Functions of third extracellular loop and helix 8 of family B GPCRs complexed with RAMPs and characteristics of their receptor trafficking

Current Protein and Peptide Science

Volumn 14, Issue 5, 2013, Pages 416-428

  Kuwasako, Kenji ^a   Hay, Debbie L ^b   Nagata, Sayaka ^a   Murakami, Manabu ^a   Kitamura, Kazuo ^a   Kato, Johji ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Adrenomedullin; Calcitonin gene related peptide; Calcitonin receptor like receptor; G protein coupled receptor kinase; Receptor activation; Receptor activity modifying protein; Receptor internalization

Indexed keywords

AMYLIN RECEPTOR; BETA ARRESTIN; CALCITONIN RECEPTOR; CALCITONIN RECEPTOR LIKE RECEPTOR; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE 2; G PROTEIN COUPLED RECEPTOR KINASE 3; G PROTEIN COUPLED RECEPTOR KINASE 4; G PROTEIN COUPLED RECEPTOR KINASE 5; G PROTEIN COUPLED RECEPTOR KINASE 6; GLUCAGON RECEPTOR; HELIX LOOP HELIX PROTEIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1; MEMBRANE PROTEIN; RECEPTOR ACTIVITY MODIFYING PROTEIN; RECEPTOR ACTIVITY MODIFYING PROTEIN 1; RECEPTOR ACTIVITY MODIFYING PROTEIN 2; RECEPTOR ACTIVITY MODIFYING PROTEIN 3; RHODOPSIN KINASE; SECRETIN; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 2;

BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CRYSTAL STRUCTURE; DESENSITIZATION; DISULFIDE BOND; ENERGY TRANSFER; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; INTERNALIZATION; MEMBRANE STABILIZATION; NONHUMAN; PDZ DOMAIN; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STOICHIOMETRY; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; HUMANS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTOR ACTIVITY-MODIFYING PROTEINS; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 84882709183     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/13892037113149990058     Document Type: Review

References (130)

1. Barwell, J.; Gingell, J.J.; Watkins, H.A.; Archbold, J.K.; Poyner, D.R.; Hay, D.L. Calcitonin and calcitonin receptor-like receptors: common themes with family B GPCRs? Br. J. Pharmacol., 2012, 166 (1), 51-65.
2. Poyner, D.R.; Hay, D.L. Secretin family (Class B) G proteincoupled receptors -from molecular to clinical perspectives. Br. J. Pharmaco., 2012, 166 (1), 1-3.
3. Wootten, D.; Lindmark, H.; Kadmiel, M.; Willcockson, H.; Caron, K.M.; Barwell, J.; Drmota, T.; Poyner, D.R. Receptor Activity Modifying Proteins (RAMPs) Interact with the VPAC(2) Receptor and CRF(1) Receptors and modulate their function. Br. J. Pharmacol., 2012.
4. McLatchie, L.M.; Fraser, N.J.; Main, M.J.; Wise, A.; Brown, J.; Thompson, N.; Solari, R.; Lee, M.G.; Foord, S.M. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature, 1998, 393 (6683), 333-339.
5. Couvineau, A.; Laburthe, M. VPAC receptors: structure, molecular pharmacology and interaction with accessory proteins. Br. J. Pharmacol., 2012, 166 (1), 42-50.
6. Muff, R.; Buhlmann, N.; Fischer, J.A.; Born, W. An amylin receptor is revealed following co-transfection of a calcitonin receptor with receptor activity modifying proteins-1 or -3. Endocrinology, 1999, 140 (6), 2924-2927.
7. Harikumar, K.G.; Simms, J.; Christopoulos, G.; Sexton, P.M.; Miller, L.J. Molecular basis of association of receptor activitymodifying protein 3 with the family B G protein-coupled secretin receptor. Biochemistry, 2009, 48 (49), 11773-11785.
8. Sexton, P.M.; Poyner, D.R.; Simms, J.; Christopoulos, A.; Hay, D.L. Modulating receptor function through RAMPs: can they represent drug targets in themselves? Drug Discov. Today, 2009, 14 (7-8), 413-419.
9. Morfis, M.; Christopoulos, A.; Sexton, P.M. RAMPs: 5 years on, where to now? Trends Pharmacol. Sci., 2003, 24 (11), 596-601.
10. Christopoulos, A.; Christopoulos, G.; Morfis, M.; Udawela, M.; Laburthe, M.; Couvineau, A.; Kuwasako, K.; Tilakaratne, N.; Sexton, P.M. Novel receptor partners and function of receptor activity-modifying proteins. J. Biol. Chem., 2003, 278 (5), 3293-3297.
11. Muff, R.; Born, W.; Fischer, J.A. Adrenomedullin selectivity of calcitonin-like receptor/receptor activity modifying proteins. Hypertens. Res., 2003, 26 Suppl, S3-8.
