Structural basis for adhesion G protein-coupled receptor Gpr126 function

Leon, Katherine; Cunningham, Rebecca L.; Riback, Joshua A.; Feldman, Ezra; Li, Jingxian; Sosnick, Tobin R.; Zhao, Minglei; Monk, Kelly R.; Araç, Demet

doi:10.1038/s41467-019-14040-1

Title: Structural basis for adhesion G protein-coupled receptor Gpr126 function

Journal Article · Fri Jan 10 00:00:00 EST 2020 · Nature Communications

DOI:https://doi.org/10.1038/s41467-019-14040-1· OSTI ID:1591910

Leon, Katherine ^[1]; Cunningham, Rebecca L. ^[2]; Riback, Joshua A. ^[1]; Feldman, Ezra ^[1]; Li, Jingxian ^[1]; Sosnick, Tobin R. ^[1]; Zhao, Minglei ^[1]; Monk, Kelly R. ^[3];

^[1]

Univ. of Chicago, IL (United States)
Washington Univ. School of Medicine, St. Louis, MO (United States)
Washington Univ. School of Medicine, St. Louis, MO (United States); Oregon Health & Science Univ., Portland, OR (United States)

Many drugs target the extracellular regions (ECRs) of cell-surface receptors. The large and alternatively-spliced ECRs of adhesion G protein-coupled receptors (aGPCRs) have key functions in diverse biological processes including neurodevelopment, embryogenesis, and tumorigenesis. However, their structures and mechanisms of action remain unclear, hampering drug development. The aGPCR Gpr126/Adgrg6 regulates Schwann cell myelination, ear canal formation, and heart development; and GPR126 mutations cause myelination defects in human. Here, we determine the structure of the complete zebrafish Gpr126 ECR and reveal five domains including a previously unknown domain. Strikingly, the Gpr126 ECR adopts a closed conformation that is stabilized by an alternatively spliced linker and a conserved calcium-binding site. Alternative splicing regulates ECR conformation and receptor signaling, while mutagenesis of the calcium-binding site abolishes Gpr126 function in vivo. These results demonstrate that Gpr126 ECR utilizes a multi-faceted dynamic approach to regulate receptor function and provide relevant insights for ECR-targeted drug design.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH); National Science Foundation Graduate Research Fellowship

Grant/Contract Number:: AC02-06CH11357; 9 P41 GM103622-18; R01-GM120322; R01-NS079445; T32GM007183; DGE-1745038

OSTI ID:: 1591910

Journal Information:: Nature Communications, Vol. 11, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 31 works

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References (101)

