Receptor Activity-Modifying Proteins (RAMPs): New Insights and Roles

Literature Cited

1. Hay DL, Poyner DR, Sexton PM. 1.  2006. GPCR modulation by RAMPs. Pharmacol. Ther. 109:173–97 [Google Scholar]
2. McLatchie LM, Fraser NJ, Main MJ, Wise A, Brown J. 2.  et al. 1998. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393:333–39 [Google Scholar]
3. Garland SL. 3.  2013. Are GPCRs still a source of new targets?. J. Biomol. Screen. 18:947–66 [Google Scholar]
4. Poyner DR, Sexton PM, Marshall I, Smith DM, Quirion R. 4.  et al. 2002. International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol. Rev. 54:233–46 [Google Scholar]
5. Christopoulos A, Christopoulos G, Morfis M, Udawela M, Laburthe M. 5.  et al. 2003. Novel receptor partners and function of receptor activity-modifying proteins. J. Biol. Chem. 278:3293–97 [Google Scholar]
6. Wootten D, Lindmark H, Kadmiel M, Willcockson H, Caron KM. 6.  et al. 2013. Receptor activity modifying proteins (RAMPs) interact with the VPAC2 receptor and CRF1 receptors and modulate their function. Br. J. Pharmacol. 168:822–34 [Google Scholar]
7. Steiner S, Muff R, Gujer R, Fischer JA, Born W. 7.  2002. The transmembrane domain of receptor-activity-modifying protein 1 is essential for the functional expression of a calcitonin gene-related peptide receptor. Biochemistry 41:11398–404 [Google Scholar]
8. Bomberger JM, Parameswaran N, Hall CS, Aiyar N, Spielman WS. 8.  2005. Novel function for receptor activity-modifying proteins (RAMPs) in post-endocytic receptor trafficking. J. Biol. Chem. 280:9297–307 [Google Scholar]
9. Bomberger JM, Spielman WS, Hall CS, Weinman EJ, Parameswaran N. 9.  2005. Receptor activity-modifying protein (RAMP) isoform-specific regulation of adrenomedullin receptor trafficking by NHERF-1. J. Biol. Chem. 280:23926–35 [Google Scholar]
10. Udawela M, Christopoulos G, Morfis M, Christopoulos A, Ye S. 10.  et al. 2006. A critical role for the short intracellular C terminus in receptor activity-modifying protein function. Mol. Pharmacol. 70:1750–60 [Google Scholar]
11. Udawela M, Christopoulos G, Morfis M, Tilakaratne N, Christopoulos A, Sexton PM. 11.  2008. The effects of C-terminal truncation of receptor activity modifying proteins on the induction of amylin receptor phenotype from human CTb receptors. Regul. Pept. 145:65–71 [Google Scholar]
12. Parameswaran N, Spielman W. 12.  2012. Introduction to RAMPs. RAMPs W Spielman, N Parameswaran 1–11 Adv. Exp. Med. Biol. 744. New York: Springer [Google Scholar]
13. Parameswaran N, Spielman WS. 13.  2006. RAMPs: the past, present and future. Trends Biochem. Sci. 31:631–38 [Google Scholar]
14. Nishikimi T, Yoshihara F, Kanazawa A, Okano I, Horio T. 14.  et al. 2001. Role of increased circulating and renal adrenomedullin in rats with malignant hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R2079–87 [Google Scholar]
15. Udawela M, Hay DL, Sexton PM. 15.  2004. The receptor activity modifying protein family of G protein coupled receptor accessory proteins. Semin. Cell Dev. Biol. 15:299–308 [Google Scholar]
16. Buhlmann N, Leuthauser K, Muff R, Fischer JA, Born W. 16.  1999. A receptor activity modifying protein (RAMP)2-dependent adrenomedullin receptor is a calcitonin gene-related peptide receptor when coexpressed with human RAMP1. Endocrinology 140:2883–90 [Google Scholar]