12. Hay, D.L.; Howitt, S.G.; Conner, A.C.; Schindler, M.; Smith, D.M.; Poyner, D.R. CL/RAMP2 and CL/RAMP3 produce pharmacologically distinct adrenomedullin receptors: a comparison of effects of adrenomedullin22-52, CGRP8-37 and BIBN4096BS. Br. J. Pharmacol., 2003, 140 (3), 477-486.
13. Poyner, D.R.; Sexton, P.M.; Marshall, I.; Smith, D.M.; Quirion, R.; Born, W.; Muff, R.; Fischer, J.A.; Foord, S.M. International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol. Rev., 2002, 54 (2), 233-246.
14. Hay, D.L.; Walker, C.S.; Poyner, D.R. Adrenomedullin and calcitonin gene-related peptide receptors in endocrine-related cancers: opportunities and challenges. Endocr. Relat. Cancer, 2011, 18 (1), C1-14.
15. Kuwasako, K.; Cao, Y.N.; Nagoshi, Y.; Kitamura, K.; Eto, T. Adrenomedullin receptors: pharmacological features and possible pathophysiological roles. Peptides, 2004, 25 (11), 2003-2012.
16. Smillie, S.J.; Brain, S.D. Calcitonin gene-related peptide (CGRP) and its role in hypertension. Neuropeptides, 2011, 45 (2), 93-104.
17. Ejaz, A.; LoGerfo, F.W.; Pradhan, L. Diabetic neuropathy and heart failure: role of neuropeptides. Expert rev. Mol. Med., 2011, 13, e26.
18. Kuwasako, K.; Kitamura, K.; Nagata, S.; Hikosaka, T.; Takei, Y.; Kato, J. Shared and separate functions of the RAMP-based adrenomedullin receptors. Peptides, 2011.
19. Gibbons, C.; Dackor, R.; Dunworth, W.; Fritz-Six, K.; Caron, K.M. Receptor activity-modifying proteins: RAMPing up adrenomedullin signaling. Mol. Endocrinol., 2007, 21 (4), 783-796.
20. Standfuss, J.; Edwards, P.C.; D'Antona, A.; Fransen, M.; Xie, G.; Oprian, D.D.; Schertler, G.F. The structural basis of agonistinduced activation in constitutively active rhodopsin. Nature, 2011, 471 (7340), 656-660.
21. Simpson, L.M.; Wall, I.D.; Blaney, F.E.; Reynolds, C.A. Modeling GPCR active state conformations: the beta(2)-adrenergic receptor. Proteins, 2011, 79 (5), 1441-1457.
22. Topiol, S.; Sabio, M. X-ray structure breakthroughs in the GPCR transmembrane region. Biochem. Pharmacol., 2009, 78 (1), 11-20.
23. Wess, J.; Han, S.J.; Kim, S.K.; Jacobson, K.A.; Li, J.H. Conformational changes involved in G-protein-coupled-receptor activation. Trends Pharmacol. Sci., 2008, 29 (12), 616-625.
24. Mustafi, D.; Palczewski, K. Topology of class A G protein-coupled receptors: insights gained from crystal structures of rhodopsins, adrenergic and adenosine receptors. Mol. Pharmacol., 2009, 75 (1), 1-12.
25. Langer, I. Conformational switches in the VPAC(1) receptor. Br. J. Pharmacol., 2012, 166 (1), 79-84.
26. Conner, A.C.; Hay, D.L.; Simms, J.; Howitt, S.G.; Schindler, M.; Smith, D.M.; Wheatley, M.; Poyner, D.R. A key role for transmembrane prolines in calcitonin receptor-like receptor agonist binding and signalling: implications for family B G-proteincoupled receptors. Mol. Pharmaco.l, 2005, 67 (1), 20-31.
27. Chugunov, A.O.; Simms, J.; Poyner, D.R.; Dehouck, Y.; Rooman, M.; Gilis, D.; Langer, I. Evidence that interaction between conserved residues in transmembrane helices 2, 3, and 7 are crucial for human VPAC1 receptor activation. Mol. Pharmacol., 2010, 78 (3), 394-401.
28. Conner, A.C.; Simms, J.; Barwell, J.; Wheatley, M.; Poyner, D.R. Ligand binding and activation of the CGRP receptor. Biochem Soc Trans, 2007, 35 (Pt 4), 729-732.
29. Kuwasako, K.; Kitamura, K.; Nagata, S.; Hikosaka, T.; Kato, J. Structure-function analysis of helix 8 of human calcitonin receptorlike receptor within the adrenomedullin 1 receptor. Peptides, 2011, 32 (1), 144-149.
30. Kuwasako, K.; Kitamura, K.; Nagata, S.; Hikosaka, T.; Kato, J. Function of the cytoplasmic tail of human calcitonin receptor-like receptor in complex with receptor activity-modifying protein 2. Biochem. Biophys. Res. Commun., 2010, 392 (3), 380-385.