A Tethered Agonist within the Ectodomain Activates the Adhesion G Protein-Coupled Receptors GPR126 and GPR133 Liebscher, Ines; Schön, Julia; Petersen, Sarah C. Cell Reports, Vol. 9, Issue 6 https://doi.org/10.1016/j.celrep.2014.11.036	journal	December 2014
Adhesion G protein-coupled receptors are activated by exposure of a cryptic tethered agonist Stoveken, Hannah M.; Hajduczok, Alexander G.; Xu, Lei Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1421785112	journal	April 2015
Gpr126 Functions in Schwann Cells to Control Differentiation and Myelination via G-Protein Activation Mogha, A.; Benesh, A. E.; Patra, C. Journal of Neuroscience, Vol. 33, Issue 46 https://doi.org/10.1523/JNEUROSCI.1809-13.2013	journal	November 2013
SEA Domain Autoproteolysis Accelerated by Conformational Strain: Energetic Aspects Sandberg, Anders; Johansson, Denny G. A.; Macao, Bertil Journal of Molecular Biology, Vol. 377, Issue 4 https://doi.org/10.1016/j.jmb.2008.01.051	journal	April 2008
erbb3 and erbb2 Are Essential for Schwann Cell Migration and Myelination in Zebrafish Lyons, David A.; Pogoda, Hans-Martin; Voas, Matthew G. Current Biology, Vol. 15, Issue 6, p. 513-524 https://doi.org/10.1016/j.cub.2005.02.030	journal	March 2005
Structural Basis of Latrophilin-FLRT Interaction Jackson, Verity A.; del Toro, Daniel; Carrasquero, Maria Structure, Vol. 23, Issue 4 https://doi.org/10.1016/j.str.2015.01.013	journal	April 2015
A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis: Cell-adhesion GPCRs mediates autoproteolysis Araç, Demet; Boucard, Antony A.; Bolliger, Marc F. The EMBO Journal, Vol. 31, Issue 6 https://doi.org/10.1038/emboj.2012.26	journal	February 2012
Stalk-dependent and Stalk-independent Signaling by the Adhesion G Protein-coupled Receptors GPR56 (ADGRG1) and BAI1 (ADGRB1) Kishore, Ayush; Purcell, Ryan H.; Nassiri-Toosi, Zahra Journal of Biological Chemistry, Vol. 291, Issue 7 https://doi.org/10.1074/jbc.M115.689349	journal	December 2015
The Adhesion GPCR GPR126 Has Distinct, Domain-Dependent Functions in Schwann Cell Development Mediated by Interaction with Laminin-211 Petersen, Sarah C.; Luo, Rong; Liebscher, Ines Neuron, Vol. 85, Issue 4 https://doi.org/10.1016/j.neuron.2014.12.057	journal	February 2015
Structural Basis for Teneurin Function in Circuit-Wiring: A Toxin Motif at the Synapse Li, Jingxian; Shalev-Benami, Moran; Sando, Richard Cell, Vol. 173, Issue 3 https://doi.org/10.1016/j.cell.2018.03.036	journal	April 2018
Extracellular fragment of brain-specific angiogenesis inhibitor 1 suppresses endothelial cell proliferation by blocking αvβ5 integrin Koh, Jeong Tae; Kook, Hyun; Kee, Hae Jin Experimental Cell Research, Vol. 294, Issue 1 https://doi.org/10.1016/j.yexcr.2003.11.008	journal	March 2004
The constitutive activity of the adhesion GPCR GPR114/ADGRG5 is mediated by its tethered agonist Wilde, Caroline; Fischer, Liane; Lede, Vera The FASEB Journal, Vol. 30, Issue 2 https://doi.org/10.1096/fj.15-276220	journal	February 2016
The prion protein is an agonistic ligand of the G protein-coupled receptor Adgrg6 Küffer, Alexander; Lakkaraju, Asvin K. K.; Mogha, Amit Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19312	journal	August 2016
High Prevalence of a Hotspot of Noncoding Somatic Mutations in Intron 6 of GPR126 in Bladder Cancer Garinet, Simon; Pignot, Géraldine; Vacher, Sophie Molecular Cancer Research, Vol. 17, Issue 2 https://doi.org/10.1158/1541-7786.MCR-18-0363	journal	February 2019
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	journal	April 2016
Super-complexes of adhesion GPCRs and neural guidance receptors Jackson, Verity A.; Mehmood, Shahid; Chavent, Matthieu Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11184	journal	April 2016
Mechanisms of Disease: inherited demyelinating neuropathies—from basic to clinical research Nave, Klaus-Armin; Sereda, Michael W.; Ehrenreich, Hannelore Nature Clinical Practice Neurology, Vol. 3, Issue 8 https://doi.org/10.1038/ncpneuro0583	journal	August 2007
Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin Macao, Bertil; Johansson, Denny G. A.; Hansson, Gunnar C. Nature Structural & Molecular Biology, Vol. 13, Issue 1 https://doi.org/10.1038/nsmb1035	journal	December 2005
Single-Cell mRNA Profiling Reveals Cell-Type-Specific Expression of Neurexin Isoforms Fuccillo, Marc V.; Földy, Csaba; Gökce, Özgün Neuron, Vol. 87, Issue 2 https://doi.org/10.1016/j.neuron.2015.06.028	journal	July 2015
Integrin bi-directional signaling across the plasma membrane Hu, Ping; Luo, Bing-Hao Journal of Cellular Physiology, Vol. 228, Issue 2 https://doi.org/10.1002/jcp.24154	journal	October 2012
A G Protein-Coupled Receptor Is Essential for Schwann Cells to Initiate Myelination Monk, K. R.; Naylor, S. G.; Glenn, T. D. Science, Vol. 325, Issue 5946 https://doi.org/10.1126/science.1173474	journal	September 2009
Genetic variants in GPR126 are associated with adolescent idiopathic scoliosis Kou, Ikuyo; Takahashi, Yohei; Johnson, Todd A. Nature Genetics, Vol. 45, Issue 6 https://doi.org/10.1038/ng.2639	journal	May 2013
VIGR - a novel inducible adhesion family G-protein coupled receptor in endothelial cells Stehlik, Christian; Kroismayr, Renate; Dorfleutner, Andrea FEBS Letters, Vol. 569, Issue 1-3 https://doi.org/10.1016/j.febslet.2004.05.038	journal	June 2004
Charcot-Marie-Tooth disease: Emerging mechanisms and therapies d’Ydewalle, Constantin; Benoy, Veronick; Van Den Bosch, Ludo The International Journal of Biochemistry & Cell Biology, Vol. 44, Issue 8 https://doi.org/10.1016/j.biocel.2012.04.020	journal	August 2012
Semicircular canal morphogenesis in the zebrafish inner ear requires the function of gpr126 (lauscher), an adhesion class G protein-coupled receptor gene Geng, F. -S.; Abbas, L.; Baxendale, S. Development, Vol. 140, Issue 21 https://doi.org/10.1242/dev.098061	journal	September 2013
A Highly Conserved Program of Neuronal Microexons Is Misregulated in Autistic Brains Irimia, Manuel; Weatheritt, Robert J.; Ellis, Jonathan D. Cell, Vol. 159, Issue 7 https://doi.org/10.1016/j.cell.2014.11.035	journal	December 2014
Structural basis for receptor recognition by Lujo virus Cohen-Dvashi, Hadas; Kilimnik, Itay; Diskin, Ron Nature Microbiology, Vol. 3, Issue 10 https://doi.org/10.1038/s41564-018-0224-5	journal	August 2018
Stachel -independent modulation of GPR56/ADGRG1 signaling by synthetic ligands directed to its extracellular region Salzman, Gabriel S.; Zhang, Shu; Gupta, Ankit Proceedings of the National Academy of Sciences, Vol. 114, Issue 38 https://doi.org/10.1073/pnas.1708810114	journal	September 2017
Pharmacologic Characterization of AMG 334, a Potent and Selective Human Monoclonal Antibody against the Calcitonin Gene-Related Peptide Receptor Shi, L.; Lehto, S. G.; Zhu, D. X. D. Journal of Pharmacology and Experimental Therapeutics, Vol. 356, Issue 1 https://doi.org/10.1124/jpet.115.227793	journal	November 2015
Oriented Cell Division in the C. elegans Embryo Is Coordinated by G-Protein Signaling Dependent on the Adhesion GPCR LAT-1 Müller, Antje; Winkler, Jana; Fiedler, Franziska PLOS Genetics, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pgen.1005624	journal	October 2015
Structural Basis of Latrophilin-FLRT-UNC5 Interaction in Cell Adhesion Lu, Yue C.; Nazarko, Olha V.; Sando, Richard Structure, Vol. 23, Issue 9 https://doi.org/10.1016/j.str.2015.06.024	journal	September 2015
Structure of the Extracellular Region of HER3 Reveals an Interdomain Tether Cho, H. -S. Science, Vol. 297, Issue 5585 https://doi.org/10.1126/science.1074611	journal	August 2002
Orphan receptor GPR110, an oncogene overexpressed in lung and prostate cancer Lum, Amy M.; Wang, Bruce B.; Beck-Engeser, Gabriele B. BMC Cancer, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2407-10-40	journal	February 2010
The GPS Motif Is a Molecular Switch for Bimodal Activities of Adhesion Class G Protein-Coupled Receptors Prömel, Simone; Frickenhaus, Marie; Hughes, Samantha Cell Reports, Vol. 2, Issue 2 https://doi.org/10.1016/j.celrep.2012.06.015	journal	August 2012
