Molecular basis of sidekick-mediated cell-cell adhesion and specificity

Goodman, Kerry M.; Yamagata, Masahito; Jin, Xiangshu; Mannepalli, Seetha; Katsamba, Phinikoula S.; Ahlsén, Göran; Sergeeva, Alina P.; Honig, Barry; Sanes, Joshua R.; Shapiro, Lawrence

doi:10.7554/elife.19058

Title: Molecular basis of sidekick-mediated cell-cell adhesion and specificity

Journal Article · Mon Sep 19 00:00:00 EDT 2016 · eLife

DOI:https://doi.org/10.7554/elife.19058· OSTI ID:1328787

Goodman, Kerry M. ^[1];

^[2]; Jin, Xiangshu ^[1]; Mannepalli, Seetha ^[1]; Katsamba, Phinikoula S. ^[1]; Ahlsén, Göran ^[1]; Sergeeva, Alina P. ^[1];

^[1];

^[2];

^[1]

Columbia Univ., New York, NY (United States)
Harvard Univ., Cambridge, MA (United States)

Sidekick (Sdk) 1 and 2 are related immunoglobulin superfamily cell adhesion proteins required for appropriate synaptic connections between specific subtypes of retinal neurons. Sdks mediate cell-cell adhesion with homophilic specificity that underlies their neuronal targeting function. Here we report crystal structures of Sdk1 and Sdk2 ectodomain regions, revealing similar homodimers mediated by the four N-terminal immunoglobulin domains (Ig1–4), arranged in a horseshoe conformation. These Ig1–4 horseshoes interact in a novel back-to-back orientation in both homodimers through Ig1:Ig2, Ig1:Ig1 and Ig3:Ig4 interactions. Structure-guided mutagenesis results show that this canonical dimer is required for both Sdk-mediated cell aggregation (via trans interactions) and Sdk clustering in isolated cells (via cis interactions). Sdk1/Sdk2 recognition specificity is encoded across Ig1–4, with Ig1–2 conferring the majority of binding affinity and differential specificity. We suggest that competition between cis and trans interactions provides a novel mechanism to sharpen the specificity of cell-cell interactions.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH); Howard Hughes Medical Institute (HHMI); National Science Foundation (NSF)

Grant/Contract Number:: P41 GM103403; MCB-1412472; NS029169; EY022073

OSTI ID:: 1328787

Journal Information:: eLife, Vol. 5; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 24 works

Citation information provided by
Web of Science

References (78)