31. Conner, M.; Hicks, M.R.; Dafforn, T.; Knowles, T.J.; Ludwig, C.; Staddon, S.; Overduin, M.; Gunther, U.L.; Thome, J.; Wheatley, M.; Poyner, D.R.; Conner, A.C. Functional and biophysical analysis of the C-terminus of the CGRP-receptor; a family B GPCR. Biochemistry, 2008, 47 (32), 8434-8444.
32. Perrin, M.H.; Grace, C.R.; Riek, R.; Vale, W.W. The threedimensional structure of the N-terminal domain of corticotropinreleasing factor receptors: sushi domains and the B1 family of G protein-coupled receptors. Ann. N. Y. Acad. Sci., 2006, 1070, 105-119.
33. Grace, C.R.; Perrin, M.H.; Gulyas, J.; Digruccio, M.R.; Cantle, J.P.; Rivier, J.E.; Vale, W.W.; Riek, R. Structure of the N-terminal domain of a type B1 G protein-coupled receptor in complex with a peptide ligand. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104 (12), 4858-4863.
34. Grace, C.R.; Perrin, M.H.; DiGruccio, M.R.; Miller, C.L.; Rivier, J.E.; Vale, W.W.; Riek, R. NMR structure and peptide hormone binding site of the first extracellular domain of a type B1 G proteincoupled receptor. Proc. Natl. Acad. Sci. U.S.A., 2004, 101 (35), 12836-12841.
35. Siu, F.Y.; Stevens, R.C. RAMP-ing up class-B GPCR ECD structural coverage. Structure, 2010, 18 (9), 1067-1068.
36. Neumann, J.M.; Couvineau, A.; Murail, S.; Lacapere, J.J.; Jamin, N.; Laburthe, M. Class-B GPCR activation: is ligand helix-capping the key? Trends Biochem. Sci., 2008, 33 (7), 314-319.
37. Hoare, S.R. Mechanisms of peptide and nonpeptide ligand binding to Class B G-protein-coupled receptors. Drug discov. today, 2005, 10 (6), 417-427.
38. Pioszak, A.A.; Xu, H.E. Molecular recognition of parathyroid hormone by its G protein-coupled receptor. Proc. Natl. Acad. Sci. U.S.A., 2008, 105 (13), 5034-5039.
39. Runge, S.; Thogersen, H.; Madsen, K.; Lau, J.; Rudolph, R. Crystal structure of the ligand-bound glucagon-like peptide-1 receptor extracellular domain. J. Biol. Chem., 2008, 283 (17), 11340-11347.
40. Parthier, C.; Kleinschmidt, M.; Neumann, P.; Rudolph, R.; Manhart, S.; Schlenzig, D.; Fanghanel, J.; Rahfeld, J.U.; Demuth, H.U.; Stubbs, M.T. Crystal structure of the incretin-bound extracellular domain of a G protein-coupled receptor. Proc. Nat. Acad. Sci. USA., 2007, 104 (35), 13942-13947.
41. Grace, C.R.; Perrin, M.H.; Gulyas, J.; Rivier, J.E.; Vale, W.W.; Riek, R. NMR structure of the first extracellular domain of corticotropin-releasing factor receptor 1 (ECD1-CRF-R1) complexed with a high affinity agonist. J. Biol. Chem., 2010, 285 (49), 38580-38589.
42. Sun, C.; Song, D.; Davis-Taber, R.A.; Barrett, L.W.; Scott, V.E.; Richardson, P.L.; Pereda-Lopez, A.; Uchic, M.E.; Solomon, L.R.; Lake, M.R.; Walter, K.A.; Hajduk, P.J.; Olejniczak, E.T. Solution structure and mutational analysis of pituitary adenylate cyclaseactivating polypeptide binding to the extracellular domain of PAC1-RS. Proc. Nat. Acad. Sci. USA., 2007, 104 (19), 7875-7880.
43. Kusano, S.; Kukimoto-Niino, M.; Hino, N.; Ohsawa, N.; Okuda, K.; Sakamoto, K.; Shirouzu, M.; Shindo, T.; Yokoyama, S. Structural basis for extracellular interactions between calcitonin receptor-like receptor and receptor activity-modifying protein 2 for adrenomedullin-specific binding. Protein science: a publication of the Protein Society, 2012, 21 (2), 199-210.
44. Bisello, A.; Manen, D.; Pierroz, D.D.; Usdin, T.B.; Rizzoli, R.; Ferrari, S.L. Agonist-specific regulation of parathyroid hormone (PTH) receptor type 2 activity: structural and functional analysis of PTH-and tuberoinfundibular peptide (TIP) 39-stimulated desensitization and internalization. Mol. Endocrinol., 2004, 18 (6), 1486-1498.
45. Garrido, J.L.; Wheeler, D.; Vega, L.L.; Friedman, P.A.; Romero, G. Role of phospholipase D in parathyroid hormone type 1 receptor signaling and trafficking. Mol. Endocrinol., 2009, 23 (12), 2048-2059.