Structural basis of the C1q/C1s interaction and its central role in assembly of the C1 complex of complement activation Venkatraman Girija, Umakhanth; Gingras, Alexandre R.; Marshall, Jamie E. Proceedings of the National Academy of Sciences, Vol. 110, Issue 34 https://doi.org/10.1073/pnas.1311113110	journal	August 2013
Gpr124 Controls CNS Angiogenesis and Blood-Brain Barrier Integrity by Promoting Ligand-Specific Canonical Wnt Signaling Zhou, Yulian; Nathans, Jeremy Developmental Cell, Vol. 31, Issue 2 https://doi.org/10.1016/j.devcel.2014.08.018	journal	October 2014
Adhesion-GPCRs: emerging roles for novel receptors Yona, Simon; Lin, Hsi-Hsien; Siu, Willie O. Trends in Biochemical Sciences, Vol. 33, Issue 10 https://doi.org/10.1016/j.tibs.2008.07.005	journal	October 2008
Identification of the tethered peptide agonist of the adhesion G protein-coupled receptor GPR64/ADGRG2 Demberg, Lilian M.; Rothemund, Sven; Schöneberg, Torsten Biochemical and Biophysical Research Communications, Vol. 464, Issue 3 https://doi.org/10.1016/j.bbrc.2015.07.020	journal	August 2015
Structural Basis of Mannan-Binding Lectin Recognition by Its Associated Serine Protease MASP-1: Implications for Complement Activation Gingras, Alexandre R.; Girija, Umakhanth Venkatraman; Keeble, Anthony H. Structure, Vol. 19, Issue 11 https://doi.org/10.1016/j.str.2011.08.014	journal	November 2011
The N Terminus of the Adhesion G Protein-coupled Receptor GPR56 Controls Receptor Signaling Activity Paavola, Kevin J.; Stephenson, Jason R.; Ritter, Stefanie L. Journal of Biological Chemistry, Vol. 286, Issue 33 https://doi.org/10.1074/jbc.M111.247973	journal	June 2011
Disease-associated extracellular loop mutations in the adhesion G protein-coupled receptor G1 (ADGRG1; GPR56) differentially regulate downstream signaling Kishore, Ayush; Hall, Randy A. Journal of Biological Chemistry, Vol. 292, Issue 23 https://doi.org/10.1074/jbc.M117.780551	journal	April 2017
Effects of S1 Cleavage on the Structure, Surface Export, and Signaling Activity of Human Notch1 and Notch2 Gordon, Wendy R.; Vardar-Ulu, Didem; L'Heureux, Sarah PLoS ONE, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pone.0006613	journal	August 2009
International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G Protein–Coupled Receptors Hamann, Jörg; Aust, Gabriela; Araç, Demet Pharmacological Reviews, Vol. 67, Issue 2 https://doi.org/10.1124/pr.114.009647	journal	February 2015
Identification of coding and non-coding mutational hotspots in cancer genomes Piraino, Scott W.; Furney, Simon J. BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-016-3420-9	journal	January 2017
Structural basis for receptor recognition of vitamin-B12–intrinsic factor complexes Andersen, Christian Brix Folsted; Madsen, Mette; Storm, Tina Nature, Vol. 464, Issue 7287 https://doi.org/10.1038/nature08874	journal	March 2010
Reck and Gpr124 Are Essential Receptor Cofactors for Wnt7a/Wnt7b-Specific Signaling in Mammalian CNS Angiogenesis and Blood-Brain Barrier Regulation Cho, Chris; Smallwood, Philip M.; Nathans, Jeremy Neuron, Vol. 95, Issue 5 https://doi.org/10.1016/j.neuron.2017.07.031	journal	August 2017
Structure and ligand recognition of class C GPCRs Chun, Lei; Zhang, Wen-hua; Liu, Jian-feng Acta Pharmacologica Sinica, Vol. 33, Issue 3 https://doi.org/10.1038/aps.2011.186	journal	January 2012
A molecular mechanism for Wnt ligand-specific signaling Eubelen, Marie; Bostaille, Naguissa; Cabochette, Pauline Science, Vol. 361, Issue 6403 https://doi.org/10.1126/science.aat1178	journal	July 2018
A RECK-WNT7 Receptor-Ligand Interaction Enables Isoform-Specific Regulation of Wnt Bioavailability Vallon, Mario; Yuki, Kanako; Nguyen, Thi D. Cell Reports, Vol. 25, Issue 2 https://doi.org/10.1016/j.celrep.2018.09.045	journal	October 2018
