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Introduction: History of the Adhesion GPCR Field

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Adhesion G Protein-coupled Receptors

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 234))

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References

  1. Baud V, Chissoe SL, Viegas-Péquignot E, Diriong S, N’Guyen VC, Roe BA et al (1995) EMR1, an unusual member in the family of hormone receptors with seven transmembrane segments. Genomics 26:334–344

    Article  CAS  PubMed  Google Scholar 

  2. Hamann J, Eichler W, Hamann D, Kerstens HM, Poddighe PJ, Hoovers JM et al (1995) Expression cloning and chromosomal mapping of the leukocyte activation antigen CD97, a new seven-span transmembrane molecule of the secretion receptor superfamily with an unusual extracellular domain. J Immunol 155:1942–1950

    CAS  PubMed  Google Scholar 

  3. McKnight AJ, Gordon S (1996) EGF-TM7: a novel subfamily of seven-transmembrane-region leukocyte cell-surface molecules. Immunol Today 17:283–287

    Article  CAS  PubMed  Google Scholar 

  4. Krasnoperov VG, Bittner MA, Beavis R, Kuang Y, Salnikow KV, Chepurny OG et al (1997) alpha-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 18:925–937

    Article  CAS  PubMed  Google Scholar 

  5. Lelianova VG, Davletov BA, Sterling A, Rahman MA, Grishin EV, Totty NF et al (1997) Alpha-latrotoxin receptor, latrophilin, is a novel member of the secretin family of G protein-coupled receptors. J Biol Chem 272:21504–21508

    Article  CAS  PubMed  Google Scholar 

  6. Araç D, Boucard AA, Bolliger MF, Nguyen J, Soltis SM, Südhof TC et al (2012) A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis. EMBO J 31:1364–1378

    Article  PubMed  PubMed Central  Google Scholar 

  7. Gray JX, Haino M, Roth MJ, Maguire JE, Jensen PN, Yarme A et al (1996) CD97 is a processed, seven-transmembrane, heterodimeric receptor associated with inflammation. J Immunol 157:5438–5447

    CAS  PubMed  Google Scholar 

  8. Krasnoperov V, Lu Y, Buryanovsky L, Neubert TA, Ichtchenko K, Petrenko AG (2002) Post-translational proteolytic processing of the calcium-independent receptor of alpha-latrotoxin (CIRL), a natural chimera of the cell adhesion protein and the G protein-coupled receptor. Role of the G protein-coupled receptor proteolysis site (GPS) motif. J Biol Chem 277:46518–46526

    Article  CAS  PubMed  Google Scholar 

  9. Lin HH, Chang GW, Davies JQ, Stacey M, Harris J, Gordon S (2004) Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J Biol Chem 279:31823–31832

    Article  CAS  PubMed  Google Scholar 

  10. Bjarnadóttir TK, Fredriksson R, Höglund PJ, Gloriam DE, Lagerström MC, Schiöth HB (2004) The human and mouse repertoire of the adhesion family of G-protein-coupled receptors. Genomics 84:23–33

    Article  PubMed  Google Scholar 

  11. Lagerström MC, Schiöth HB (2008) Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat Rev Drug Discov 7:339–357

    Article  PubMed  Google Scholar 

  12. Nordström KJ, Lagerström MC, Wallér LM, Fredriksson R, Schiöth HB (2009) The Secretin GPCRs descended from the family of Adhesion GPCRs. Mol Biol Evol 26:71–84

    Article  PubMed  Google Scholar 

  13. Hamann J, Aust G, Araç D, Engel FB, Formstone C, Fredriksson R et al (2015) International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G protein-coupled receptors. Pharmacol Rev 67:338–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Austyn JM, Gordon S (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 11:805–815

    Article  CAS  PubMed  Google Scholar 

  15. Gordon S, Hamann J, Lin HH, Stacey M (2011) F4/80 and the related adhesion-GPCRs. Eur J Immunol 41:2472–2476

    Article  CAS  PubMed  Google Scholar 

  16. Park D, Tosello-Trampont AC, Elliott MR, Lu M, Haney LB, Ma Z et al (2007) BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 450:430–434

    Article  CAS  PubMed  Google Scholar 

  17. Das S, Owen KA, Ly KT, Park D, Black SG, Wilson JM et al (2011) Brain angiogenesis inhibitor 1 (BAI1) is a pattern recognition receptor that mediates macrophage binding and engulfment of Gram-negative bacteria. Proc Natl Acad Sci U S A 108:2136–2141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lang J, Ushkaryov Y, Grasso A, Wollheim CB (1998) Ca2+-independent insulin exocytosis induced by alpha-latrotoxin requires latrophilin, a G protein-coupled receptor. EMBO J 17:648–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Silva JP, Lelianova VG, Ermolyuk YS, Vysokov N, Hitchen PG, Berninghausen O et al (2011) Latrophilin 1 and its endogenous ligand Lasso/teneurin-2 form a high-affinity transsynaptic receptor pair with signaling capabilities. Proc Natl Acad Sci U S A 108:12113–12118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Boucard AA, Maxeiner S, Südhof TC (2014) Latrophilins function as heterophilic cell-adhesion molecules by binding to teneurins: regulation by alternative splicing. J Biol Chem 289:387–402

