Extracellular architecture of the SYG-1/SYG-2 adhesion complex instructs synaptogenesis

Cell

Volumn 156, Issue 3, 2014, Pages 482-494

  Özkan, Engin ^a   Chia, Poh Hui ^b   Wang, Ruiqi Rachel ^c   Goriatcheva, Natalia ^a   Borek, Dominika ^d   Otwinowski, Zbyszek ^d   Walz, Thomas ^c   Shen, Kang ^a,b   Garcia, K Christopher ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; HOMODIMER; SYG1 PROTEIN; SYG2 PROTEIN; UNCLASSIFIED DRUG; SYG 1 PROTEIN; SYG 2 PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL ADHESION; CELL STRUCTURE; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; DISSOCIATION CONSTANT; DISULFIDE BOND; EXTRACELLULAR MATRIX; GLOMERULUS FILTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SYNAPSE; SYNAPSE VESICLE; SYNAPTOGENESIS; ANIMAL CELL; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; GEOMETRY; IN VIVO STUDY; MOLECULAR DOCKING; MOUSE; PROTEIN INTERACTION;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION; DIMERIZATION; IMMUNOGLOBULINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SYNAPSES;

EID: 84893506782     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.01.004     Document Type: Article

References (82)

1. S.M. Abmayr, and G.K. Pavlath Myoblast fusion: lessons from flies and mice Development 139 2012 641 656
2. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
3. A. Al-Amoudi, D.C. Díez, M.J. Betts, and A.S. Frangakis The molecular architecture of cadherins in native epidermal desmosomes Nature 450 2007 832 837
4. S. Bao, and R. Cagan Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye Dev. Cell 8 2005 925 935
5. P. Bork, L. Holm, and C. Sander The immunoglobulin fold. Structural classification, sequence patterns and common core J. Mol. Biol. 242 1994 309 320
6. U. Boschert, R.G. Ramos, S. Tix, G.M. Technau, and K.F. Fischbach Genetic and developmental analysis of irreC, a genetic function required for optic chiasm formation in Drosophila J. Neurogenet. 6 1990 153 171
7. D.L. Chao, and K. Shen Functional dissection of SYG-1 and SYG-2, cell adhesion molecules required for selective synaptogenesis in C. elegans Mol. Cell. Neurosci. 39 2008 248 257
8. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
9. P.H. Chia, M.R. Patel, and K. Shen NAB-1 instructs synapse assembly by linking adhesion molecules and F-actin to active zone proteins Nat. Neurosci. 15 2012 234 242
10. M. Ding, D. Chao, G. Wang, and K. Shen Spatial regulation of an E3 ubiquitin ligase directs selective synapse elimination Science 317 2007 947 951
11. H.A. Dworak, M.A. Charles, L.B. Pellerano, and H. Sink Characterization of Drosophila hibris, a gene related to human nephrin Development 128 2001 4265 4276
12. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
13. N. Eswar, B. Webb, M.A. Marti-Renom, M.S. Madhusudhan, D. Eramian, M.-Y. Shen, U. Pieper, and A. Sali Comparative protein structure modeling using Modeller Curr. Protoc. Bioinformatics 15 2006 5.6.1-5.6.30
14. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
15. B.J. Galletta, M. Chakravarti, R. Banerjee, and S.M. Abmayr SNS: Adhesive properties, localization requirements and ectodomain dependence in S2 cells and embryonic myoblasts Mech. Dev. 121 2004 1455 1468
16. P. Gerke, T.B. Huber, L. Sellin, T. Benzing, and G. Walz Homodimerization and heterodimerization of the glomerular podocyte proteins nephrin and NEPH1 J. Am. Soc. Nephrol. 14 2003 918 926
17. B. Haraldsson, J. Nyström, and W.M. Deen Properties of the glomerular barrier and mechanisms of proteinuria Physiol. Rev. 88 2008 451 487
18. O.J. Harrison, J. Vendome, J. Brasch, X. Jin, S. Hong, P.S. Katsamba, G. Ahlsen, R.B. Troyanovsky, S.M. Troyanovsky, B. Honig, and L. Shapiro Nectin ectodomain structures reveal a canonical adhesive interface Nat. Struct. Mol. Biol. 19 2012 906 915