17. Marchalant Y, Brownjohn PW, Bonnet A, Kleffmann T, Ashton JC. 17.  2014. Validating antibodies to the cannabinoid CB2 receptor: Antibody sensitivity is not evidence of antibody specificity. J. Histochem. Cytochem. 62:395–404 [Google Scholar]
18. Gore AC. 18.  2013. Editorial: antibody validation requirements for articles published in Endocrinology. Endocrinology 154:579–80 [Google Scholar]
19. Zhao Y, Bell D, Smith LR, Zhao L, Devine AB. 19.  et al. 2006. Differential expression of components of the cardiomyocyte adrenomedullin/intermedin receptor system following blood pressure reduction in nitric oxide-deficient hypertension. J. Pharmacol. Exp. Ther. 316:1269–81 [Google Scholar]
20. Cueille C, Pidoux E, de Vernejoul M-C, Ventura-Clapier R, Garel J-M. 20.  2002. Increased myocardial expression of RAMP1 and RAMP3 in rats with chronic heart failure. Biochem. Biophys. Res. Commun. 294:340–46 [Google Scholar]
21. Eftekhari S, Salvatore CA, Calamari A, Kane SA, Tajti J, Edvinsson L. 21.  2010. Differential distribution of calcitonin gene-related peptide and its receptor components in the human trigeminal ganglion. Neuroscience 169:683–96 [Google Scholar]
22. Lennerz JK, Rühle V, Ceppa EP, Neuhuber WL, Bunnett NW. 22.  et al. 2008. Calcitonin receptor-like receptor (CLR), receptor activity-modifying protein 1 (RAMP1), and calcitonin gene-related peptide (CGRP) immunoreactivity in the rat trigeminovascular system: differences between peripheral and central CGRP receptor distribution. J. Comp. Neurol. 507:1277–99 [Google Scholar]
23. Walker CS, Eftekhari S, Bower RL, Wilderman A, Insel PA. 23.  et al. 2015. A second trigeminal CGRP receptor: function and expression of the AMY1 receptor. Ann. Clin. Transl. Neurol. 2:6595–608 [Google Scholar]
24. Morfis M, Tilakaratne N, Furness SGB, Christopoulos G, Werry TD. 24.  et al. 2008. Receptor activity-modifying proteins differentially modulate the G protein–coupling efficiency of amylin receptors. Endocrinology 149:5423–31 [Google Scholar]
25. Muller J-M, Debaigt C, Goursaud S, Montoni A, Pineau N. 25.  et al. 2007. Unconventional binding sites and receptors for VIP and related peptides PACAP and PHI/PHM: an update. Peptides 28:1655–66 [Google Scholar]
26. Desai AJ, Roberts DJ, Richards GO, Skerry TM. 26.  2014. Role of receptor activity modifying protein 1 in function of the calcium sensing receptor in the human TT thyroid carcinoma cell line. PLOS ONE 9:e85237 [Google Scholar]
27. Bouschet T, Martin S, Henley JM. 27.  2005. Receptor-activity-modifying proteins are required for forward trafficking of the calcium-sensing receptor to the plasma membrane. J. Cell Sci. 118:4709–20 [Google Scholar]
28. Lenhart PM, Broselid S, Barrick CJ, Leeb-Lundberg LMF, Caron KM. 28.  2013. G-protein-coupled receptor 30 interacts with receptor activity-modifying protein 3 and confers sex-dependent cardioprotection. J. Mol. Endocrinol. 51:191–202 [Google Scholar]
29. Ferré S, Casadó V, Devi LA, Filizola M, Jockers R. 29.  et al. 2014. G protein–coupled receptor oligomerization revisited: functional and pharmacological perspectives. Pharmacol. Rev. 66:413–34 [Google Scholar]
