The constitutive activity of the adhesion GPCR GPR114/ADGRG5 is mediated by its tethered agonist

FASEB Journal

Volumn 30, Issue 2, 2016, Pages 666-673

  Wilde, Caroline ^a   Fischer, Liane ^a   Lede, Vera ^a   Kirchberger, Jürgen ^a   Rothemund, Sven ^a   Schöneberg, Torsten ^a   Liebscher, Ines ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Peptide agonist; Receptor activation; Receptor structure function; Signal transduction; Tissue specific splicing

Indexed keywords

ADGRG 5 PROTEIN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR AGONIST; GPR 114 PROTEIN; UNCLASSIFIED DRUG; GPR114 PROTEIN, MOUSE; ISOPROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAMP ASSAY; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL CULTURE; EXON; MOUSE; MUTAGENESIS; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTIGENE FAMILY; MUTATION; PHYSIOLOGY; TISSUE DISTRIBUTION;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GENE EXPRESSION REGULATION; MICE; MULTIGENE FAMILY; MUTATION; PROTEIN ISOFORMS; RECEPTORS, G-PROTEIN-COUPLED; TISSUE DISTRIBUTION;

EID: 84958778198     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-276220     Document Type: Article

References (35)

1. Kuhnert, F., Mancuso, M. R., Shamloo, A., Wang, H.-T., Choksi, V., Florek, M., Su, H., Fruttiger, M., Young, W.L., Heilshorn, S.C., and Kuo, C. J. (2010) Essential regulation of CNS angiogenesis by the orphan G protein-coupled receptor GPR124. Science 330, 985-989
2. Langenhan, T., Promel, S., Mestek, L., Esmaeili, B., Waller-Evans, H., Hennig, C., Kohara, Y., Avery, L., Vakonakis, I., Schnabel, R., and Russ, A.P. (2009)Latrophilinsignaling links anterior-posterior tissue polarity and oriented cell divisions in theC. elegans embryo. Dev. Cell 17, 494-504
3. Lawrence, P. A., Struhl, G., and Casal, J. (2007) Planar cell polarity: one or two pathways? Nat. Rev. Genet. 8, 555-563.
4. Tissir, F., Bar, I., Jossin, Y., De Backer, O., and Goffinet, A.M. (2005) Protocadherin Celsr3 is crucial in axonal tract development. Nat. Neurosci. 8, 451-457.
5. Waller-Evans, H., Promel, S., Langenhan, T., Dixon, J., Zahn, D., Colledge, W. H., Doran, J., Carlton, M. B., Davies, B., Aparicio, S.A., Grosse, J., and Russ, A. P. (2010) The orphan adhesion-GPCR GPR126 is required for embryonic development in themouse. PLoS One 5, e14047
6. Weston, M. D., Luijendijk, M. W., Humphrey, K. D., Moller, C., and Kimberling, W. J. (2004)Mutations in the VLGR1 gene implicate Gprotein signaling in the pathogenesis ofUsher syndrome type II. Am. J. Hum. Genet. 74, 357-366
7. Piao, X., Hill, R. S., Bodell, A., Chang, B. S., Basel-Vanagaite, L., Straussberg, R., Dobyns, W. B., Qasrawi, B., Winter, R. M., Innes, A.M., Voit, T., Ross, M. E., Michaud, J. L., Descarie, J.-C., Barkovich, A. J., and Walsh, C. A. (2004)Gprotein-coupled receptor-dependent development of human frontal cortex. Science 303, 2033-2036
8. Bjarnadottir, T. K., Fredriksson, R., Hoglund, P. J., Gloriam, D. E., Lagerstrom, M.C., andSchioth, H.B. (2004)Thehumanandmouse repertoire of the adhesion family of G-protein-coupled receptors. Genomics 84, 23-33
9. Bjarnadottir, T. K., Fredriksson, R., and Schioth, H. B. (2007) The adhesion GPCRs: a unique family of G protein-coupled receptors with important roles in both central and peripheral tissues. Cell.Mol. Life Sci. 64, 2104-2119
10. Yona, S., Lin, H.H., Siu, W. O., Gordon, S., and Stacey, M. (2008) Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem. Sci. 33, 491-500
11. Bjarnadottir, T.K., Geirardsdottir, K., Ingemansson, M., Mirza, M.A., Fredriksson, R., and Schioth, H. B. (2007) Identification of novel splice variants of Adhesion G protein-coupled receptors. Gene 387, 38-48
12. Ara, D., Boucard, A. A., Bolliger, M. F., Nguyen, J., Soltis, S. M., Sudhof, T. C., and Brunger, A. T. (2012) A novel evolutionarily conserved domain of cell-adhesionGPCRsmediates autoproteolysis. EMBO J. 31, 1364-1378
13. Bohnekamp, J., and Schoneberg, T. (2011) Cell adhesion receptor GPR133 couples to Gs protein. J. Biol. Chem. 286, 41912-41916
14. Gupte, J., Swaminath, G., Danao, J., Tian, H., Li, Y., and Wu, X. (2012) Signaling property study of adhesion G-protein-coupled receptors. FEBS Lett. 586, 1214-1219
15. Mogha, A., Benesh, A. E., Patra, C., Engel, F. B., Schoneberg, T., Liebscher, I., and Monk, K. R. (2013) Gpr126 functions in Schwann cells to control differentiation and myelination via G-protein activation. J. Neurosci. 33, 17976-17985.
16. Stoveken, H. M., Hajduczok, A. G., Xu, L., and Tall, G. G. (2015) Adhesion G protein-coupled receptors are activated by exposure of a cryptic tethered agonist. Proc. Natl. Acad. Sci. USA 112, 6194-6199
