determinants for folding and cell adhesion Neuron 56, 979-991 10.1016/j.neuron.2007.11.013
20. Bunch, T. A., Grinblat, Y., and Goldstein, L. S. (1988) Characterization and use of the drosophila metallothionein promoter in cultured drosophila melanogaster cells Nucleic Acids Res. 16, 1043-1061 10.1093/nar/16.3.1043
21. Keinanen, K., Jouppila, A., and Kuusinen, A. (1998) Characterization of the kainate-binding domain of the glutamate receptor GluR-6 subunit Biochem. J. 330 (Part 3) 1461-1467 10.1042/bj3301461
22. Kajava, A. V. (1998) Structural diversity of leucine-rich repeat proteins J. Mol. Biol. 277, 519-527 10.1006/jmbi.1998.1643
23. Uvarov, P., Kajander, T., and Airaksinen, M. S. (2014) Origin and loss of nested LRRTM/alpha-catenin genes during vertebrate evolution PLoS One 9, e89910 10.1371/journal.pone.0089910
24. Kajander, T., Kuja-Panula, J., Rauvala, H., and Goldman, A. (2011) Crystal structure and role of glycans and dimerization in folding of neuronal leucine-rich repeat protein AMIGO-1 J. Mol. Biol. 413, 1001-1015 10.1016/j.jmb.2011.09.032
25. Newman, J. (2004) Novel buffer systems for macromolecular crystallization Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 610-612 10.1107/S0907444903029640
26. Kabsch, W. (2010) Xds Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 125-132 10.1107/S0907444909047337
27. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 10.1107/S0021889807021206
28. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221 10.1107/S0907444909052925
29. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS: A windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36, 1277-1282 10.1107/S0021889803012779
30. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25, 495-503 10.1107/S0021889892001663
31. Petoukhov, M. V., Franke, D., Shkumatov, A. V., Tria, G., Kikhney, A. G., Gajda, M., Gorba, C., Mertens, H. D., Konarev, P. V., and Svergun, D. I. (2012) New developments in the program package for small-angle scattering data analysis J. Appl. Crystallogr. 45, 342-350 10.1107/S0021889812007662
32. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing Biophys. J. 76, 2879-2886 10.1016/S0006-3495(99)77443-6
33. Fischer, H., de Oliveira Neto, M., Napolitano, H. B., Polikarpov, I., and Craievich, A. F. (2010) (2010) Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale J. Appl. Crystallogr. 43, 101-109 10.1107/S0021889809043076
34. Svergun, D., Barberato, C., and Koch, M. H. J. (1995) CRYSOL: A program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates J. Appl. Crystallogr. 28, 768 10.1107/S0021889895007047
35. Jokinen, V., Sakha, P., Suvanto, P., Rivera, C., Franssila, S., Lauri, S. E., and Huttunen, H. J. (2013) A microfluidic chip for axonal isolation and electrophysiological measurements J. Neurosci. Methods 212, 276-282 10.1016/j.jneumeth.2012.10.013
36. Lee, S. C., Park, K., Han, J., Lee, J. J., Kim, H. J., Hong, S., Heu, W., Kim, Y. J., Ha, J. S., Lee, S. G., Cheong, H. K., Jeon, Y. H., Kim, D., and Kim, H. S. (2012) Design of a binding scaffold based on variable lymphocyte receptors of jawless vertebrates by module engineering Proc. Natl. Acad. Sci. U. S. A. 109, 3299-3304 10.1073/pnas.1113193109
37. Binz, H. K., Stumpp, M. T., Forrer, P., Amstutz, P., and Pluckthun, A. (2003) Designing repeat proteins: Well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins J. Mol. Biol. 332, 489-503 10.1016/S0022-2836(03)00896-9
38. Main, E. R., Xiong, Y., Cocco, M. J., Dándrea, L., and Regan, L. (2003) Design of stable alpha-helical arrays from an idealized TPR motif Structure 11, 497-508 10.1016/S0969-2126(03)00076-5
39. McEwan, P. A., Scott, P. G., Bishop, P. N., and Bella, J. (2006) Structural correlations in the family of small leucine-rich repeat proteins and proteoglycans J. Struct. Biol. 155, 294-305 10.1016/j.jsb.2006.01.016
40. Seiradake, E., del Toro, D., Nagel, D., Cop, F., Hartl, R., Ruff, T., Seyit-Bremer, G., Harlos, K., Border, E. C., Acker-Palmer, A., Jones, E. Y., and Klein, R. (2014) FLRT structure: Balancing repulsion and cell adhesion in cortical and vascular development Neuron 84, 370-385 10.1016/j.neuron.2014.10.008
41. Durand, D., Vives, C., Cannella, D., Perez, J., Pebay-Peyroula, E., Vachette, P., and Fieschi, F. (2010) NADPH oxidase activator p67(phox) behaves in solution as a multidomain protein with semi-flexible linkers J. Struct. Biol. 169, 45-53 10.1016/j.jsb.2009.08.009
42. de Vries, S. J., van Dijk, M., and Bonvin, A. M. (2010) The HADDOCK web server for data-driven biomolecular docking Nat. Protoc. 5, 883-897 10.1038/nprot.2010.32
43. Leone, P., Comoletti, D., Ferracci, G., Conrod, S., Garcia, S. U., Taylor, P., Bourne, Y., and Marchot, P. (2010) Structural insights into the exquisite selectivity of neurexin/neuroligin synaptic interactions EMBO J. 29, 2461-2471 10.1038/emboj.2010.123
44. 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 10.1016/j.str.2008.01.005
45. Bohne-Lang, A. and von der Lieth, C. W. (2005) GlyProt: In silico glycosylation of proteins Nucleic Acids Res. 33, W214-9 10.1093/nar/gki385
46. Shkumatov, A. V., Chinnathambi, S., Mandelkow, E., and Svergun, D. I. (2011) Structural memory of natively unfolded tau protein detected by small-angle X-ray scattering Proteins: Struct., Funct., Genet. 79, 2122-2131 10.1002/prot.23033