Neurite arborization and mosaic spacing in the mouse retina require DSCAM Fuerst, Peter G.; Koizumi, Amane; Masland, Richard H. Nature, Vol. 451, Issue 7177 https://doi.org/10.1038/nature06514	journal	January 2008
Kinetic Analysis of L1 Homophilic Interaction: ROLE OF THE FIRST FOUR IMMUNOGLOBULIN DOMAINS AND IMPLICATIONS ON BINDING MECHANISM Gouveia, Ricardo M.; Gomes, Cláudio M.; Sousa, Marcos Journal of Biological Chemistry, Vol. 283, Issue 42 https://doi.org/10.1074/jbc.M804991200	journal	August 2008
The Neuronal Organization of the Retina Masland, Richard H. Neuron, Vol. 76, Issue 2 https://doi.org/10.1016/j.neuron.2012.10.002	journal	October 2012
The crystal structure of the ligand-binding module of human TAG-1 suggests a new mode of homophilic interaction Mörtl, Mario; Sonderegger, Peter; Diederichs, Kay Protein Science, Vol. 16, Issue 10 https://doi.org/10.1110/ps.072802707	journal	October 2007
Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes Schmucker, D.; Chen, B. Genes & Development, Vol. 23, Issue 2 https://doi.org/10.1101/gad.1752909	journal	January 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Definition of the critical domains required for homophilic targeting of mouse sidekick molecules Hayashi, Kayo; Kaufman, Lewis; Ross, Michael D. The FASEB Journal, Vol. 19, Issue 6 https://doi.org/10.1096/fj.04-2947fje	journal	January 2005
Contactins: Emerging key roles in the development and function of the nervous system Shimoda, Yasushi; Watanabe, Kazutada Cell Adhesion & Migration, Vol. 3, Issue 1 https://doi.org/10.4161/cam.3.1.7764	journal	January 2009
Synaptic Localization and Function of Sidekick Recognition Molecules Require MAGI Scaffolding Proteins Yamagata, M.; Sanes, J. R. Journal of Neuroscience, Vol. 30, Issue 10 https://doi.org/10.1523/JNEUROSCI.6319-09.2010	journal	March 2010
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
A robust pipeline for rapid production of versatile nanobody repertoires Fridy, Peter C.; Li, Yinyin; Keegan, Sarah Nature Methods, Vol. 11, Issue 12 https://doi.org/10.1038/nmeth.3170	journal	November 2014
Structure and Binding Mechanism of Vascular Endothelial Cadherin: A Divergent Classical Cadherin Brasch, Julia; Harrison, Oliver J.; Ahlsen, Goran Journal of Molecular Biology, Vol. 408, Issue 1 https://doi.org/10.1016/j.jmb.2011.01.031	journal	April 2011
Crystal Structure of Hemolin: A Horseshoe Shape with Implications for Homophilic Adhesion Su, X. Science, Vol. 281, Issue 5379 https://doi.org/10.1126/science.281.5379.991	journal	August 1998
Comprehensive Classification of Retinal Bipolar Neurons by Single-Cell Transcriptomics Shekhar, Karthik; Lapan, Sylvain W.; Whitney, Irene E. Cell, Vol. 166, Issue 5 https://doi.org/10.1016/j.cell.2016.07.054	journal	August 2016
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
The Extracellular Architecture of Adherens Junctions Revealed by Crystal Structures of Type I Cadherins Harrison, Oliver J.; Jin, Xiangshu; Hong, Soonjin Structure, Vol. 19, Issue 2 https://doi.org/10.1016/j.str.2010.11.016	journal	February 2011
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
Molecular design principles underlying β-strand swapping in the adhesive dimerization of cadherins Vendome, Jeremie; Posy, Shoshana; Jin, Xiangshu Nature Structural & Molecular Biology, Vol. 18, Issue 6 https://doi.org/10.1038/nsmb.2051	journal	May 2011
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000061	journal	June 2013
Complementary Chimeric Isoforms Reveal Dscam1 Binding Specificity In Vivo Wu, Wei; Ahlsen, Goran; Baker, David Neuron, Vol. 76, Issue 3 https://doi.org/10.1016/j.neuron.2012.10.010	journal	November 2012
X-Ray Diffraction data from Mouse Sidekick-2 immunoglobulin domains 1-4 H18R/N22S mutant, source of 5K70 structure ., Goodman, Kerry M. SBGrid Data Bank https://doi.org/10.15785/sbgrid/373	dataset	January 2016
X-Ray Diffraction data from Sidekick chimera of sidekick-2 immunoglobulin domains 1-2 and sidekick-1 immunoglobulin domains 3-4, source of 5K6Z structure Goodman, Kerry M. SBGrid Data Bank https://doi.org/10.15785/sbgrid/372	dataset	January 2016
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Comparative Protein Structure Modeling Using MODELLER Webb, Benjamin; Sali, Andrej Current Protocols in Bioinformatics, Vol. 47, Issue 1 https://doi.org/10.1002/0471250953.bi0506s47	journal	September 2014
X-Ray Diffraction data from Mouse Sidekick-2 immunoglobulin domains 1-4, crystal form 2, source of 5K6Y structure ., Goodman, Kerry M. SBGrid Data Bank https://doi.org/10.15785/sbgrid/371	dataset	January 2016
X-Ray Diffraction data from Mouse Sidekick-2 immunoglobulin domains 1-4, crystal form 1, source of 5K6X structure Goodman, Kerry M. SBGrid Data Bank https://doi.org/10.15785/sbgrid/370	dataset	January 2016
Transgenic strategy for identifying synaptic connections in mice by fluorescence complementation (GRASP) Yamagata, Masahito; Sanes, Joshua R. Frontiers in Molecular Neuroscience, Vol. 5 https://doi.org/10.3389/fnmol.2012.00018	journal	January 2012
