Tethered agonism: A common activation mechanism of adhesion GPCRs

Handbook of Experimental Pharmacology

Volumn 234, Issue , 2016, Pages 111-125

  Liebscher, Ines ^a   Schöneberg, Torsten ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Activation mechanism; Adhesion GPCR; Peptide agonist; Signal transduction; Tethered agonism

Indexed keywords

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; AUTOCLEAVAGE SITE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; EX VIVO STUDY; GENOMIC ORGANIZATION; GENOMICS; HUMAN; INTERNALIZATION; MECHANICAL STRESS; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SEVEN TRANSMEMBRANE DOMAIN; SIGNAL TRANSDUCTION; STACHEL RELEASE; STACHEL SEQUENCE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TETHERED AGONISM; AGONISTS; ANIMAL; CELL ADHESION; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; METABOLISM; MOLECULAR MODEL; SYNTHESIS;

G PROTEIN COUPLED RECEPTOR; PEPTIDE; PROTEIN BINDING;

ANIMALS; BINDING SITES; CELL ADHESION; CELL MEMBRANE; HUMANS; MODELS, MOLECULAR; PEPTIDES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84995404823     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/978-3-319-41523-9_6     Document Type: Chapter

References (61)

1. Ritter E, Zimmermann K, Heck M, Hofmann KP, Bartl FJ (2004) Transition of rhodopsin into the active metarhodopsin II state opens a new light-induced pathway linked to Schiff base isomerization. J Biol Chem 279:48102-48111
2. Coughlin SR (2005) Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost 3:1800-1814
3. Adams MN, Ramachandran R, Yau M-K, Suen JY, Fairlie DP, Hollenberg MD et al (2011) Structure, function and pathophysiology of protease activated receptors. Pharmacol Ther 130:248-282
4. Austin KM, Covic L, Kuliopulos A (2013) Matrix metalloproteases and PAR1 activation. Blood 121:431-439
5. Araç D, Sträter N, Seiradake E. (2016) Understanding the structural basis of adhesion GPCR functions. In: Langenhan T, Schöneberg T (eds) Adhesion G protein-coupled receptors: molecular, physiological and pharmacological principles in health and disease. Springer, Heidelberg
6. Schulz A, Schoneberg T (2003) The structural evolution of a P2Y-like G-protein-coupled receptor. J Biol Chem 278:35531-35541
7. Böselt I, Römpler H, Hermsdorf T, Thor D, Busch W, Schulz A et al (2009) Involvement of the V2 vasopressin receptor in adaptation to limited water supply. PLoS One 4, e5573
8. Sanchez-Mas J, Hahmann C, Gerritsen I, Garcia-Borron JC, Jimenez-Cervantes C (2004) Agonist-independent, high constitutive activity of the human melanocortin 1 receptor. Pigment Cell Res 17:386-395
9. Iguchi T, Sakata K, Yoshizaki K, Tago K, Mizuno N, Itoh H (2008) Orphan G protein-coupled receptor GPR56 regulates neural progenitor cell migration via a G alpha 12/13 and Rho pathway. J Biol Chem 283:14469-14478
10. Luo R, Jeong S-J, Jin Z, Strokes N, Li S, Piao X (2011) G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc Natl Acad Sci U S A 108:12925-12930
11. 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
12. Bohnekamp J, Schöneberg T (2011) Cell adhesion receptor GPR133 couples to Gs protein. J Biol Chem 286:41912-41916
13. 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
14. Stephenson JR, Paavola KJ, Schaefer SA, Kaur B, Van Meir EG, Hall RA (2013) Brainspecific angiogenesis inhibitor-1 signaling, regulation, and enrichment in the postsynaptic density. J Biol Chem 288:22248-22256
15. Mogha A, Benesh AE, Patra C, Engel FB, Schoneberg T, Liebscher I et al (2013) Gpr126 functions in Schwann cells to control differentiation and myelination via G-protein activation. J Neurosci 33:17976-17985
16. Hu QX, Dong JH, Du HB, Zhang DL, Ren HZ, Ma ML et al (2014) Constitutive Galphai coupling activity of very large G protein-coupled receptor 1 (VLGR1) and its regulation by PDZD7 protein. J Biol Chem 289:24215-24225