Structural Basis for G Protein-Coupled Receptor Activation Manglik, Aashish; Kruse, Andrew C. Biochemistry, Vol. 56, Issue 42 https://doi.org/10.1021/acs.biochem.7b00747	journal	September 2017
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
Therapeutic antagonists and conformational regulation of integrin function Shimaoka, Motomu; Springer, Timothy A. Nature Reviews Drug Discovery, Vol. 2, Issue 9 https://doi.org/10.1038/nrd1174	journal	September 2003
The Adhesion-GPCR BAI1 Promotes Excitatory Synaptogenesis by Coordinating Bidirectional Trans-synaptic Signaling Tu, Yen-Kuei; Duman, Joseph G.; Tolias, Kimberley F. The Journal of Neuroscience, Vol. 38, Issue 39 https://doi.org/10.1523/JNEUROSCI.3461-17.2018	journal	August 2018
Unfolding dynamics of the mucin SEA domain probed by force spectroscopy suggest that it acts as a cell-protective device Pelaseyed, Thaher; Zäch, Michael; Petersson, Åsa C. FEBS Journal, Vol. 280, Issue 6 https://doi.org/10.1111/febs.12144	journal	February 2013
Organ-specific function of adhesion G protein-coupled receptor GPR126 is domain-dependent Patra, C.; van Amerongen, M. J.; Ghosh, S. Proceedings of the National Academy of Sciences, Vol. 110, Issue 42 https://doi.org/10.1073/pnas.1304837110	journal	September 2013
Landscape of somatic mutations in 560 breast cancer whole-genome sequences Nik-Zainal, Serena; Davies, Helen; Staaf, Johan Nature, Vol. 534, Issue 7605 https://doi.org/10.1038/nature17676	journal	May 2016
Adhesion G Protein-Coupled Receptors: Signaling, Pharmacology, and Mechanisms of Activation Paavola, Kevin J.; Hall, Randy A. Molecular Pharmacology, Vol. 82, Issue 5 https://doi.org/10.1124/mol.112.080309	journal	July 2012
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
A Structural Perspective on the Regulation of the Epidermal Growth Factor Receptor Kovacs, Erika; Zorn, Julie Anne; Huang, Yongjian Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-034402	journal	June 2015
Mutations of GPR126 Are Responsible for Severe Arthrogryposis Multiplex Congenita Ravenscroft, Gianina; Nolent, Flora; Rajagopalan, Sulekha The American Journal of Human Genetics, Vol. 96, Issue 6 https://doi.org/10.1016/j.ajhg.2015.04.014	journal	June 2015
Extending the Structural View of Class B GPCRs de Graaf, Chris; Song, Gaojie; Cao, Can Trends in Biochemical Sciences, Vol. 42, Issue 12 https://doi.org/10.1016/j.tibs.2017.10.003	journal	December 2017
Sticky Signaling--Adhesion Class G Protein-Coupled Receptors Take the Stage Langenhan, T.; Aust, G.; Hamann, J. Science Signaling, Vol. 6, Issue 276 https://doi.org/10.1126/scisignal.2003825	journal	May 2013
Presynaptic Neurexin-3 Alternative Splicing trans-Synaptically Controls Postsynaptic AMPA Receptor Trafficking Aoto, Jason; Martinelli, David C.; Malenka, Robert C. Cell, Vol. 154, Issue 1 https://doi.org/10.1016/j.cell.2013.05.060	journal	July 2013
Structural basis for inhibition of the epidermal growth factor receptor by cetuximab Li, Shiqing; Schmitz, Karl R.; Jeffrey, Philip D. Cancer Cell, Vol. 7, Issue 4 https://doi.org/10.1016/j.ccr.2005.03.003	journal	April 2005
Integrin-based therapeutics: biological basis, clinical use and new drugs Ley, Klaus; Rivera-Nieves, Jesus; Sandborn, William J. Nature Reviews Drug Discovery, Vol. 15, Issue 3 https://doi.org/10.1038/nrd.2015.10	journal	January 2016
Identification of novel splice variants of Adhesion G protein-coupled receptors Bjarnadóttir, Thóra K.; Geirardsdóttir, Kristín; Ingemansson, Malena Gene, Vol. 387, Issue 1-2 https://doi.org/10.1016/j.gene.2006.07.039	journal	January 2007
Type IV collagen is an activating ligand for the adhesion G protein-coupled receptor GPR126 Paavola, K. J.; Sidik, H.; Zuchero, J. B. Science Signaling, Vol. 7, Issue 338 https://doi.org/10.1126/scisignal.2005347	journal	August 2014
Integrin-mediated mechanotransduction Sun, Zhiqi; Guo, Shengzhen S.; Fässler, Reinhard The Journal of Cell Biology, Vol. 215, Issue 4 https://doi.org/10.1083/jcb.201609037	journal	November 2016