    Article  CAS  PubMed  Google Scholar 

  21. O’Sullivan ML, de Wit J, Savas JN, Comoletti D, Otto-Hitt S, Yates JR III et al (2012) FLRT proteins are endogenous latrophilin ligands and regulate excitatory synapse development. Neuron 73:903–910

    Article  PubMed  PubMed Central  Google Scholar 

  22. Piao X, Hill RS, Bodell A, Chang BS, Basel-Vanagaite L, Straussberg R et al (2004) G protein-coupled receptor-dependent development of human frontal cortex. Science 303:2033–2036

    Article  CAS  PubMed  Google Scholar 

  23. Bae BI, Tietjen I, Atabay KD, Evrony GD, Johnson MB, Asare E et al (2014) Evolutionarily dynamic alternative splicing of GPR56 regulates regional cerebral cortical patterning. Science 343:764–768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Giera S, Deng Y, Luo R, Ackerman SD, Mogha A, Monk KR et al (2015) The adhesion G protein-coupled receptor GPR56 is a cell-autonomous regulator of oligodendrocyte development. Nat Commun 6:6121

    Article  PubMed  PubMed Central  Google Scholar 

  25. Ackerman SD, Garcia C, Piao X, Gutmann DH, Monk KR (2015) The adhesion GPCR Gpr56 regulates oligodendrocyte development via interactions with Gα12/13 and RhoA. Nat Commun 21:6122

    Article  Google Scholar 

  26. Monk KR, Naylor SG, Glenn TD, Mercurio S, Perlin JR, Dominguez C et al (2009) A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 325:1402–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Petersen SC, Luo R, Liebscher I, Giera S, Jeong SJ, Mogha A et al (2015) The adhesion GPCR GPR126 has distinct, domain-dependent functions in Schwann cell development mediated by interaction with laminin-211. Neuron 85:755–769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, Schwarz TL et al (1999) Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98:585–595

    Article  CAS  PubMed  Google Scholar 

  29. Shimada Y, Usui T, Yanagawa S, Takeichi M, Uemura T (2001) Asymmetric colocalization of Flamingo, a seven-pass transmembrane cadherin, and Dishevelled in planar cell polarization. Curr Biol 11:859–863

    Article  CAS  PubMed  Google Scholar 

  30. Chen WS, Antic D, Matis M, Logan CY, Povelones M, Anderson GA et al (2008) Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 133:1093–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Nishimura T, Honda H, Takeichi M (2012) Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149:1084–1097

    Article  CAS  PubMed  Google Scholar 

  32. Langenhan T, Prömel S, Mestek L, Esmaeili B, Waller-Evans H, Hennig C et al (2009) Latrophilin signaling links anterior-posterior tissue polarity and oriented cell divisions in the C. elegans embryo. Dev Cell 17:494–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Steimel A, Wong L, Najarro EH, Ackley BD, Garriga G, Hutter H (2010) The Flamingo ortholog FMI-1 controls pioneer-dependent navigation of follower axons in C. elegans. Development 137:3663–3673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Tissir F, Goffinet AM (2013) Shaping the nervous system: role of the core planar cell polarity genes. Nat Rev Neurosci 14:525–535

    Article  CAS  PubMed  Google Scholar 

  35. Weston MD, Luijendijk MW, Humphrey KD, Möller C, Kimberling WJ (2004) Mutations in the VLGR1 gene implicate G-protein signaling in the pathogenesis of Usher syndrome type II. Am J Hum Genet 74:357–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Aust G, Eichler W, Laue S, Lehmann I, Heldin NE, Lotz O et al (1997) CD97: a dedifferentiation marker in human thyroid carcinomas. Cancer Res 57:1798–1806

    CAS  PubMed  Google Scholar 

  37. Steinert M, Wobus M, Boltze C, Schütz A, Wahlbuhl M, Hamann J et al (2002) Expression and regulation of CD97 in colorectal carcinoma cell lines and tumor tissues. Am J Pathol 161:1657–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Xu L, Begum S, Hearn JD, Hynes RO (2006) GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci U S A 103:9023–9028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Araç D, Aust G, Calebiro D, Engel FB, Formstone C, Goffinet A, Hamann J et al (2012) Dissecting signaling and functions of adhesion G protein-coupled receptors. Ann N Y Acad Sci 1276:1–25