46. Langlet, C.; Langer, I.; Vertongen, P.; Gaspard, N.; Vanderwinden, J.M.; Robberecht, P. Contribution of the carboxyl terminus of the VPAC1 receptor to agonist-induced receptor phosphorylation, internalization, and recycling. J. Biol. Chem., 2005, 280 (30), 28034-28043.
47. Marie, J.C.; Rouyer-Fessard, C.; Couvineau, A.; Nicole, P.; Devaud, H.; El Benna, J.; Laburthe, M. Serine 447 in the carboxyl tail of human VPAC1 receptor is crucial for agonist-induced desensitization but not internalization of the receptor. Mol.Pharmacol., 2003, 64 (6), 1565-1574.
48. Seck, T.; Baron, R.; Horne, W.C. Binding of filamin to the Cterminal tail of the calcitonin receptor controls recycling. J. Biol. Chem., 2003, 278 (12), 10408-10416.
49. Hilairet, S.; Belanger, C.; Bertrand, J.; Laperriere, A.; Foord, S.M.; Bouvier, M. Agonist-promoted internalization of a ternary complex between calcitonin receptor-like receptor, receptor activitymodifying protein 1 (RAMP1), and beta-arrestin. J. Biol. Chem., 2001, 276 (45), 42182-42190.
50. Kuwasako, K.; Shimekake, Y.; Masuda, M.; Nakahara, K.; Yoshida, T.; Kitaura, M.; Kitamura, K.; Eto, T.; Sakata, T. Visualization of the calcitonin receptor-like receptor and its receptor activity-modifying proteins during internalization and recycling. J. Biol. Chem., 2000, 275 (38), 29602-29609.
51. Kuwasako, K.; Cao, Y.N.; Chu, C.P.; Iwatsubo, S.; Eto, T.; Kitamura, K. Functions of the cytoplasmic tails of the human receptor activity-modifying protein components of calcitonin generelated peptide and adrenomedullin receptors. J. Biol. Chem., 2006, 281 (11), 7205-7213.
52. Ribas, C.; Penela, P.; Murga, C.; Salcedo, A.; Garcia-Hoz, C.; Jurado-Pueyo, M.; Aymerich, I.; Mayor, F., Jr. The G proteincoupled receptor kinase (GRK) interactome: role of GRKs in GPCR regulation and signaling. Biochim. Biophys. Acta, 2007, 1768 (4), 913-922.
53. Gurevich, E.V.; Tesmer, J.J.; Mushegian, A.; Gurevich, V.V. G protein-coupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol. Ther., 2012, 133 (1), 40-69.
54. Premont, R.T.; Gainetdinov, R.R. Physiological roles of G proteincoupled receptor kinases and arrestins. Ann.l Rev. Physiolo., 2007, 69, 511-534.
55. Sexton, P.M.; Albiston, A.; Morfis, M.; Tilakaratne, N. Receptor activity modifying proteins. Cell Signal, 2001, 13 (2), 73-83.
56. Hay, D.L.; Poyner, D.R.; Sexton, P.M. GPCR modulation by RAMPs. Pharmacol. Ther, 2006, 109 (1-2), 173-197.
57. ter Haar, E.; Koth, C.M.; Abdul-Manan, N.; Swenson, L.; Coll, J.T.; Lippke, J.A.; Lepre, C.A.; Garcia-Guzman, M.; Moore, J.M. Crystal structure of the ectodomain complex of the CGRP receptor, a class-B GPCR, reveals the site of drug antagonism. Structure, 2010, 18 (9), 1083-1093.
58. Kusano, S.; Kukimoto-Niino, M.; Akasaka, R.; Toyama, M.; Terada, T.; Shirouzu, M.; Shindo, T.; Yokoyama, S. Crystal structure of the human receptor activity-modifying protein 1 extracellular domain. Protein Sci., 2008, 17 (11), 1907-1914.
59. Steiner, S.; Born, W.; Fischer, J.A.; Muff, R. The function of conserved cysteine residues in the extracellular domain of human receptor-activity-modifying protein. FEBS Lett., 2003, 555 (2), 285-290.
60. Simms, J.; Hay, D.L.; Wheatley, M.; Poyner, D.R. Characterization of the structure of RAMP1 by mutagenesis and molecular modeling. Biophys. J., 2006, 91 (2), 662-669.
61. Simms, J.; Hay, D.L.; Bailey, R.J.; Konycheva, G.; Bailey, G.; Wheatley, M.; Poyner, D.R. Structure-function analysis of RAMP1 by alanine mutagenesis. Biochemistry, 2009, 48 (1), 198-205.
62. Kuwasako, K.; Kitamura, K.; Uemura, T.; Nagoshi, Y.; Kato, J.; Eto, T. The function of extracellular cysteines in the human adrenomedullin receptor. Hypertens. Res., 2003, 26 Suppl, S25-31.