Molecular mechanisms regulating myelination in the peripheral nervous system Pereira, Jorge A.; Lebrun-Julien, Frédéric; Suter, Ueli Trends in Neurosciences, Vol. 35, Issue 2 https://doi.org/10.1016/j.tins.2011.11.006	journal	February 2012
Structural Basis for Regulation of GPR56/ADGRG1 by Its Alternatively Spliced Extracellular Domains Salzman, Gabriel S.; Ackerman, Sarah D.; Ding, Chen Neuron, Vol. 91, Issue 6 https://doi.org/10.1016/j.neuron.2016.08.022	journal	September 2016
Structural basis for autoinhibition of Notch Gordon, Wendy R.; Vardar-Ulu, Didem; Histen, Gavin Nature Structural & Molecular Biology, Vol. 14, Issue 4 https://doi.org/10.1038/nsmb1227	journal	April 2007
The Orphan Adhesion-GPCR GPR126 Is Required for Embryonic Development in the Mouse Waller-Evans, Helen; Prömel, Simone; Langenhan, Tobias PLoS ONE, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pone.0014047	journal	November 2010
Insights into MHC Class I Peptide Loading from the Structure of the Tapasin-ERp57 Thiol Oxidoreductase Heterodimer Dong, Gang; Wearsch, Pamela A.; Peaper, David R. Immunity, Vol. 30, Issue 1 https://doi.org/10.1016/j.immuni.2008.10.018	journal	January 2009
Structural insights into the role of the Smoothened cysteine-rich domain in Hedgehog signalling Rana, Rajashree; Carroll, Candace E.; Lee, Ho-Jin Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3965	journal	December 2013
Transmembrane Mucins: Signaling Receptors at the Intersection of Inflammation and Cancer van Putten, Jos P. M.; Strijbis, Karin Journal of Innate Immunity, Vol. 9, Issue 3 https://doi.org/10.1159/000453594	journal	January 2017
Efficient genome editing in zebrafish using a CRISPR-Cas system Hwang, Woong Y.; Fu, Yanfang; Reyon, Deepak Nature Biotechnology, Vol. 31, Issue 3, p. 227-229 https://doi.org/10.1038/nbt.2501	journal	January 2013
ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules Ashkenazy, Haim; Abadi, Shiran; Martz, Eric Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw408	journal	May 2016
Structural Basis of Integrin Regulation and Signaling Luo, Bing-Hao; Carman, Christopher V.; Springer, Timothy A. Annual Review of Immunology, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.immunol.25.022106.141618	journal	April 2007
Heritability and genome-wide association study of diffusing capacity of the lung Terzikhan, Natalie; Sun, Fangui; Verhamme, Fien M. European Respiratory Journal, Vol. 52, Issue 3 https://doi.org/10.1183/13993003.00647-2018	journal	July 2018
DREG, a developmentally regulated G protein-coupled receptor containing two conserved proteolytic cleavage sites Moriguchi, Tetsuo; Haraguchi, Keiko; Ueda, Naoko Genes to Cells, Vol. 9, Issue 6 https://doi.org/10.1111/j.1356-9597.2004.00743.x	journal	June 2004
Alternative Splicing of P/Q-Type Ca 2+ Channels Shapes Presynaptic Plasticity Thalhammer, Agnes; Contestabile, Andrea; Ermolyuk, Yaroslav S. Cell Reports, Vol. 20, Issue 2 https://doi.org/10.1016/j.celrep.2017.06.055	journal	July 2017
Genetic Variant of GPR126 Gene is Functionally Associated With Adolescent Idiopathic Scoliosis in Chinese Population Qin, Xiaodong; Xu, Leilei; Xia, Chao SPINE, Vol. 42, Issue 19 https://doi.org/10.1097/BRS.0000000000002123	journal	January 2017
Gpr126 is essential for peripheral nerve development and myelination in mammals Monk, K. R.; Oshima, K.; Jors, S. Development, Vol. 138, Issue 13 https://doi.org/10.1242/dev.062224	journal	May 2011
Adhesion G protein-coupled receptors in nervous system development and disease Langenhan, Tobias; Piao, Xianhua; Monk, Kelly R. Nature Reviews Neuroscience, Vol. 17, Issue 9 https://doi.org/10.1038/nrn.2016.86	journal	July 2016
The GPS Motif Is a Molecular Switch for Bimodal Activities of Adhesion Class G Protein-Coupled Receptors Prömel, Simone; Frickenhaus, Marie; Hughes, Samantha Cell Reports, Vol. 2, Issue 3 https://doi.org/10.1016/j.celrep.2012.09.012	journal	September 2012
