Selective CGRP and adrenomedullin peptide binding by tethered RAMP-calcitonin receptor-like receptor extracellular domain fusion proteins

Protein Science

Volumn 22, Issue 12, 2013, Pages 1775-1785

  Moad, Heather E ^a   Pioszak, Augen A ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Calcitonin family peptide; Class B G protein coupled receptor; Neuropeptide; Vasodilator

Indexed keywords

ADRENOMEDULLIN; ALANINE; BACTERIAL PROTEIN; CALCITONIN GENE RELATED PEPTIDE; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; HETERODIMER; HYBRID PROTEIN; MONOMER; RECEPTOR ACTIVITY MODIFYING PROTEIN 1; RECEPTOR ACTIVITY MODIFYING PROTEIN 2; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; RECEPTOR BINDING; STOICHIOMETRY;

CALCITONIN FAMILY PEPTIDE; CLASS B G PROTEIN-COUPLED RECEPTOR; NEUROPEPTIDE; VASODILATOR;

ADRENOMEDULLIN; AMINO ACID SEQUENCE; BINDING SITES; CALCITONIN GENE-RELATED PEPTIDE; CALCITONIN RECEPTOR-LIKE PROTEIN; ESCHERICHIA COLI; HUMANS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR ACTIVITY-MODIFYING PROTEINS; RECEPTORS, ADRENOMEDULLIN; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 84892376928     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2377     Document Type: Article

References (38)