63. Qi, T.; Hay, D.L. Structure-function relationships of the Nterminus of receptor activity-modifying proteins. Br. J. Pharmacol., 2010, 159 (5), 1059-1068.
64. Hilairet, S.; Foord, S.M.; Marshall, F.H.; Bouvier, M. Proteinprotein interaction and not glycosylation determines the binding selectivity of heterodimers between the calcitonin receptor-like receptor and the receptor activity-modifying proteins. J. Biol. Chem., 2001, 276 (31), 29575-29581.
65. Heroux, M.; Breton, B.; Hogue, M.; Bouvier, M. Assembly and signaling of CRLR and RAMP1 complexes assessed by BRET. Biochemistry, 2007, 46 (23), 7022-7033.
66. Heroux, M.; Hogue, M.; Lemieux, S.; Bouvier, M. Functional calcitonin gene-related peptide receptors are formed by the asymmetric assembly of a calcitonin receptor-like receptor homooligomer and a monomer of receptor activity-modifying protein-1. J. Biol. Chem., 2007, 282 (43), 31610-31620.
67. Kuwasako, K.; Kitamura, K.; Nagata, S.; Kato, J. Flow cytometric analysis of the calcitonin receptor-like receptor domains responsible for cell-surface translocation of receptor activitymodifying proteins. Biochem. Biophys. Res. Commun., 2009, 384 (2), 249-254.
68. Qi, T.; Ly, K.; Poyner, D.R.; Christopoulos, G.; Sexton, P.M.; Hay, D.L. Structure-function analysis of amino acid 74 of human RAMP1 and RAMP3 and its role in peptide interactions with adrenomedullin and calcitonin gene-related peptide receptors. Peptides, 2011, 32 (5), 1060-1067.
69. Tilakaratne, N.; Christopoulos, G.; Zumpe, E.T.; Foord, S.M.; Sexton, P.M. Amylin receptor phenotypes derived from human calcitonin receptor/RAMP coexpression exhibit pharmacological differences dependent on receptor isoform and host cell environment. J. pharmacol. exp. ther., 2000, 294 (1), 61-72.
70. Kuwasako, K.; Cao, Y.N.; Nagoshi, Y.; Tsuruda, T.; Kitamura, K.; Eto, T. Characterization of the human calcitonin gene-related peptide receptor subtypes associated with receptor activitymodifying proteins. Mol. Pharmacol., 2004, 65 (1), 207-213.
71. Morfis, M.; Tilakaratne, N.; Furness, S.G.; Christopoulos, G.; Werry, T.D.; Christopoulos, A.; Sexton, P.M. Receptor activitymodifying proteins differentially modulate the G protein-coupling efficiency of amylin receptors. Endocrinology, 2008, 149 (11), 5423-5431.
72. Rasmussen, S.G.; DeVree, B.T.; Zou, Y.; Kruse, A.C.; Chung, K.Y.; Kobilka, T.S.; Thian, F.S.; Chae, P.S.; Pardon, E.; Calinski, D.; Mathiesen, J.M.; Shah, S.T.; Lyons, J.A.; Caffrey, M.; Gellman, S.H.; Steyaert, J.; Skiniotis, G.; Weis, W.I.; Sunahara, R.K.; Kobilka, B.K. Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature, 2011, 477 (7366), 549-555.
73. Oldham, W.M.; Hamm, H.E. Heterotrimeric G protein activation by G-protein-coupled receptors. Nature reviews. Mol. cell biol., 2008, 9 (1), 60-71.
74. Hofmann, K.P.; Scheerer, P.; Hildebrand, P.W.; Choe, H.W.; Park, J.H.; Heck, M.; Ernst, O.P. A G protein-coupled receptor at work: the rhodopsin model. Trends Biochem. Sci., 2009, 34 (11), 540-552.
75. Choe, H.W.; Kim, Y.J.; Park, J.H.; Morizumi, T.; Pai, E.F.; Krauss, N.; Hofmann, K.P.; Scheerer, P.; Ernst, O.P. Crystal structure of metarhodopsin II. Nature, 2011, 471 (7340), 651-655.
76. Wheatley, M.; Wootten, D.; Conner, M.T.; Simms, J.; Kendrick, R.; Logan, R.T.; Poyner, D.R.; Barwell, J. Lifting the lid on GPCRs: the role of extracellular loops. Br. J. Pharmacol., 2012, 165 (6), 1688-1703.
77. Peeters, M.C.; van Westen, G.J.; Li, Q.; Ijzerman, A.P. Importance of the extracellular loops in G protein-coupled receptors for ligand recognition and receptor activation. Trends Pharmacol. Sci., 2011, 32 (1), 35-42.