17. Demberg LM, Rothemund S, Schoneberg T, Liebscher I (2015) Identification of the tethered peptide agonist of the adhesion G protein-coupled receptor GPR64/ADGRG 2. Biochem Biophys Res Commun 464:743-747
18. Peeters MC, Fokkelman M, Boogaard B, Egerod KL, van de Water B, IJzerman AP et al (2015) The adhesion G protein-coupled receptor G2 (ADGRG2/GPR64) constitutively activates SRE and NFkB and is involved in cell adhesion and migration. Cell Signal 27 (12):2579-2588
19. Müller A, Winkler J, Fiedler F, Sastradihardja T, Binder C, Schnabel R et al (2015) Oriented cell division in the C. elegans embryo is coordinated by G-protein signaling dependent on the adhesion GPCR LAT-1. PLoS Genet 11, e1005624
20. Okajima D, Kudo G, Yokota H (2010) Brain-specific angiogenesis inhibitor 2 (BAI2) may be activated by proteolytic processing. J Recept Signal Transduct Res 30:143-153
21. 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
22. 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
23. Liebscher I, Schoneberg T, Promel S (2013) Progress in demystification of adhesion G proteincoupled receptors. Biol Chem 394:937-950
24. Liebscher I, Schon 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 GPR 133. Cell Rep 9:2018-2026
25. 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
26. 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
27. Wilde C, Fischer L, Lede V, Kirchberger J, Rothemund S, Schoneberg T et al (2016) The constitutive activity of the adhesion GPCR GPR114/ADGRG5 is mediated by its tethered agonist. FASEB J 30:666-673
28. Kishore A, Purcell RH, Nassiri-Toosi Z, Hall RA (2016) Stalk-dependent and stalkindependent signaling by the adhesion G protein-coupled receptors GPR56 (ADGRG1) and BAI1 (ADGRB1). J Biol Chem 291:3385-3394
29. Kishore A, Hall RA (2016) Versatile signaling activity of adhesion GPCRs. In: Langenhan T, Schöneberg T (eds) Adhesion G protein-coupled receptors: molecular, physiological and pharmacological principles in health and disease. Springer, Heidelberg
30. 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
31. Lu YC, Nazarko OV, Sando R, Salzman GS, Südhof TC, Araç D (2015) Structural basis of latrophilin-FLRT-UNC5 interaction in cell adhesion. Structure 23:1678-1691
32. Nijmeijer S, Wolf S, Ernst OP, de Graaf C (2016) 7TM domain structure of adhesion GPCRs. In: Langenhan T, Schöneberg T (eds) Adhesion G protein-coupled receptors: molecular, physiological and pharmacological principles in health and disease. Springer, Heidelberg
33. Petersen SC, Luo R, Liebscher I, Giera S, Jeong S-J, 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
34. 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
35. Scholz N, Monk KR, Kittel RJ, Langenhan T (2016) Adhesion GPCRs as a putative class of metabotropic mechanosensors. In: Langenhan T, Schöneberg T (eds) Adhesion G proteincoupled receptors: molecular, physiological and pharmacological principles in health and disease. Springer, Heidelberg
36. Luo R, Jeong S-J, Yang A, Wen M, Saslowsky DE, Lencer WI et al (2014) Mechanism for adhesion G protein-coupled receptor GPR56-mediated RhoA activation induced by collagen III stimulation. PLoS One 9, e100043
37. White JP, Wrann CD, Rao RR, Nair SK, Jedrychowski MP, You J-S et al (2014) G proteincoupled receptor 56 regulates mechanical overload-induced muscle hypertrophy. Proc Natl Acad Sci U S A 111:15756-15761
38. 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
39. 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 GPR 126. Sci Signal 7:ra76
40. Yang L, Friedland S, Corson N, Xu L (2014) GPR56 inhibits melanoma growth by internalizing and degrading its ligand TG 2. Cancer Res 74:1022-1031