1. Poyner DR, Sexton PM, Marshall I, Smith DM, Quirion R, Born W, Muff R, Fischer JA, Foord SM (2002) International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev 54:233-246.
2. Brain SD, Grant AD (2004) Vascular actions of calcitonin gene-related peptide and adrenomedullin. Physiol Rev 84:903-934.
3. Caron KM, Smithies O (2001) Extreme hydrops fetalis and cardiovascular abnormalities in mice lacking a functional Adrenomedullin gene. Proc Natl Acad Sci USA 98:615-619.
4. Karpinich NO, Hoopes SL, Kechele DO, Lenhart PM, Caron KM (2011) Adrenomedullin function in vascular endothelial cells: Insights from genetic mouse models. Curr Hyperten Rev 7:228-239.
5. Hamid SA, Baxter GF (2006) A critical cytoprotective role of endogenous adrenomedullin in acute myocardial infarction. J Mol Cell Cardiol 41:360-363.
6. Nikitenko LL, Fox SB, Kehoe S, Rees MC, Bicknell R (2006) Adrenomedullin and tumour angiogenesis. Br J Cancer 94:1-7.
7. Toda M, Suzuki T, Hosono K, Hayashi I, Hashiba S, Onuma Y, Amano H, Kurihara Y, Kurihara H, Okamoto H, Hoka S, Majima M (2008) Neuronal system-dependent facilitation of tumor angiogenesis and tumor growth by calcitonin gene-related peptide. Proc Natl Acad Sci USA 105:13550-13555.
8. Gibbons C, Dackor R, Dunworth W, Fritz-Six K, Caron KM (2007) Receptor activity-modifying proteins: RAMPing up adrenomedullin signaling. Mol Endocrinol 21:783-796.
9. Recober A, Russo AF (2009) Calcitonin gene-related peptide: An update on the biology. Curr Opin Neurol 22:241-246.
10. Sexton PM, Poyner DR, Simms J, Christopoulos A, Hay DL (2012) RAMPs as drug targets. Advan Exp Med Biol 744:61-74.
11. McLatchie LM, Fraser NJ, Main MJ, Wise A, Brown J, Thompson N, Solari R, Lee MG, Foord SM (1998) RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393:333- 339.
12. Christopoulos G, Perry KJ, Morfis M, Tilakaratne N, Gao Y, Fraser NJ, Main MJ, Foord SM, Sexton PM (1999) Multiple amylin receptors arise from receptor activity-modifying protein interaction with the calcitonin receptor gene product. Mol Pharmacol 56:235-242.
13. Muff R, Buhlmann N, Fischer JA, Born W (1999) An amylin receptor is revealed following co-transfection of a calcitonin receptor with receptor activity modifying proteins-1 or -3. Endocrinology 140:2924-2927.
14. Tilakaratne N, Christopoulos G, Zumpe ET, Foord SM, Sexton PM (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 294:61-72.
15. Kusano S, Kukimoto-Niino M, Akasaka R, Toyama M, Terada T, Shirouzu M, Shindo T, Yokoyama S (2008) Crystal structure of the human receptor activitymodifying protein 1 extracellular domain. Protein Sci 17:1907-1914.
16. ter Haar E, Koth CM, Abdul-Manan N, Swenson L, Coll JT, Lippke JA, Lepre CA, Garcia-Guzman M, Moore JM (2010) Crystal structure of the ectodomain complex of the CGRP receptor, a class-B GPCR, reveals the site of drug antagonism. Structure 18:1083-1093.
17. Kusano S, Kukimoto-Niino M, Hino N, Ohsawa N, Okuda K, Sakamoto K, Shirouzu M, Shindo T, Yokoyama S (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.
18. Hoare SR (2005) Mechanisms of peptide and nonpeptide ligand binding to Class B G-protein-coupled receptors. Drug Discov Today 10:417-427.
19. Barwell J, Gingell JJ, Watkins HA, Archbold JK, Poyner DR, Hay DL (2012) Calcitonin and calcitonin receptor-like receptors: Common themes with family B GPCRs Br J Pharmacol 166:51-65.
20. Hall JM, Siney L, Lippton H, Hyman A, Kang-Chang J, Brain SD (1995) Interaction of human adrenomedullin 13-52 with calcitonin gene-related peptide receptors in the microvasculature of the rat and hamster. Br J Pharmacol 114:592-597.
21. Watkins HA, Au M, Hay DL (2012) The structure of secretin family GPCR peptide ligands: Implications for receptor pharmacology and drug development. Drug Discov Today 17:1006-1014.
22. Rist B, Entzeroth M, Beck-Sickinger AG (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 41:117-123.
23. Fitzsimmons TJ, Zhao X, Wank SA (2003) The extracellular domain of receptor activity-modifying protein 1 is sufficient for calcitonin receptor-like receptor function. J Biol Chem 278:14313-14320.
24. Qi T, Christopoulos G, Bailey RJ, Christopoulos A, Sexton PM, Hay DL (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- 1071.
25. Qi T, Hay DL (2010) Structure-function relationships of the N-terminus of receptor activity-modifying proteins. Br J Pharmacol 159:1059-1068.
26. Watkins HA, Rathbone DL, Barwell J, Hay DL, Poyner DR (2012) Structure-activity relationships for alpha calcitonin gene-related peptide. Br J Pharmacol. PMID: 23186257 {Medline}.
27. Watkins HA, Au M, Bobby R, Archbold JK, Abdul- Manan N, Moore JM, Middleditch MJ, Williams GM, Brimble MA, Dingley AJ, Hay DL (2013) Identification of key residues involved in adrenomedullin binding to the AM1 receptor. Br J Pharmacol 169:143-155.
28. Heroux M, Hogue M, Lemieux S, Bouvier M (2007) Functional calcitonin gene-related peptide receptors are formed by the asymmetric assembly of a calcitonin receptor-like receptor homo-oligomer and a monomer of receptor activity-modifying protein-1. J Biol Chem 282: 31610-31620.
29. Hill HE, Pioszak AA (2013) Bacterial expression and purification of a heterodimeric adrenomedullin receptor extracellular domain complex using DsbC-assisted disulfide shuffling. Prot Express Purif 88:107-113.
30. Pioszak AA, Parker NR, Suino-Powell K, Xu HE (2008) Molecular recognition of corticotropin-releasing factor by its G-protein-coupled receptor CRFR1. J Biol Chem 283:32900-32912.
31. Pioszak AA, Xu HE (2008) Molecular recognition of parathyroid hormone by its G protein-coupled receptor. Proc Natl Acad Sci USA 105:5034-5039.
32. Pioszak AA, Parker NR, Gardella TJ, Xu HE (2009) Structural basis for parathyroid hormone-related protein binding to the parathyroid hormone receptor and design of conformation-selective peptides. J Biol Chem 284:28382-28391.
33. Pal K, Swaminathan K, Xu HE, Pioszak AA (2010) Structural basis for hormone recognition by the Human CRFR2{alpha} G protein-coupled receptor. J Biol Chem 285:40351-40361.
34. Pioszak AA, Harikumar KG, Parker NR, Miller LJ, Xu HE (2010) Dimeric arrangement of the parathyroid hormone receptor and a structural mechanism for ligand-induced dissociation. J Biol Chem 285:12435- 12444.
35. Kumar S, Pioszak A, Zhang C, Swaminathan K, Xu HE (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.
36. Chakder S, Rattan S (1990) [Tyr0]-calcitonin generelated peptide 28-37 (rat) as a putative antagonist of calcitonin gene-related peptide responses on opossum internal anal sphincter smooth muscle. J Pharmacol Exp Ther 253:200-206.
37. Koth CM, Abdul-Manan N, Lepre CA, Connolly PJ, Yoo S, Mohanty AK, Lippke JA, Zwahlen J, Coll JT, Doran JD, Garcia-Guzman M, Moore JM (2010) Refolding and characterization of a soluble ectodomain complex of the calcitonin gene-related peptide receptor. Biochemistry 49:1862-1872.
38. Pin JP, Neubig R, Bouvier M, Devi L, Filizola M, Javitch JA, Lohse MJ, Milligan G, Palczewski K, Parmentier M, Spedding M (2007) International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol Rev 59:5-13.