Structural basis of Dscam isoform specificity Meijers, R.; Puettmann Holgado, R.; Skiniotis, Y. Acta Crystallographica Section A Foundations of Crystallography, Vol. 62, Issue a1 https://doi.org/10.1107/s0108767306099442	journal	August 2006
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
Comparative Protein Structure Modeling Using MODELLER Webb, Benjamin; Sali, Andrej Current Protocols in Protein Science, Vol. 86, Issue 1 https://doi.org/10.1002/cpps.20	journal	November 2016
Alternative Splicing of Drosophila Dscam Generates Axon Guidance Receptors that Exhibit Isoform-Specific Homophilic Binding Wojtowicz, Woj M.; Flanagan, John J.; Millard, S. Sean Cell, Vol. 118, Issue 5 https://doi.org/10.1016/j.cell.2004.08.021	journal	September 2004
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
WebLogo: A Sequence Logo Generator Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc Genome Research, Vol. 14, Issue 6, p. 1188-1190 https://doi.org/10.1101/gr.849004	journal	May 2004
Linking molecular affinity and cellular specificity in cadherin-mediated adhesion Katsamba, P.; Carroll, K.; Ahlsen, G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 28 https://doi.org/10.1073/pnas.0905349106	journal	June 2009
DSCAM: a novel member of the immunoglobulin superfamily maps in a Down syndrome region and is involved in the development of the nervous system Yamakawa, K. Human Molecular Genetics, Vol. 7, Issue 2 https://doi.org/10.1093/hmg/7.2.227	journal	February 1998
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration Maness, Patricia F.; Schachner, Melitta Nature Neuroscience, Vol. 10, Issue 1 https://doi.org/10.1038/nn1827	journal	December 2006
X-Ray Diffraction data from Mouse Sidekick-1 immunoglobulin domains 1-5, source of 5K6W structure Goodman, Kerry M. SBGrid Data Bank https://doi.org/10.15785/sbgrid/369	dataset	January 2016
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Mechanism of nicotinic acetylcholine receptor cluster formation by rapsyn Ramarao, M. K.; Cohen, J. B. Proceedings of the National Academy of Sciences, Vol. 95, Issue 7 https://doi.org/10.1073/pnas.95.7.4007	journal	March 1998
Design Principles of Insect and Vertebrate Visual Systems Sanes, Joshua R.; Zipursky, S. Lawrence Neuron, Vol. 66, Issue 1 https://doi.org/10.1016/j.neuron.2010.01.018	journal	April 2010
The Types of Retinal Ganglion Cells: Current Status and Implications for Neuronal Classification Sanes, Joshua R.; Masland, Richard H. Annual Review of Neuroscience, Vol. 38, Issue 1 https://doi.org/10.1146/annurev-neuro-071714-034120	journal	July 2015
Structural and energetic determinants of adhesive binding specificity in type I cadherins Vendome, Jeremie; Felsovalyi, Klara; Song, Hang Proceedings of the National Academy of Sciences, Vol. 111, Issue 40 https://doi.org/10.1073/pnas.1416737111	journal	September 2014
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Specificity of cell-cell adhesion by classical cadherins: Critical role for low-affinity dimerization through -strand swapping Chen, C. P.; Posy, S.; Ben-Shaul, A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 24 https://doi.org/10.1073/pnas.0503319102	journal	June 2005
Sidekick 2 directs formation of a retinal circuit that detects differential motion Krishnaswamy, Arjun; Yamagata, Masahito; Duan, Xin Nature, Vol. 524, Issue 7566 https://doi.org/10.1038/nature14682	journal	August 2015
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
COBALT: constraint-based alignment tool for multiple protein sequences Papadopoulos, J. S.; Agarwala, R. Bioinformatics, Vol. 23, Issue 9 https://doi.org/10.1093/bioinformatics/btm076	journal	March 2007
The Crystal Structure of the Ligand Binding Module of Axonin-1/TAG-1 Suggests a Zipper Mechanism for Neural Cell Adhesion Freigang, Jörg; Proba, Karl; Leder, Lukas Cell, Vol. 101, Issue 4 https://doi.org/10.1016/S0092-8674(00)80852-1	journal	May 2000
Complementary Chimeric Isoforms Reveal Dscam1 Binding Specificity In Vivo Wu, Wei; Ahlsen, Goran; Baker, David Neuron, Vol. 74, Issue 2 https://doi.org/10.1016/j.neuron.2012.02.029	journal	April 2012
Classical electrostatics in biology and chemistry Honig, B.; Nicholls, A. Science, Vol. 268, Issue 5214 https://doi.org/10.1126/science.7761829	journal	May 1995
DSCAM, a Highly Conserved Gene in Mammals, Expressed in Differentiating Mouse Brain Agarwala, Kishan Lal; Ganesh, Subramaniam; Amano, Kenji Biochemical and Biophysical Research Communications, Vol. 281, Issue 3 https://doi.org/10.1006/bbrc.2001.4420	journal	March 2001
Homophilic Adhesion Mechanism of Neurofascin, a Member of the L1 Family of Neural Cell Adhesion Molecules Liu, Heli; Focia, Pamela J.; He, Xiaolin Journal of Biological Chemistry, Vol. 286, Issue 1 https://doi.org/10.1074/jbc.M110.180281	journal	November 2010
Structural basis of Dscam isoform specificity Meijers, Rob; Puettmann-Holgado, Roland; Skiniotis, Georgios Nature, Vol. 449, Issue 7161 https://doi.org/10.1038/nature06147	journal	August 2007