30. Kadmiel M, Fritz-Six KL, Caron KM. 30.  2012. Understanding RAMPs through genetically engineered mouse models. Adv. Exp. Med. Biol. 744:49–60 [Google Scholar]
31. Li M, Wetzel-Strong SE, Hua X, Tilley SL, Oswald E. 31.  et al. 2014. Deficiency of RAMP1 attenuates antigen-induced airway hyperresponsiveness in mice. PLOS ONE 9:e102356 [Google Scholar]
32. Kurashige C, Hosono K, Matsuda H, Tsujikawa K, Okamoto H, Majima M. 32.  2014. Roles of receptor activity-modifying protein 1 in angiogenesis and lymphangiogenesis during skin wound healing in mice. FASEB J. 28:1237–47 [Google Scholar]
33. Jusek G, Reim D, Tsujikawa K, Holzmann B. 33.  2012. Deficiency of the CGRP receptor component RAMP1 attenuates immunosuppression during the early phase of septic peritonitis. Immunobiology 217:761–67 [Google Scholar]
34. Dackor R, Fritz-Six K, Smithies O, Caron K. 34.  2007. Receptor activity-modifying proteins 2 and 3 have distinct physiological functions from embryogenesis to old age. J. Biol. Chem. 282:18094–99 [Google Scholar]
35. Yamauchi A, Sakurai T, Kamiyoshi A, Ichikawa-Shindo Y, Kawate H. 35.  et al. 2014. Functional differentiation of RAMP2 and RAMP3 in their regulation of the vascular system. J. Mol. Cell. Cardiol. 77:73–85 [Google Scholar]
36. Barrick CJ, Lenhart PM, Dackor RT, Nagle E, Caron KM. 36.  2012. Loss of receptor activity-modifying protein 3 exacerbates cardiac hypertrophy and transition to heart failure in a sex-dependent manner. J. Mol. Cell. Cardiol. 52:165–74 [Google Scholar]
37. Tsujikawa K, Yayama K, Hayashi T, Matsushita H, Yamaguchi T. 37.  et al. 2007. Hypertension and dysregulated proinflammatory cytokine production in receptor activity-modifying protein 1-deficient mice. PNAS 104:16702–7 [Google Scholar]
38. Mikami N, Sueda K, Ogitani Y, Otani I, Takatsuji M. 38.  et al. 2014. Calcitonin gene-related peptide regulates type IV hypersensitivity through dendritic cell functions. PLOS ONE 9:e86367 [Google Scholar]
39. Zhang Z, Liu X, Morgan DA, Kuburas A, Thedens DR. 39.  et al. 2011. Neuronal receptor activity-modifying protein 1 promotes energy expenditure in mice. Diabetes 60:1063–71 [Google Scholar]
40. Sabharwal R, Zhang Z, Lu Y, Abboud FM, Russo AF, Chapleau MW. 40.  2010. Receptor activity-modifying protein 1 increases baroreflex sensitivity and attenuates angiotensin-induced hypertension. Hypertension 55:627–35 [Google Scholar]
41. Zhang Z, Winborn CS, Marquez de Prado B, Russo AF. 41.  2007. Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J. Neurosci. 27:2693–703 [Google Scholar]
42. Hay DL, Chen S, Lutz TA, Parkes DG, Roth JD. 42.  2015. Amylin: pharmacology, physiology, and clinical potential. Pharmacol. Rev. 67:564–600 [Google Scholar]
43. Kadmiel M, Fritz-Six K, Pacharne S, Richards GO, Li M. 43.  et al. 2011. Research resource: Haploinsufficiency of receptor activity-modifying protein-2 (RAMP2) causes reduced fertility, hyperprolactinemia, skeletal abnormalities, and endocrine dysfunction in mice. Mol. Endocrinol. 25:1244–53 [Google Scholar]
44. Katritch V, Cherezov V, Stevens RC. 44.  2013. Structure-function of the G protein–coupled receptor superfamily. Annu. Rev. Pharmacol. Toxicol. 53:531–56 [Google Scholar]
45. Hollenstein K, de Graaf C, Bortolato A, Wang MW, Marshall FH, Stevens RC. 45.  2014. Insights into the structure of class B GPCRs. Trends Pharmacol. Sci. 35:12–22 [Google Scholar]