Reck and Gpr124 Are Essential Receptor Cofactors for Wnt7a/Wnt7b-Specific Signaling in Mammalian CNS Angiogenesis and Blood-Brain Barrier Regulation Cho, Chris; Smallwood, Philip M.; Nathans, Jeremy Neuron, Vol. 95, Issue 5 https://doi.org/10.1016/j.neuron.2017.08.032	journal	August 2017
Structural Basis of Latrophilin-FLRT-UNC5 Interaction in Cell Adhesion Lu, Yue C.; Nazarko, Olha V.; Sando, Richard Structure, Vol. 24, Issue 2 https://doi.org/10.1016/j.str.2016.01.006	journal	February 2016
Preclinical Development of a Fusion Peptide Conjugate as an HIV Vaccine Immunogen Ou, Li; Kong, Wing-Pui; Chuang, Gwo-Yu Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-59711-y	journal	February 2020
Heritability and genome-wide association study of diffusing capacity of the lung (DLCO) Terzikhan, Natalie; Sun, Fanfgui; Verhamme, Fien ERS International Congress 2018 abstracts, Genes and environment https://doi.org/10.1183/13993003.congress-2018.oa2189	conference	November 2018
FDA approves licensing of erenumab-aooe to prevent migraine Traynor, Kate American Journal of Health-System Pharmacy, Vol. 75, Issue 13 https://doi.org/10.2146/news180044	journal	July 2018
Visualizing Proteins and Macromolecular Complexes by Negative Stain EM: from Grid Preparation to Image Acquisition Booth, David S.; Avila-Sakar, Agustin; Cheng, Yifan Journal of Visualized Experiments, Issue 58 https://doi.org/10.3791/3227	journal	January 2011
The prion protein is an agonistic ligand of the G protein-coupled receptor Adgrg6 Küffer, Alexander; Lakkaraju, Asvin K. K.; Mogha, Amit Nature Publishing Group https://doi.org/10.5167/uzh-125485	text	January 2016
A molecular mechanism for Wnt ligand-specific signaling Eubelen, Marie; Bostaille, Naguissa; Cabochette, Pauline Frontiers in Neuroscience, Vol. 12 https://doi.org/10.3389/conf.fnins.2018.95.00097	journal	January 2018
Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nik-Zainal, Serena; Davies, Helen; Staaf, Johan Springer Science and Business Media LLC https://doi.org/10.17863/cam.31887	journalarticle	January 2016
A Tethered Agonist within the Ectodomain Activates the Adhesion G Protein-Coupled Receptors GPR126 and GPR133 Liebscher, Ines; Schön, Julia; Petersen, Sarah C. Cell Reports, Vol. 10, Issue 6 https://doi.org/10.1016/j.celrep.2015.01.065	journal	February 2015
Proteolytic cleavage of the EMR2 receptor requires both the extracellular stalk and the GPS motif Chang, Gin-Wen; Stacey, Martin; Kwakkenbos, Mark J. FEBS Letters, Vol. 547, Issue 1-3 https://doi.org/10.1016/s0014-5793(03)00695-1	journal	June 2003
Structure and properties of the Ca2+-binding CUB domain, a widespread ligand-recognition unit involved in major biological functions Gaboriaud, Christine; Gregory-Pauron, Lynn; Teillet, Florence Biochemical Journal, Vol. 439, Issue 2 https://doi.org/10.1042/bj20111027	journal	September 2011
The adhesion GPCR latrophilin – a novel signaling cascade in oriented cell division and anterior-posterior polarity Winkler, Jana; Prömel, Simone Worm, Vol. 5, Issue 2 https://doi.org/10.1080/21624054.2016.1170274	journal	March 2016
The geometry of metal–ligand interactions relevant to proteins. II. Angles at the metal atom, additional weak metal–donor interactions Harding, Marjorie M. Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 7 https://doi.org/10.1107/s0907444900005849	journal	July 2000
A Genetic Variant in GPR126 Causing a Decreased Inclusion of Exon 6 Is Associated with Cartilage Development in Adolescent Idiopathic Scoliosis Population Xu, Enjie; Shao, Wei; Jiang, Heng BioMed Research International, Vol. 2019 https://doi.org/10.1155/2019/4678969	journal	February 2019
Computed Origami Tomography Kittenberger, Axel; Mindrinos, Leonidas; Scherzer, Otmar arXiv https://doi.org/10.48550/arxiv.2006.03446	preprint	January 2020

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Title: Structural basis for adhesion G protein-coupled receptor Gpr126 function

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