19. D. Hatherley, S.C. Graham, J. Turner, K. Harlos, D.I. Stuart, and A.N. Barclay Paired receptor specificity explained by structures of signal regulatory proteins alone and complexed with CD47 Mol. Cell 31 2008 266 277
20. T.B. Huber, M. Schmidts, P. Gerke, B. Schermer, A. Zahn, B. Hartleben, L. Sellin, G. Walz, and T. Benzing The carboxyl terminus of Neph family members binds to the PDZ domain protein zonula occludens-1 J. Biol. Chem. 278 2003 13417 13421
21. R.O. Hynes, and Q. Zhao The evolution of cell adhesion J. Cell Biol. 150 2000 F89 F96
22. N. Jones, I.M. Blasutig, V. Eremina, J.M. Ruston, F. Bladt, H. Li, H. Huang, L. Larose, S.S.-C. Li, and T. Takano et al. Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes Nature 440 2006 818 823
23. M. Kestilä, U. Lenkkeri, M. Männikkö, J. Lamerdin, P. McCready, H. Putaala, V. Ruotsalainen, T. Morita, M. Nissinen, and R. Herva et al. Positionally cloned gene for a novel glomerular protein - nephrin - is mutated in congenital nephrotic syndrome Mol. Cell 1 1998 575 582
24. J. Khoshnoodi, K. Sigmundsson, L.-G. Ofverstedt, U. Skoglund, B. Obrink, J. Wartiovaara, and K. Tryggvason Nephrin promotes cell-cell adhesion through homophilic interactions Am. J. Pathol. 163 2003 2337 2346
25. G. Liu, B. Kaw, J. Kurfis, S. Rahmanuddin, Y.S. Kanwar, and S.S. Chugh Neph1 and nephrin interaction in the slit diaphragm is an important determinant of glomerular permeability J. Clin. Invest. 112 2003 209 221
26. E. Mizuhara, Y. Minaki, T. Nakatani, M. Kumai, T. Inoue, K. Muguruma, Y. Sasai, and Y. Ono Purkinje cells originate from cerebellar ventricular zone progenitors positive for Neph3 and E-cadherin Dev. Biol. 338 2010 202 214
27. E. Neumann-Haefelin, A. Kramer-Zucker, K. Slanchev, B. Hartleben, F. Noutsou, K. Martin, N. Wanner, A. Ritter, M. Gödel, and P. Pagel et al. A model organism approach: defining the role of Neph proteins as regulators of neuron and kidney morphogenesis Hum. Mol. Genet. 19 2010 2347 2359
28. M. Ohi, Y. Li, Y. Cheng, and T. Walz Negative staining and image classification - powerful tools in modern electron microscopy Biol. Proced. Online 6 2004 23 34
29. E. Özkan, R.A. Carrillo, C.L. Eastman, R. Weiszmann, D. Waghray, K.G. Johnson, K. Zinn, S.E. Celniker, and K.C. Garcia An extracellular interactome of immunoglobulin and LRR proteins reveals receptor-ligand networks Cell 154 2013 228 239
30. R.G. Ramos, G.L. Igloi, B. Lichte, U. Baumann, D. Maier, T. Schneider, J.H. Brandstätter, A. Fröhlich, and K.F. Fischbach The irregular chiasm C-roughest locus of Drosophila, which affects axonal projections and programmed cell death, encodes a novel immunoglobulin-like protein Genes Dev. 7 12B 1993 2533 2547
31. T. Schneider, C. Reiter, E. Eule, B. Bader, B. Lichte, Z. Nie, T. Schimansky, R.G. Ramos, and K.F. Fischbach Restricted expression of the irreC-rst protein is required for normal axonal projections of columnar visual neurons Neuron 15 1995 259 271
32. G.F. Schröder, A.T. Brunger, and M. Levitt Combining efficient conformational sampling with a deformable elastic network model facilitates structure refinement at low resolution Structure 15 2007 1630 1641
33. S. Serizawa, K. Miyamichi, H. Takeuchi, Y. Yamagishi, M. Suzuki, and H. Sakano A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting Cell 127 2006 1057 1069
34. L. Shapiro, and W.I. Weis Structure and biochemistry of cadherins and catenins Cold Spring Harb. Perspect. Biol. 1 2009 a003053
35. C. Shelton, K.S. Kocherlakota, S. Zhuang, and S.M. Abmayr The immunoglobulin superfamily member Hbs functions redundantly with Sns in interactions between founder and fusion-competent myoblasts Development 136 2009 1159 1168
36. K. Shen, and C.I. Bargmann The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans Cell 112 2003 619 630
37. K. Shen, R.D. Fetter, and C.I. Bargmann Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1 Cell 116 2004 869 881