46. Hoare SR. 46.  2005. Mechanisms of peptide and nonpeptide ligand binding to Class B G-protein–coupled receptors. Drug Discov. Today 10:417–27 [Google Scholar]
47. Barwell J, Gingell JJ, Watkins HA, Archbold JK, Poyner DR, Hay DL. 47.  2012. Calcitonin and calcitonin receptor-like receptors: common themes with family B GPCRs?. Br. J. Pharmacol. 166:51–65 [Google Scholar]
48. Grace CR, Perrin MH, Gulyas J, Digruccio MR, Cantle JP. 48.  et al. 2007. Structure of the N-terminal domain of a type B1 G protein-coupled receptor in complex with a peptide ligand. PNAS 104:4858–63 [Google Scholar]
49. Grace CR, Perrin MH, Gulyas J, Rivier JE, Vale WW, Riek R. 49.  2010. 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. 285:38580–89 [Google Scholar]
50. Kumar S, Pioszak A, Zhang C, Swaminathan K, Xu HE. 50.  2011. Crystal structure of the PAC1R extracellular domain unifies a consensus fold for hormone recognition by class B G-protein coupled receptors. PLOS ONE 6:e19682 [Google Scholar]
51. Pal K, Swaminathan K, Xu HE, Pioszak AA. 51.  2010. Structural basis for hormone recognition by the human CRFR2α G protein–coupled receptor. J. Biol. Chem. 285:40351–61 [Google Scholar]
52. Parthier C, Kleinschmidt M, Neumann P, Rudolph R, Manhart S. 52.  et al. 2007. Crystal structure of the incretin-bound extracellular domain of a G protein–coupled receptor. PNAS 104:13942–47 [Google Scholar]
53. Pioszak AA, Harikumar KG, Parker NR, Miller LJ, Xu HE. 53.  2010. Dimeric arrangement of the parathyroid hormone receptor and a structural mechanism for ligand-induced dissociation. J. Biol. Chem. 285:12435–44 [Google Scholar]
54. Pioszak AA, Parker NR, Gardella TJ, Xu HE. 54.  2009. Structural basis for parathyroid hormone-related protein binding to the parathyroid hormone receptor and design of conformation-selective peptides. J. Biol. Chem. 284:28382–91 [Google Scholar]
55. Pioszak AA, Parker NR, Suino-Powell K, Xu HE. 55.  2008. Molecular recognition of corticotropin-releasing factor by its G-protein-coupled receptor CRFR1. J. Biol. Chem. 283:32900–12 [Google Scholar]
56. Pioszak AA, Xu HE. 56.  2008. Molecular recognition of parathyroid hormone by its G protein-coupled receptor. PNAS 105:5034–39 [Google Scholar]
57. Runge S, Thogersen H, Madsen K, Lau J, Rudolph R. 57.  2008. Crystal structure of the ligand-bound glucagon-like peptide-1 receptor extracellular domain. J. Biol. Chem. 283:11340–47 [Google Scholar]
58. Underwood CR, Garibay P, Knudsen LB, Hastrup S, Peters GH. 58.  et al. 2010. Crystal structure of glucagon-like peptide-1 in complex with the extracellular domain of the glucagon-like peptide-1 receptor. J. Biol. Chem. 285:723–30 [Google Scholar]
59. Hollenstein K, Kean J, Bortolato A, Cheng RK, Dore AS. 59.  et al. 2013. Structure of class B GPCR corticotropin-releasing factor receptor 1. Nature 499:438–43 [Google Scholar]
60. Siu FY, He M, de Graaf C, Han GW, Yang D. 60.  et al. 2013. Structure of the human glucagon class B G-protein-coupled receptor. Nature 499:444–49 [Google Scholar]
61. Fitzsimmons TJ, Zhao X, Wank SA. 61.  2003. The extracellular domain of receptor activity-modifying protein 1 is sufficient for calcitonin receptor-like receptor function. J. Biol. Chem. 278:14313–20 [Google Scholar]