78. Hawtin, S.R.; Simms, J.; Conner, M.; Lawson, Z.; Parslow, R.A.; Trim, J.; Sheppard, A.; Wheatley, M. Charged extracellular residues, conserved throughout a G-protein-coupled receptor family, are required for ligand binding, receptor activation, and cell-surface expression. J. Biol. Chem., 2006, 281 (50), 38478-38488.
79. Lawson, Z.; Wheatley, M. The third extracellular loop of Gprotein-coupled receptors: more than just a linker between two important transmembrane helices. Biochem. Soc. Trans., 2004, 32 (Pt 6), 1048-1050.
80. Li, J.; Edwards, P.C.; Burghammer, M.; Villa, C.; Schertler, G.F. Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol., 2004, 343 (5), 1409-1438.
81. Palczewski, K.; Kumasaka, T.; Hori, T.; Behnke, C.A.; Motoshima, H.; Fox, B.A.; Le Trong, I.; Teller, D.C.; Okada, T.; Stenkamp, R.E.; Yamamoto, M.; Miyano, M. Crystal structure of rhodopsin: A G protein-coupled receptor. Science, 2000, 289 (5480), 739-745.
82. Barwell, J.; Conner, A.; Poyner, D.R. Extracellular loops 1 and 3 and their associated transmembrane regions of the calcitonin receptor-like receptor are needed for CGRP receptor function. Biochim. biophys. acta, 2011, 1813 (10), 1906-1916.
83. Kuwasako, K.; Hay, D.L.; Nagata, S.; Hikosaka, T.; Kitamura, K.; Kato, J. The third extracellular loop of the human calcitonin receptor-like receptor is crucial for the activation of adrenomedullin signalling. Br. J. Pharmacol., 2012, 166 (1), 137-150.
84. Qi, T.; Christopoulos, G.; Bailey, R.J.; Christopoulos, A.; Sexton, P.M.; Hay, D.L. Identification of N-terminal receptor activitymodifying protein residues important for calcitonin gene-related peptide, adrenomedullin, and amylin receptor function. Mol. Pharmacol., 2008, 74 (4), 1059-1071.
85. Faussner, A.; Bauer, A.; Kalatskaya, I.; Schussler, S.; Seidl, C.; Proud, D.; Jochum, M. The role of helix 8 and of the cytosolic Ctermini in the internalization and signal transduction of B(1) and B(2) bradykinin receptors. The FEBS journal, 2005, 272 (1), 129-140.
86. Wess, J.; Han, S.J.; Kim, S.K.; Jacobson, K.A.; Li, J.H. Conformational changes involved in G-protein-coupled-receptor activation. Trends in Pharmacological Sciences, 2008, 29 (12), 616-625.
87. Tetsuka, M.; Saito, Y.; Imai, K.; Doi, H.; Maruyama, K. The basic residues in the membrane-proximal C-terminal tail of the rat melanin-concentrating hormone receptor 1 are required for receptor function. Endocrinology, 2004, 145 (8), 3712-3723.
88. Swift, S.; Leger, A.J.; Talavera, J.; Zhang, L.; Bohm, A.; Kuliopulos, A. Role of the PAR1 receptor 8th helix in signaling: the 7-8-1 receptor activation mechanism. J. Biol. Chem,. 2006, 281 (7), 4109-4116.
89. Sano, T.; Ohyama, K.; Yamano, Y.; Nakagomi, Y.; Nakazawa, S.; Kikyo, M.; Shirai, H.; Blank, J.S.; Exton, J.H.; Inagami, T. A domain for G protein coupling in carboxyl-terminal tail of rat angiotensin II receptor type 1A. J. Biol. Chem., 1997, 272 (38), 23631-23636.
90. Delos Santos, N.M.; Gardner, L.A.; White, S.W.; Bahouth, S.W. Characterization of the residues in helix 8 of the human beta1-adrenergic receptor that are involved in coupling the receptor to G proteins. J. Biol. Chem., 2006, 281 (18), 12896-12907.
91. Zhao, M.M.; Gaivin, R.J.; Perez, D.M. The third extracellular loop of the beta2-adrenergic receptor can modulate receptor/G protein affinity. Mol. pharmacol., 1998, 53 (3), 524-529.
92. Couvineau, A.; Lacapere, J.J.; Tan, Y.V.; Rouyer-Fessard, C.; Nicole, P.; Laburthe, M. Identification of cytoplasmic domains of hVPAC1 receptor required for activation of adenylyl cyclase. Crucial role of two charged amino acids strictly conserved in class II G protein-coupled receptors. J. Biol. Chem., 2003, 278 (27), 24759-24766.
93. Findlay, D.M.; Houssami, S.; Lin, H.Y.; Myers, D.E.; Brady, C.L.; Darcy, P.K.; Ikeda, K.; Martin, T.J.; Sexton, P.M. Truncation of the porcine calcitonin receptor cytoplasmic tail inhibits internalization and signal transduction but increases receptor affinity. Mole. Endocrinol., 1994, 8 (12), 1691-1700.