38. R.L. Sohn, P. Huang, G. Kawahara, M. Mitchell, J. Guyon, R. Kalluri, L.M. Kunkel, and E. Gussoni A role for nephrin, a renal protein, in vertebrate skeletal muscle cell fusion Proc. Natl. Acad. Sci. USA 106 2009 9274 9279
39. M. Sotomayor, W.A. Weihofen, R. Gaudet, and D.P. Corey Structure of a force-conveying cadherin bond essential for inner-ear mechanotransduction Nature 492 2012 128 132
40. G. Tang, L. Peng, P.R. Baldwin, D.S. Mann, W. Jiang, I. Rees, and S.J. Ludtke EMAN2: an extensible image processing suite for electron microscopy J. Struct. Biol. 157 2007 38 46
41. G. Venugopala Reddy, C. Reiter, S. Shanbhag, K.F. Fischbach, and V. Rodrigues Irregular chiasm-C-roughest, a member of the immunoglobulin superfamily, affects sense organ spacing on the Drosophila antenna by influencing the positioning of founder cells on the disc ectoderm Dev. Genes Evol. 209 1999 581 591
42. P. Verdino, D.A. Witherden, W.L. Havran, and I.A. Wilson The molecular interaction of CAR and JAML recruits the central cell signal transducer PI3K Science 329 2010 1210 1214
43. R. Verma, I. Kovari, A. Soofi, D. Nihalani, K. Patrie, and L.B. Holzman Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization J. Clin. Invest. 116 2006 1346 1359
44. S. Vishnu, A. Hertenstein, J. Betschinger, J.A. Knoblich, H. Gert de Couet, and K.-F. Fischbach The adaptor protein X11Lalpha/Dmint1 interacts with the PDZ-binding domain of the cell recognition protein Rst in Drosophila Dev. Biol. 289 2006 296 307
45. L.A. Völker, M. Petry, M. Abdelsabour-Khalaf, H. Schweizer, F. Yusuf, T. Busch, B. Schermer, T. Benzing, B. Brand-Saberi, and O. Kretz et al. Comparative analysis of Neph gene expression in mouse and chicken development Histochem. Cell Biol. 137 2012 355 366
46. N. Wanner, F. Noutsou, R. Baumeister, G. Walz, T.B. Huber, and E. Neumann-Haefelin Functional and spatial analysis of C. elegans SYG-1 and SYG-2, orthologs of the Neph/nephrin cell adhesion module directing selective synaptogenesis PLoS ONE 6 2011 e23598
47. H. Weavers, S. Prieto-Sánchez, F. Grawe, A. Garcia-López, R. Artero, M. Wilsch-Bräuninger, M. Ruiz-Gómez, H. Skaer, and B. Denholm The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm Nature 457 2009 322 326
48. K. Weiskopf, A.M. Ring, C.C.M. Ho, J.-P. Volkmer, A.M. Levin, A.K. Volkmer, E. Ozkan, N.B. Fernhoff, M. van de Rijn, I.L. Weissman, and K.C. Garcia Engineered SIRPα variants as immunotherapeutic adjuvants to anticancer antibodies Science 341 2013 88 91
49. T. Wolff, and D.F. Ready Cell death in normal and rough eye mutants of Drosophila Development 113 1991 825 839
50. M. Yamagata, J.R. Sanes, and J.A. Weiner Synaptic adhesion molecules Curr. Opin. Cell Biol. 15 2003 621 632
51. P.V. Afonine, R.W. Grosse-Kunstleve, N. Echols, J.J. Headd, N.W. Moriarty, M. Mustyakimov, T.C. Terwilliger, A. Urzhumtsev, P.H. Zwart, and P.D. Adams Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr. D Biol. Crystallogr. 68 2012 352 367
52. S. Banumathi, M. Dauter, and Z. Dauter Phasing at high resolution using Ta6Br12 cluster Acta Crystallogr. D Biol. Crystallogr. 59 2003 492 498
53. D. Borek, W. Minor, and Z. Otwinowski Measurement errors and their consequences in protein crystallography Acta Crystallogr. D Biol. Crystallogr. 59 2003 2031 2038
54. D. Borek, S.L. Ginell, M. Cymborowski, W. Minor, and Z. Otwinowski The many faces of radiation-induced changes J. Synchrotron Radiat. 14 2007 24 33
55. D. Borek, M. Cymborowski, M. Machius, W. Minor, and Z. Otwinowski Diffraction data analysis in the presence of radiation damage Acta Crystallogr. D Biol. Crystallogr. 66 2010 426 436
56. G. Bricogne, C. Vonrhein, C. Flensburg, M. Schiltz, and W. Paciorek Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0 Acta Crystallogr. D Biol. Crystallogr. 59 2003 2023 2030