62. Udawela M, Christopoulos G, Tilakaratne N, Christopoulos A, Albiston A, Sexton PM. 62.  2006. Distinct receptor activity-modifying protein domains differentially modulate interaction with calcitonin receptors. Mol. Pharmacol. 69:1984–89 [Google Scholar]
63. Koth CM, Abdul-Manan N, Lepre CA, Connolly PJ, Yoo S. 63.  et al. 2010. Refolding and characterization of a soluble ectodomain complex of the calcitonin gene-related peptide receptor. Biochemistry 49:1862–72 [Google Scholar]
64. ter Haar E, Koth CM, Abdul-Manan N, Swenson L, Coll JT. 64.  et al. 2010. Crystal structure of the ectodomain complex of the CGRP receptor, a class-B GPCR, reveals the site of drug antagonism. Structure 18:1083–93 [Google Scholar]
65. Kusano S, Kukimoto-Niino M, Hino N, Ohsawa N, Okuda K. 65.  et al. 2012. Structural basis for extracellular interactions between calcitonin receptor-like receptor and receptor activity-modifying protein 2 for adrenomedullin-specific binding. Protein Sci. 21:199–210 [Google Scholar]
66. Watkins HA, Au M, Bobby R, Archbold JK, Abdul-Manan N. 66.  et al. 2013. Identification of key residues involved in adrenomedullin binding to the AM1 receptor. Br. J. Pharmacol. 169:143–55 [Google Scholar]
67. Hill HE, Pioszak AA. 67.  2013. Bacterial expression and purification of a heterodimeric adrenomedullin receptor extracellular domain complex using DsbC-assisted disulfide shuffling. Protein Expr. Purif. 88:107–13 [Google Scholar]
68. Moad HE, Pioszak AA. 68.  2013. Selective CGRP and adrenomedullin peptide binding by tethered RAMP-calcitonin receptor-like receptor extracellular domain fusion proteins. Protein Sci. 22:1775–85 [Google Scholar]
69. Archbold JK, Flanagan JU, Watkins HA, Gingell JJ, Hay DL. 69.  2011. Structural insights into RAMP modification of secretin family G protein–coupled receptors: implications for drug development. Trends Pharmacol. Sci. 32:591–600 [Google Scholar]
70. Kusano S, Yokoyama S. 70.  2013. Ectodomain structures of the CGRP and AM receptors. Curr. Protein Peptide Sci. 14:375–85 [Google Scholar]
71. Booe JM, Walker CS, Barwell J, Kuteyi G, Simms J. 71.  et al. 2015. Structural basis for receptor activity-modifying protein-dependent selective peptide recognition by a G protein–coupled receptor. Mol. Cell 58:1040–52 [Google Scholar]
72. Harikumar KG, Simms J, Christopoulos G, Sexton PM, Miller LJ. 72.  2009. Molecular basis of association of receptor activity-modifying protein 3 with the family B G protein–coupled secretin receptor. Biochemistry 48:11773–85 [Google Scholar]
73. Rist B, Entzeroth M, Beck-Sickinger AG. 73.  1998. From micromolar to nanomolar affinity: a systematic approach to identify the binding site of CGRP at the human calcitonin gene-related peptide 1 receptor. J. Med. Chem. 41:117–23 [Google Scholar]
74. Breeze AL, Harvey TS, Bazzo R, Campbell ID. 74.  1991. Solution structure of human calcitonin gene-related peptide by ¹H NMR and distance geometry with restrained molecular dynamics. Biochemistry 30:575–82 [Google Scholar]
75. Carpenter KA, Schmidt R, von Mentzer B, Haglund U, Roberts E, Walpole C. 75.  2001. Turn structures in CGRP C-terminal analogues promote stable arrangements of key residue side chains. Biochemistry 40:8317–25 [Google Scholar]