94. Unson, C.G.; Cypess, A.M.; Kim, H.N.; Goldsmith, P.K.; Carruthers, C.J.; Merrifield, R.B.; Sakmar, T.P. Characterization of deletion and truncation mutants of the rat glucagon receptor. Seven transmembrane segments are necessary for receptor transport to the plasma membrane and glucagon binding. J. Biol. Chem., 1995, 270 (46), 27720-27727.
95. Huang, Z.; Chen, Y.; Pratt, S.; Chen, T.H.; Bambino, T.; Shoback, D.M.; Nissenson, R.A. Mutational analysis of the cytoplasmic tail of the G protein-coupled receptor for parathyroid hormone (PTH) and PTH-related protein: effects on receptor expression and signaling. Mol.Endocrinol., 1995, 9 (9), 1240-1249.
96. Holtmann, M.H.; Roettger, B.F.; Pinon, D.I.; Miller, L.J. Role of receptor phosphorylation in desensitization and internalization of the secretin receptor. J. Biol. Chem., 1996, 271 (38), 23566-23571.
97. Krilov, L.; Nguyen, A.; Miyazaki, T.; Unson, C.G.; Williams, R.; Lee, N.H.; Ceryak, S.; Bouscarel, B. Dual mode of glucagon receptor internalization: role of PKCalpha, GRKs and betaarrestins. Experimental Cell Research, 2011, 317 (20), 2981-2994.
98. Kelly, E.; Bailey, C.P.; Henderson, G. Agonist-selective mechanisms of GPCR desensitization. Br. J. Pharmacol., 2008, 153 Suppl 1, S379-388.
99. Pitcher, J.A.; Freedman, N.J.; Lefkowitz, R.J. G protein-coupled receptor kinases. Ann. Rev. Biochem., 1998, 67, 653-692.
100. Platta, H.W.; Stenmark, H. Endocytosis and signaling. Current Opinion in Cell Biology, 2011, 23 (4), 393-403.
101. Jean-Alphonse, F.; Hanyaloglu, A.C. Regulation of GPCR signal networks via membrane trafficking. Mol. Cell. Endocrinol., 2011, 331 (2), 205-214.
102. Drake, M.T.; Shenoy, S.K.; Lefkowitz, R.J. Trafficking of G protein-coupled receptors. Cir. Res., 2006, 99 (6), 570-582.
103. Sever, S. Dynamin and endocytosis. Curr. Opin. Cell Biol., 2002, 14 (4), 463-467.
104. Prossnitz, E.R. Novel roles for arrestins in the post-endocytic trafficking of G protein-coupled receptors. Life Sci., 2004, 75 (8), 893-899.
105. Oakley, R.H.; Laporte, S.A.; Holt, J.A.; Caron, M.G.; Barak, L.S. Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J. Biol. Chem., 2000, 275 (22), 17201-17210.
106. Mundell, S.J.; Kelly, E. The effect of inhibitors of receptor internalization on the desensitization and resensitization of three Gs-coupled receptor responses. Br. J. Pharmacol., 1998, 125 (7), 1594-1600.
107. Krilov, L.; Nguyen, A.; Miyazaki, T.; Unson, C.G.; Bouscarel, B. Glucagon receptor recycling: role of carboxyl terminus, betaarrestins, and cytoskeleton. American journal of physiology. Cell physiol., 2008, 295 (5), C1230-1237.
108. Wang, B.; Bisello, A.; Yang, Y.; Romero, G.G.; Friedman, P.A. NHERF1 regulates parathyroid hormone receptor membrane retention without affecting recycling. J. Biol. Chem., 2007, 282 (50), 36214-36222.
109. Bomberger, J.M.; Parameswaran, N.; Hall, C.S.; Aiyar, N.; Spielman, W.S. Novel function for receptor activity-modifying proteins (RAMPs) in post-endocytic receptor trafficking. J. Biol. Chem., 2005, 280 (10), 9297-9307.
110. Nikitenko, L.L.; Blucher, N.; Fox, S.B.; Bicknell, R.; Smith, D.M.; Rees, M.C. Adrenomedullin and CGRP interact with endogenous calcitonin-receptor-like receptor in endothelial cells and induce its desensitisation by different mechanisms. J. Cell Sc.i, 2006, 119 (Pt 5), 910-922.
111. Cottrell, G.S.; Padilla, B.; Pikios, S.; Roosterman, D.; Steinhoff, M.; Grady, E.F.; Bunnett, N.W. Post-endocytic sorting of calcitonin receptor-like receptor and receptor activity-modifying protein 1. J. Biol. Chem., 2007, 282 (16), 12260-12271.
112. Shetzline, M.A.; Walker, J.K.; Valenzano, K.J.; Premont, R.T. Vasoactive intestinal polypeptide type-1 receptor regulation. Desensitization, phosphorylation, and sequestration. J. Biol. Chem., 2002, 277 (28), 25519-25526.