17. Okajima, D., Kudo, G., and Yokota, H. (2010) Brain-specific angiogenesis inhibitor 2 (BAI2)may be activatedby proteolytic processing. J. Recept. Signal Transduct. Res. 30, 143-153
18. Paavola, K. J., Stephenson, J. R., Ritter, S. L., Alter, S. P., and Hall, R. A. (2011) The N terminus of the adhesion G protein-coupled receptorGPR56 controls receptor signaling activity. J. Biol.Chem. 286, 28914-28921
19. Ward, Y., Lake, R., Yin, J. J., Heger, C.D., Raffeld, M., Goldsmith, P.K., Merino, M., and Kelly, K. (2011) LPA receptor heterodimerizes with CD97 to amplify LPA-initiated RHO-dependent signaling and invasion in prostate cancer cells. Cancer Res. 71, 7301-7311
20. Liebscher, I., Schon, J., Petersen, S. C., Fischer, L., Auerbach, N., Demberg, L.M., Mogha, A., Coster, M., Simon, K.U., Rothemund, S., Monk, K. R., and Schoneberg, T. (2014) A tethered agonist within the ectodomain activates the adhesion G protein-coupled receptors GPR126 and GPR133. Cell Rep. 9, 2018-2026
21. Demberg, L. M., Rothemund, S., Schoneberg, T., and Liebscher, I. (2015) Identification of the tethered peptide agonistof the adhesion G protein-coupled receptor GPR64/ADGRG2. Biochem. Biophys. Res. Commun. 464, 743-747
22. Petersen, S.C., Luo, R., Liebscher, I., Giera, S., Jeong, S.-J., Mogha, A., Ghidinelli, M., Feltri, M. L., Schoneberg, T., Piao, X., and Monk, K.R. (2015) The adhesion GPCR GPR126 has distinct, domaindependent functions in Schwann cell development mediated by interaction with laminin-211. Neuron 85, 755-769
23. Schioth, H. B., Nordstrom, K. J., and Fredriksson, R. (2010) The adhesion GPCRs; gene repertoire, phylogeny and evolution. Adv. Exp. Med. Biol. 706, 1-13
24. Engelman, C. D., Meyers, K. J., Ziegler, J. T., Taylor, K. D., Palmer, N.D., Haffner, S.M., Fingerlin, T.E., Wagenknecht, L.E., Rotter, J. I., Bowden, D. W., Langefeld, C.D., and Norris, J. M. (2010) Genomewide association study of vitamin D concentrations in Hispanic Americans: the IRAS family study. J. Steroid Biochem. Mol. Biol. 122, 186-192
25. Burset, M., Seledtsov, I. A., and Solovyev, V. V. (2000) Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Res. 28, 4364-4375
26. Preissler, J., Grosche, A., Lede, V., LeDuc, D., Krugel, K., Matyash, V., Szulzewsky, F., Kallendrusch, S., Immig, K., Kettenmann, H., Bechmann, I., Schoneberg, T., and Schulz, A. (2015) Altered microglial phagocytosis in GPR34-deficient mice. Glia 63, 206-215
27. Quinlan, A. R., and Hall, I. M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842
28. Sangkuhl, K., Schulz, A., Schultz, G., and Schoneberg, T. (2002) Structural requirements formutational lutropin/choriogonadotropin receptor activation. J. Biol. Chem. 277, 47748-47755
29. Schoneberg, T., Schulz, A., Biebermann, H., Hermsdorf, T., Rompler, H., and Sangkuhl, K. (2004) Mutant G-protein-coupled receptors as a cause of humandiseases. Pharmacol.Ther. 104, 173-206
30. Rompler, H., Yu, H.T., Arnold, A., Orth, A., and Schoneberg, T. (2006) Functional consequences of naturally occurring DRY motif variants in the mammalian chemoattractant receptor GPR33. Genomics 87, 724-732.
31. Moriguchi, T., Haraguchi, K., Ueda, N., Okada, M., Furuya, T., and Akiyama, T. (2004) DREG, a developmentally regulated G proteincoupled receptor containing two conserved proteolytic cleavage sites. Genes Cells 9, 549-560
32. Krasnoperov, V. G., Bittner, M. A., Beavis, R., Kuang, Y., Salnikow, K. V., Chepurny, O. G., Little, A. R., Plotnikov, A. N., Wu, D., Holz, R. W., and Petrenko, A. G. (1997) alpha-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 18, 925-937
33. Promel, S., Frickenhaus, M., Hughes, S., Mestek, L., Staunton, D., Woollard, A., Vakonakis, I., Schoneberg, T., Schnabel, R., Russ, A. P., and Langenhan, T. (2012) The GPS motif is a molecular switch for bimodal activities of adhesion classGprotein-coupled receptors. Cell Rep. 2, 321-331
34. Luo, R., Jeong, S.-J., Yang, A., Wen, M., Saslowsky, D. E., Lencer, W. I., Ara, D., and Piao, X. (2014) Mechanism for adhesion G proteincoupled receptor GPR56-mediated RhoA activation induced by collagen III stimulation. PLoS One 9, e100043
35. Karpus, O.N., Veninga, H., Hoek, R.M., Flierman, D., vanBuul, J.D., Vandenakker, C. C., vanBavel, E., Medof, M. E., van Lier, R. A., Reedquist, K. A., and Hamann, J. (2013) Shear stress-dependent downregulation of the adhesion-G protein-coupled receptor CD97 on circulating leukocytes upon contact with its ligand CD55. J. Immunol. 190, 3740-3748.