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Neural circuit formation in the cerebellum is controlled by cell adhesion molecules of the Contactin family Stoeckli, Esther T. Cell Adhesion & Migration, Vol. 4, Issue 4 https://doi.org/10.4161/cam.4.4.12733	journal	October 2010
Up-regulation of the Homophilic Adhesion Molecule Sidekick-1 in Podocytes Contributes to Glomerulosclerosis Kaufman, Lewis; Potla, Uma; Coleman, Sarah Journal of Biological Chemistry, Vol. 285, Issue 33 https://doi.org/10.1074/jbc.M110.133959	journal	June 2010
Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina Yamagata, Masahito; Sanes, Joshua R. Nature, Vol. 451, Issue 7177 https://doi.org/10.1038/nature06469	journal	January 2008
N-terminal horseshoe conformation of DCC is functionally required for axon guidance and might be shared by other neural receptors Chen, Qiang; Sun, Xiaqin; Zhou, Xiao-hong Journal of Cell Science, Vol. 126, Issue 1 https://doi.org/10.1242/jcs.111278	journal	October 2012
A Vast Repertoire of Dscam Binding Specificities Arises from Modular Interactions of Variable Ig Domains Wojtowicz, Woj M.; Wu, Wei; Andre, Ingemar Cell, Vol. 130, Issue 6 https://doi.org/10.1016/j.cell.2007.08.026	journal	September 2007
A split horseradish peroxidase for the detection of intercellular protein–protein interactions and sensitive visualization of synapses Martell, Jeffrey D.; Yamagata, Masahito; Deerinck, Thomas J. Nature Biotechnology, Vol. 34, Issue 7 https://doi.org/10.1038/nbt.3563	journal	May 2016
Vertical interactions across ten parallel, stacked representations in the mammalian retina Roska, Botond; Werblin, Frank Nature, Vol. 410, Issue 6828 https://doi.org/10.1038/35069068	journal	March 2001
The homophilic adhesion molecule sidekick‐1 contributes to augmented podocyte aggregation in HIV‐associated nephropathy Kaufman, Lewis; Yang, Guozhe; Hayashi, Kayo The FASEB Journal, Vol. 21, Issue 7 https://doi.org/10.1096/fj.06-7191com	journal	January 2007
Sidekicks Yamagata, Masahito; Weiner, Joshua A.; Sanes, Joshua R. Cell, Vol. 110, Issue 5 https://doi.org/10.1016/S0092-8674(02)00910-8	journal	September 2002
The protein tyrosine phosphatases PTPRZ and PTPRG bind to distinct members of the contactin family of neural recognition molecules Bouyain, S.; Watkins, D. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 6 https://doi.org/10.1073/pnas.0911235107	journal	January 2010
A Double S Shape Provides the Structural Basis for the Extraordinary Binding Specificity of Dscam Isoforms Sawaya, Michael R.; Wojtowicz, Woj M.; Andre, Ingemar Cell, Vol. 134, Issue 6 https://doi.org/10.1016/j.cell.2008.07.042	journal	September 2008
Mechanism of pore opening in the calcium-activated chloride channel TMEM16A Lam, Andy K. M.; Dutzler, Raimund Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20788-8	journal	February 2021
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
DSCAM and DSCAML1 Function in Self-Avoidance in Multiple Cell Types in the Developing Mouse Retina Fuerst, Peter G.; Bruce, Freyja; Tian, Miao Neuron, Vol. 64, Issue 4 https://doi.org/10.1016/j.neuron.2009.09.027	journal	November 2009
The sidekick gene, a member of the immunoglobulin superfamily, is required for pattern formation in the Drosophila eye Nguyen, D. N.; Liu, Y.; Litsky, M. L. Development, Vol. 124, Issue 17 https://doi.org/10.1242/dev.124.17.3303	journal	September 1997
Critical and optimal Ig domains for promotion of neurite outgrowth by L1/Ng-CAM Haspel, Jeffrey; Friedlander, David R.; Ivgy-May, Neely Journal of Neurobiology, Vol. 42, Issue 3 https://doi.org/10.1002/(sici)1097-4695(20000215)42:3<287::aid-neu1>3.0.co;2-x	journal	February 2000
The effect of acidic pH on the adsorption and lytic activity of the peptides Polybia-MP1 and its histidine-containing analog in anionic lipid membrane: a biophysical study by molecular dynamics and spectroscopy Martins, Ingrid Bernardes Santana; Viegas, Taisa Giordano; dos Santos Alvares, Dayane Amino Acids, Vol. 53, Issue 5 https://doi.org/10.1007/s00726-021-02982-0	journal	April 2021
Receptor binding and priming of the spike protein of SARS-CoV-2 for membrane fusion Benton, Donald J.; Wrobel, Antoni G.; Xu, Pengqi Nature, Vol. 588, Issue 7837 https://doi.org/10.1038/s41586-020-2772-0	journal	September 2020
Sidekick-1 Is Upregulated in Glomeruli in HIV-Associated Nephropathy Kaufman, L. Journal of the American Society of Nephrology, Vol. 15, Issue 7 https://doi.org/10.1097/01.asn.0000128975.28958.c2	journal	July 2004
Expanding the Ig Superfamily Code for Laminar Specificity in Retina: Expression and Role of Contactins Yamagata, M.; Sanes, J. R. Journal of Neuroscience, Vol. 32, Issue 41 https://doi.org/10.1523/jneurosci.3193-12.2012	journal	October 2012
The crystal structure of the ligand binding module of axonin-1/TAG-1 suggests a zipper mechanism for neural cell adhesion. J., Freigang,; K., Proba,; L., Leder, Elsevier https://doi.org/10.5167/uzh-1084	text	January 2000