113. Ferrari, S.L.; Behar, V.; Chorev, M.; Rosenblatt, M.; Bisello, A. Endocytosis of ligand-human parathyroid hormone receptor 1 complexes is protein kinase C-dependent and involves betaarrestin2. Real-time monitoring by fluorescence microscopy. J. Biol. Chem., 1999, 274 (42), 29968-29975.
114. Walker, J.K.; Premont, R.T.; Barak, L.S.; Caron, M.G.; Shetzline, M.A. Properties of secretin receptor internalization differ from those of the beta(2)-adrenergic receptor. J. Biol. Chem., 1999, 274 (44), 31515-31523.
115. Zhang, M.; Breitwieser, G.E. High affinity interaction with filamin A protects against calcium-sensing receptor degradation. J. Biol. Chem., 2005, 280 (12), 11140-11146.
116. Lin, R.; Karpa, K.; Kabbani, N.; Goldman-Rakic, P.; Levenson, R. Dopamine D2 and D3 receptors are linked to the actin cytoskeleton via interaction with filamin A. Proc. Natl. Acad. Sci. U. S. A., 2001, 98 (9), 5258-5263.
117. Bomberger, J.M.; Spielman, W.S.; Hall, C.S.; Weinman, E.J.; Parameswaran, N. Receptor activity-modifying protein (RAMP) isoform-specific regulation of adrenomedullin receptor trafficking by NHERF-1. J. Biol. Chem., 2005, 280 (25), 23926-23935.
118. Wojcikiewicz, R.J. Regulated ubiquitination of proteins in GPCRinitiated signaling pathways. Trends in Pharmacological Sciences, 2004, 25 (1), 35-41.
119. Kuwasako, K.; Kitamura, K.; Nagata, S.; Nozaki, N.; Kato, J. Characterization of the single transmembrane domain of human receptor activity-modifying protein 3 in adrenomedullin receptor internalization. Biochem. Biophys. Res.Commu.,2012, 420 (3), 582-587.
120. Gainetdinov, R.R.; Premont, R.T.; Caron, M.G.; Lefkowitz, R.J. Reply: receptor specificity of G-protein-coupled receptor kinases. Trends Pharmacol. Sci., 2000, 21 (10), 366-367.
121. Ghadessy, R.S.; Willets, J.M.; Kelly, E. G protein-coupled receptor kinase 6 (GRK6) selectively regulates endogenous secretin receptor responsiveness in NG108-15 cells. Br. J. Pharmacol., 2003, 138 (4), 660-670.
122. Shetzline, M.A.; Premont, R.T.; Walker, J.K.; Vigna, S.R.; Caron, M.G. A role for receptor kinases in the regulation of class II G protein-coupled receptors. Phosphorylation and desensitization of the secretin receptor. J. Biol. Chem, 1998, 273 (12), 6756-6762.
123. Flannery, P.J.; Spurney, R.F. Domains of the parathyroid hormone (PTH) receptor required for regulation by G protein-coupled receptor kinases (GRKs). Biochem.Pharmacol., 2001, 62 (8), 1047-1058.
124. Aiyar, N.; Disa, J.; Dang, K.; Pronin, A.N.; Benovic, J.L.; Nambi, P. Involvement of G protein-coupled receptor kinase-6 in desensitization of CGRP receptors. Eur. J. Pharmacol., 2000, 403 (1-2), 1-7.
125. Horie, K.; Insel, P.A. Retrovirally mediated transfer of a G proteincoupled receptor kinase (GRK) dominant-negative mutant enhances endogenous calcitonin receptor signaling in Chinese hamster ovary cells. GRK inhibition enhances expression of receptors and receptor mRNA. J. Biol. Chem, 2000, 275 (38), 29433-29440.
126. Harris, D.M.; Cohn, H.I.; Pesant, S.; Eckhart, A.D. GPCR signalling in hypertension: role of GRKs. Clin. Sci., 2008, 115 (3), 79-89.
127. Kuwasako, K.; Kitamura, K.; Nagata, S.; Kato, J. Molecular Basis of Adrenomedullin 1 Receptor Function and Its Roles in the Cardiovascular System. Curr. Hyperten. Rev., 2011, 7 (4), 207-216.
128. Sawmiller, D.R.; Henning, R.J.; Cuevas, J.; Dehaven, W.I.; Vesely, D.L. Coronary vascular effects of vasoactive intestinal peptide in the isolated perfused rat heart. Neuropeptides, 2004, 38 (5), 289-297.
129. Dvorakova, M.C. Cardioprotective role of the VIP signaling system. Drug news Perspect., 2005, 18 (6), 387-391.
130. Thal, D.M.; Yeow, R.Y.; Schoenau, C.; Huber, J.; Tesmer, J.J. Molecular mechanism of selectivity among G protein-coupled receptor kinase 2 inhibitors. Mol.Pharmacol., 2011, 80 (2), 294-303.