    Article  PubMed  Google Scholar 

  40. Liebscher I, Ackley B, Araç D, Ariestanti DM, Aust G, Bae BI et al (2014) New functions and signaling mechanisms for the class of adhesion G protein-coupled receptors. Ann N Y Acad Sci 1333:43–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hamann J, Vogel B, van Schijndel GM, van Lier RA (1996) The seven-span transmembrane receptor CD97 has a cellular ligand (CD55, DAF). J Exp Med 184:1185–1189

    Article  CAS  PubMed  Google Scholar 

  42. Langenhan T, Aust G, Hamann J (2013) Sticky signaling–adhesion class G protein-coupled receptors take the stage. Sci Signal 6:re3

    Article  PubMed  Google Scholar 

  43. Paavola KJ, Stephenson JR, Ritter SL, Alter SP, Hall RA (2011) The N terminus of the adhesion G protein-coupled receptor GPR56 controls receptor signaling activity. J Biol Chem 286:28914–28921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Yang L, Chen G, Mohanty S, Scott G, Fazal F, Rahman A et al (2011) GPR56 Regulates VEGF production and angiogenesis during melanoma progression. Cancer Res 71:5558–5568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Prömel S, Frickenhaus M, Hughes S, Mestek L, Staunton D, Woollard A et al (2012) The GPS motif is a molecular switch for bimodal activities of adhesion class G protein-coupled receptors. Cell Rep 2:321–331

    Article  PubMed  PubMed Central  Google Scholar 

  46. Liebscher I, Schön J, Petersen SC, Fischer L, Auerbach N, Demberg LM et al (2014) A tethered agonist within the ectodomain activates the adhesion G protein-coupled receptors GPR126 and GPR133. Cell Rep 9:2018–2026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Stoveken HM, Hajduczok AG, Xu L, Tall GG (2015) Adhesion G protein-coupled receptors are activated by exposure of a cryptic tethered agonist. Proc Natl Acad Sci U S A 112:6194–6199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. White JP, Wrann CD, Rao RR, Nair SK, Jedrychowski MP, You JS et al (2014) G protein-coupled receptor 56 regulates mechanical overload-induced muscle hypertrophy. Proc Natl Acad Sci U S A 111:15756–15761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Scholz N, Gehring J, Guan C, Ljaschenko D, Fischer R, Lakshmanan V et al (2015) The adhesion GPCR latrophilin/CIRL shapes mechanosensation. Cell Rep 11:866–874

    Article  CAS  PubMed  Google Scholar 

  50. Gupte J, Swaminath G, Danao J, Tian H, Li Y, Wu X (2012) Signaling property study of adhesion G-protein-coupled receptors. FEBS Lett 586:1214–1219

    Article  CAS  PubMed  Google Scholar 

  51. Paavola KJ, Sidik H, Zuchero JB, Eckart M, Talbot WS (2014) Type IV collagen is an activating ligand for the adhesion G protein-coupled receptor GPR126. Sci Signal 7:ra76

    Article  PubMed  PubMed Central  Google Scholar 

  52. Ward Y, Lake R, Yin JJ, Heger CD, Raffeld M, Goldsmith PK et al (2011) LPA receptor heterodimerizes with CD97 to amplify LPA-initiated RHO-dependent signaling and invasion in prostate cancer cells. Cancer Res 71:7301–7311

    Article  CAS  PubMed  Google Scholar 

  53. Nishimori H, Shiratsuchi T, Urano T, Kimura Y, Kiyono K, Tatsumi K et al (1997) A novel brain-specific p53-target gene, BAI1, containing thrombospondin type 1 repeats inhibits experimental angiogenesis. Oncogene 15:2145–2150

    Article  CAS  PubMed  Google Scholar 

  54. Krasnoperov V, Deyev IE, Serova OV, Xu C, Lu Y, Buryanovsky L et al (2009) Dissociation of the subunits of the calcium-independent receptor of alpha-latrotoxin as a result of two-step proteolysis. Biochemistry 48:3230–3238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Monk KR, Hamann J, Langenhan T, Nijmeijer S, Schöneberg T, Liebscher I (2015) Adhesion G protein-coupled receptors: from in vitro pharmacology to in vivo mechanisms. Mol Pharmacol 88:617–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The writing of this manuscript was supported by the Deutsche Forschungsgemeinschaft (Research Unit 2149) and by grants of the Thyssen Foundation (2015-00387) to JH and the Russian Science Foundation (14-14-01195) to AGP.

Competing Financial Interests The authors declare no competing financial interests.

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Correspondence to Jörg Hamann or Alexander G. Petrenko .

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Hamann, J., Petrenko, A.G. (2016). Introduction: History of the Adhesion GPCR Field. In: Langenhan, T., Schöneberg, T. (eds) Adhesion G Protein-coupled Receptors. Handbook of Experimental Pharmacology, vol 234. Springer, Cham. https://doi.org/10.1007/978-3-319-41523-9_1

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