57. A.T. Brunger Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2 2007 2728 2733
58. Cowtan, K. (1994). "dm": An automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 31, 34-38.
59. K. Cowtan The Buccaneer software for automated model building. 1. Tracing protein chains Acta Crystallogr. D Biol. Crystallogr. 62 2006 1002 1011
60. K. Cowtan Recent developments in classical density modification Acta Crystallogr. D Biol. Crystallogr. 66 2010 470 478
61. S. Doublié Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems Methods Mol. Biol. 363 2007 91 108
62. D.N. Garboczi, D.T. Hung, and D.C. Wiley HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides Proc. Natl. Acad. Sci. USA 89 1992 3429 3433
63. D.N. Garboczi, U. Utz, P. Ghosh, A. Seth, J. Kim, E.A. VanTienhoven, W.E. Biddison, and D.C. Wiley Assembly, specific binding, and crystallization of a human TCR-alphabeta with an antigenic Tax peptide from human T lymphotropic virus type 1 and the class I MHC molecule HLA-A2 J. Immunol. 157 1996 5403 5410
64. W. Kabsch XDS Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
65. J. Knäblein, T. Neuefeind, F. Schneider, A. Bergner, A. Messerschmidt, J. Löwe, B. Steipe, and R. Huber Ta6Br(2+)12, a tool for phase determination of large biological assemblies by X-ray crystallography J. Mol. Biol. 270 1997 1 7
66. A.A. Lebedev, A.A. Vagin, and G.N. Murshudov Model preparation in MOLREP and examples of model improvement using X-ray data Acta Crystallogr. D Biol. Crystallogr. 64 2008 33 39
67. A.J. McCoy Solving structures of protein complexes by molecular replacement with Phaser Acta Crystallogr. D Biol. Crystallogr. 63 2007 32 41
68. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
69. W. Minor, M. Cymborowski, Z. Otwinowski, and M. Chruszcz HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes Acta Crystallogr. D Biol. Crystallogr. 62 2006 859 866
70. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
71. T. Neuefeind, A. Bergner, F. Schneider, A. Messerschmidt, and J. Knablein The suitability of Ta6Br12(2+) for phasing in protein crystallography Biol. Chem. 378 1997 219 221
72. Z. Otwinowski Maximum likelihood refinement of heavy atom parameters CCP4 Study Weekend 1991 80 86
73. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode C.W. Carter Jr. R.M. Sweet, Methods in Enzymology Volume 276 1997 Academic Press New York 307 326
74. Z. Otwinowski, D. Borek, W. Majewski, and W. Minor Multiparametric scaling of diffraction intensities Acta Crystallogr. A 59 2003 228 234
75. T.R. Schneider, and G.M. Sheldrick Substructure solution with SHELXD Acta Crystallogr. D Biol. Crystallogr. 58 2002 1772 1779
76. P. Sheffield, S. Garrard, and Z. Derewenda Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors Protein Expr. Purif. 15 1999 34 39
77. G.M. Sheldrick Macromolecular phasing with SHELXE Z. Kristallogr. 217 2002 644 650
78. G.M. Sheldrick A short history of SHELX Acta Crystallogr. A 64 2008 112 122
79. G.M. Sheldrick Experimental phasing with SHELXC/D/E: combining chain tracing with density modification Acta Crystallogr. D Biol. Crystallogr. 66 2010 479 485
80. A. Vagin, and A. Teplyakov MOLREP: an Automated Program for Molecular Replacement J. Appl. Cryst. 30 1997 1022 1025
81. C. Vonrhein, E. Blanc, P. Roversi, and G. Bricogne Automated structure solution with autoSHARP Methods Mol. Biol. 364 2007 215 230
82. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G.W. Leslie, and A. McCoy et al. Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242