Cited By (6)

Architecture of cell–cell adhesion mediated by sidekicks Tang, Hua; Chang, Haishuang; Dong, Yue Proceedings of the National Academy of Sciences, Vol. 115, Issue 37 https://doi.org/10.1073/pnas.1801810115	journal	August 2018
The tricellular vertex-specific adhesion molecule Sidekick facilitates polarised cell intercalation during Drosophila axis extension Finegan, Tara M.; Hervieux, Nathan; Nestor-Bergmann, Alexander bioRxiv https://doi.org/10.1101/704932	posted_content	July 2019
The tricellular vertex-specific adhesion molecule Sidekick facilitates polarised cell intercalation during Drosophila axis extension Finegan, Tara M.; Hervieux, Nathan; Nestor-Bergmann, Alexander PLOS Biology, Vol. 17, Issue 12 https://doi.org/10.1371/journal.pbio.3000522	journal	December 2019
The tricellular vertex-specific adhesion molecule Sidekick facilitates polarised cell intercalation during Drosophila axis extension. Finegan, Tara M.; Hervieux, Nathan; Nestor-Bergmann, Alexander Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45853	text	January 2019
The tricellular vertex-specific adhesion molecule Sidekick facilitates polarised cell intercalation during Drosophila axis extension. Finegan, Tara M.; Hervieux, Nathan; Nestor-Bergmann, Alexander Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.47556	text	January 2019
Drosophila Sidekick is required in developing photoreceptors to enable visual motion detection Astigarraga, Sergio; Douthit, Jessica; Tarnogorska, Dorota Development, Vol. 145, Issue 3 https://doi.org/10.1242/dev.158246	journal	January 2018

Similar Records

Designer molecules of the synaptic organizer MDGA1 reveal 3D conformational control of biological function

Journal Article · Tue Mar 07 00:00:00 EST 2023 · Journal of Biological Chemistry · OSTI ID:1328787

Lee, Hubert; Chofflet, Nicolas; Liu, Jianfang; +10 more

Homophilic Adhesion Mechanism of Neurofascin, a Member of the L1 Family of Neural Cell Adhesion Molecules

Journal Article · Mon Feb 13 00:00:00 EST 2012 · J. Biol. Chem. · OSTI ID:1328787

Liu, Heli; Focia, Pamela J; He, Xiaolin

Visualization of clustered protocadherin neuronal self-recognition complexes

Journal Article · Wed Apr 10 00:00:00 EDT 2019 · Nature (London) · OSTI ID:1328787

Brasch, Julia; Goodman, Kerry M.; Noble, Alex J.; +11 more

Related Subjects

36 MATERIALS SCIENCE
59 BASIC BIOLOGICAL SCIENCES

Title: Molecular basis of sidekick-mediated cell-cell adhesion and specificity

Citation Formats

References (78)

Cited By (6)

Similar Records

Related Subjects