76. Perez-Castells J, Martin-Santamaria S, Nieto L, Ramos A, Martinez A. 76.  et al. 2012. Structure of micelle-bound adrenomedullin: a first step toward the analysis of its interactions with receptors and small molecules. Biopolymers 97:45–53 [Google Scholar]
77. Watkins HA, Walker CS, Ly KN, Bailey RJ, Barwell J. 77.  et al. 2014. Receptor activity-modifying protein-dependent effects of mutations in the calcitonin receptor-like receptor: implications for adrenomedullin and calcitonin gene-related peptide pharmacology. Br. J. Pharmacol. 171:772–88 [Google Scholar]
78. Watkins HA, Rathbone DL, Barwell J, Hay DL, Poyner DR. 78.  2013. Structure-activity relationships for α-calcitonin gene-related peptide. Br. J. Pharmacol. 170:1308–22 [Google Scholar]
79. Qi T, Hay DL. 79.  2010. Structure-function relationships of the N terminus of receptor activity-modifying proteins. Br. J. Pharmacol. 159:1059–68 [Google Scholar]
80. Moore EL, Gingell JJ, Kane SA, Hay DL, Salvatore CA. 80.  2010. Mapping the CGRP receptor ligand binding domain: Tryptophan-84 of RAMP1 is critical for agonist and antagonist binding. Biochem. Biophys. Res. Commun. 394:141–45 [Google Scholar]
81. Qi T, Christopoulos G, Bailey RJ, Christopoulos A, Sexton PM, Hay DL. 81.  2008. Identification of N-terminal receptor activity-modifying protein residues important for calcitonin gene-related peptide, adrenomedullin, and amylin receptor function. Mol. Pharmacol. 74:1059–71 [Google Scholar]
82. Qi T, Ly K, Poyner DR, Christopoulos G, Sexton PM, Hay DL. 82.  2011. 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 32:1060–67 [Google Scholar]
83. Gingell JJ, Qi T, Bailey RJ, Hay DL. 83.  2010. A key role for tryptophan 84 in receptor activity-modifying protein 1 in the amylin 1 receptor. Peptides 31:1400–4 [Google Scholar]
84. Barwell J, Conner A, Poyner DR. 84.  2011. 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 1813:1906–16 [Google Scholar]
85. Woolley MJ, Watkins HA, Taddese B, Karakullukcu ZG, Barwell J. 85.  et al. 2013. The role of ECL2 in CGRP receptor activation: a combined modelling and experimental approach. J. R. Soc. Interface 10:20130589 [Google Scholar]
86. Kuwasako K, Hay DL, Nagata S, Hikosaka T, Kitamura K, Kato J. 86.  2012. The third extracellular loop of the human calcitonin receptor-like receptor is crucial for the activation of adrenomedullin signalling. Br. J. Pharmacol. 166:137–50 [Google Scholar]
87. Hay DL, Harris PW, Kowalczyk R, Brimble MA, Rathbone DL. 87.  et al. 2014. Structure-activity relationships of the N terminus of calcitonin gene-related peptide: key roles of alanine-5 and threonine-6 in receptor activation. Br. J. Pharmacol. 171:415–26 [Google Scholar]
88. Vohra S, Taddese B, Conner AC, Poyner DR, Hay DL. 88.  et al. 2013. Similarity between class A and class B G-protein-coupled receptors exemplified through calcitonin gene-related peptide receptor modelling and mutagenesis studies. J. R. Soc. Interface 10:20120846 [Google Scholar]
89. Conner M, Hicks MR, Dafforn T, Knowles TJ, Ludwig C. 89.  et al. 2008. Functional and biophysical analysis of the C-terminus of the CGRP-receptor; a family B GPCR. Biochemistry 47:8434–44 [Google Scholar]