41. Nieberler M, Kittel RJ, Petrenko AG, Lin H-H, Langenhan T (2016) Control of adhesion GPCR function through proteolytic processing. In: Langenhan T, Schöneberg T (eds) Adhesion G protein-coupled receptors: molecular, physiological and pharmacological principles in health and disease. Springer, Heidelberg
42. Krasnoperov V, Lu Y, Buryanovsky L, Neubert TA, Ichtchenko K, Petrenko AG (2002) Posttranslational 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
43. Lin H-H, Chang G-W, Davies JQ, Stacey M, Harris J (2004) Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J Biol Chem 279:31823-31832
44. Moriguchi T, Haraguchi K, Ueda N, Okada M, Furuya T, Akiyama T (2004) DREG, a developmentally regulated G protein-coupled receptor containing two conserved proteolytic cleavage sites. Genes Cells 9:549-560
45. Prömel S, Waller-Evans H, Dixon J, Zahn D, Colledge WH, Doran J et al (2012) Characterization and functional study of a cluster of four highly conserved orphan adhesion-GPCR in mouse. Dev Dyn 241:1591-1602
46. Stephenson JR, Purcell RH, Hall RA (2014) The BAI subfamily of adhesion GPCRs: synaptic regulation and beyond. Trends Pharmacol Sci 35:208-215
47. 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
48. Wald G (1968) The molecular basis of visual excitation. Nature 219:800-807
49. Vu TK, Hung DT, Wheaton VI, Coughlin SR (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64:1057-1068
50. Bruser A, Schulz A, Rothemund S, Ricken A, Calebiro D, Kleinau G et al (2016) The Activation Mechanism of Glycoprotein Hormone Receptors with Implications in the Cause and Therapy of Endocrine Diseases. J Biol Chem 291:508-520
51. Vlaeminck-Guillem V, Ho S-C, Rodien P, Vassart G, Costagliola S (2002) Activation of the cAMP pathway by the TSH receptor involves switching of the ectodomain from a tethered inverse agonist to an agonist. Mol Endocrinol 16:736-746
52. van Sande J, Massart C, Costagliola S, Allgeier A, Cetani F, Vassart G et al (1996) Specific activation of the thyrotropin receptor by trypsin. Mol Cell Endocrinol 119:161-168
53. Zhang M, Tong KP, Fremont V, Chen J, Narayan P, Puett D et al (2000) The extracellular domain suppresses constitutive activity of the transmembrane domain of the human TSH receptor: implications for hormone-receptor interaction and antagonist design. Endocrinology 141:3514-3517
54. Sangkuhl K, Schulz A, Schultz G, Schoneberg T (2002) Structural requirements for mutational lutropin/choriogonadotropin receptor activation. J Biol Chem 277:47748-47755
55. Krause G, Kreuchwig A, Kleinau G (2012) Extended and structurally supported insights into extracellular hormone binding, signal transduction and organization of the thyrotropin receptor. PLoS One 7, e52920
56. Zhang C, Srinivasan Y, Arlow DH, Fung JJ, Palmer D, Zheng Y et al (2012) High-resolution crystal structure of human protease-activated receptor 1. Nature 492:387-392
57. Heitman LH, Oosterom J, Bonger KM, Timmers CM, Wiegerinck PHG, Ijzerman AP (2008) 3HOrg 43553, the first low-molecular-weight agonistic and allosteric radioligand for the human luteinizing hormone receptor. Mol Pharmacol 73:518-524
58. Neumann S, Huang W, Titus S, Krause G, Kleinau G, Alberobello AT et al (2009) Smallmolecule agonists for the thyrotropin receptor stimulate thyroid function in human thyrocytes and mice. Proc Natl Acad Sci U S A 106:12471-12476
59. Neumann S, Nir EA, Eliseeva E, Huang W, Marugan J, Xiao J et al (2014) A selective TSH receptor antagonist inhibits stimulation of thyroid function in female mice. Endocrinology 155:310-314
60. van Amerongen PC, Machteld J, Ghosh S, Ricciardi F, Sajjad A, Novoyatleva T et al (2013) Organ-specific function of adhesion G protein-coupled receptor GPR126 is domain-dependent. Proc Natl Acad Sci U S A 110:16898-16903
61. Fukuzawa T, Hirose S (2006) Multiple processing of Ig-Hepta/GPR116, a G protein-coupled receptor with immunoglobulin (Ig)-like repeats, and generation of EGF2-like fragment. J Biochem 140:445-452