90. Conner AC, Simms J, Conner MT, Wootten DL, Wheatley M, Poyner DR. 90.  2006. Diverse functional motifs within the three intracellular loops of the CGRP1 receptor. Biochemistry 45:12976–85 [Google Scholar]
91. Conner AC, Simms J, Howitt SG, Wheatley M, Poyner DR. 91.  2006. The second intracellular loop of the calcitonin gene-related peptide receptor provides molecular determinants for signal transduction and cell surface expression. J. Biol. Chem. 281:1644–51 [Google Scholar]
92. Conner AC, Hay DL, Simms J, Howitt SG, Schindler M. 92.  et al. 2005. A key role for transmembrane prolines in calcitonin receptor-like receptor agonist binding and signalling: implications for family B G-protein-coupled receptors. Mol. Pharmacol. 67:20–31 [Google Scholar]
93. Kuwasako K, Kitamura K, Nagata S, Hikosaka T, Kato J. 93.  2011. Structure–function analysis of helix 8 of human calcitonin receptor-like receptor within the adrenomedullin 1 receptor. Peptides 32:144–49 [Google Scholar]
94. Kuwasako K, Kitamura K, Nagata S, Hikosaka T, Kato J. 94.  2010. Function of the cytoplasmic tail of human calcitonin receptor-like receptor in complex with receptor activity-modifying protein 2. Biochem. Biophys. Res. Commun. 392:380–85 [Google Scholar]
95. Bailey RJ, Hay DL. 95.  2007. Agonist-dependent consequences of proline to alanine substitution in the transmembrane helices of the calcitonin receptor. Br. J. Pharmacol. 151:678–87 [Google Scholar]
96. Benítez-Páez A. 96.  2006. Sequence analysis of the receptor activity-modifying proteins family, new putative peptides and structural conformation inference. In Silico Biol. 6:467–83 [Google Scholar]
97. Nag K, Sultana N, Kato A, Dranik A, Nakamura N. 97.  et al. 2015. Ligand-induced internalization, recycling, and resensitization of adrenomedullin receptors depend not on CLR or RAMP alone but on the receptor complex as a whole. Gen. Comp. Endocrinol. 212:156–62 [Google Scholar]
98. Nag K, Sultana N, Hirose S. 98.  2012. Calcitonin receptor-like receptor (CLR) influences posttranslational events of receptor activity-modifying proteins (RAMPs). Biochem. Biophys. Res. Commun. 418:824–29 [Google Scholar]
99. Nag K, Kato A, Nakada T, Hoshijima K, Mistry AC. 99.  et al. 2006. Molecular and functional characterization of adrenomedullin receptors in pufferfish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:2R467–78 [Google Scholar]
100. Cohen SP, Haack KKV, Halstead-Nussloch GE, Bernard KF, Hatt H. 100.  et al. 2010. Identification of RL-TGR, a coreceptor involved in aversive chemical signaling. PNAS 107:12339–44 [Google Scholar]
101. Gibbons C, Dackor R, Dunworth W, Fritz-Six K, Caron KM. 101.  2007. Receptor activity-modifying proteins: RAMPing up adrenomedullin signaling. Mol. Endocrinol. 21:783–96 [Google Scholar]
102. Bailey RJ, Hay DL. 102.  2006. Pharmacology of the human CGRP1 receptor in Cos 7 cells. Peptides 27:1367–75 [Google Scholar]
103. Tilakaratne N, Christopoulos G, Zumpe ET, Foord SM, Sexton PM. 103.  2000. 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. 294:161–72 [Google Scholar]
104. Qi T, Dong M, Watkins HA, Wootten D, Miller LJ, Hay DL. 104.  2013. Receptor activity-modifying protein-dependent impairment of calcitonin receptor splice variant Δ(1–47)hCT_(a) function. Br. J. Pharmacol. 168:644–57 [Google Scholar]