Structural basis of allosteric ligand-receptor interactions in the insulin-relaxin peptide family: Implications for other receptor tyrosine kinases and G-protein-coupled receptors

Annals of the New York Academy of Sciences

Volumn 1160, Issue , 2009, Pages 45-53

  De Meyts, Pierre ^a   Gauguin, Lisbeth ^a   Svendsen, Angela Manegold ^a   Sarhan, Mazen ^a   Knudsen, Louise ^a   Nøhr, Jane ^a   Kiselyov, Vladislav V ^a  

^a HAGEDORN RESEARCH INSTITUTE   (Denmark)

Author keywords

Allosterism; GPCR; IGF I; IGF II; INSL; Insulin; LGR; Negative cooperativity; Relaxin; RTK; RXFP

Indexed keywords

G PROTEIN COUPLED RECEPTOR; INSULIN; INSULIN RECEPTOR; PROTEIN TYROSINE KINASE; RELAXIN; SOMATOMEDIN B; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ALLOSTERISM; CONFERENCE PAPER; CRYSTAL STRUCTURE; DIMERIZATION; EXTRACELLULAR SPACE; GROWTH; LIGAND BINDING; METABOLISM; NONHUMAN; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REPRODUCTION; SURVIVAL;

EID: 64549133821     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2009.03837.x     Document Type: Conference Paper

References (64)

1. De Meyts, P., J. Roth, D.M. Neville, Jr., et al. 1973. Insulin interactions with its receptors: Experimental evidence for negative cooperativity. Biochem. Biophys. Res. Commun. 55: 154-161.
2. De Meyts, P., A.R. Bianco & J. Roth. 1976. Site-site interactions among insulin receptors: Characterization of the negative cooperativity. J. Biol. Chem. 251: 1877-1888.
3. Cuatrecasas, P. & M.D. Hollenberg. 1975. Binding of insulin and other hormones to non-receptor materials: Saturability, specificity and apparent "negative cooperativity." Biochem. Biophys. Res. Commun. 62: 31-41.
4. Pollet, R.J., M.L. Standaert & B.A. Haase. 1977. Insulin binding to the human lymphocyte receptor. Evaluation of the negative cooperativity model. J. Biol. Chem. 252: 5828-5834.
5. De Meyts, P. 1976. Cooperative properties of hormone receptors in cell membranes. J. Supramol. Struct. 4: 241-258.
6. Pollet, R.J., M.L. Standaert & B.A. Haase. 1980. Hormone-receptor interactions are noncooperative: Application to the beta-adrenergic receptor. Proc. Natl. Acad. Sci. USA 77: 4340-4344.
7. Powell-Jones C.H., C.G. Thomas, Jr., & S.N. Nayfeh. 1980. Thyrotropin receptors in normal human thyroid. Nonclassical binding kinetics not explained by the negative cooperativity model. J. Biol. Chem. 255: 4001-4010.
8. Hubbard, S.R. & W.T. Miller. 2007. Receptor tyro-sine kinases: Mechanisms of activation and signaling. Curr. Opin. Cell Biol. 19: 117-123.
9. Schäffer, L. 1994. A model for insulin binding to the insulin receptor. Eur. J. Biochem. 221: 1127-1132.
10. De Meyts, P. 1994. The structural basis of insulin and insulin-like growth factor-I (IGF-I) receptor binding and negative cooperativity, and its relevance to mitogenic versus metabolic signaling. Diabetologia 37 (Suppl. 2): S135-S148.
11. McKern, N.M., M.C. Lawrence, V.A. Streltsov, et al. 2006. Structure of the insulin receptor ectodomain reveals a folded-over conformation. Nature 443: 218-221.
12. Lawrence, M. 2007. Insulin receptor structure and its implications for the IGF-1 receptor. Curr. Opin. Struct. Biol. 17: 699-705.
13. Ward, C.W., M.C. Lawrence, V.A. Streltsov, et al. 2007. The insulin and EGF receptor structures: New insights into ligand-induced receptor activation. Trends Biochem. Sci. 32: 129-137.
14. De Meyts, P. 2008. The insulin receptor: A prototype for dimeric, allosteric membrane receptors? Trends Biochem. Sci. 33: 376-384.
15. Springael, J.Y., E. Urizar, S. Costagliola, et al. 2007. Allosteric properties of G protein-coupled receptor oligomers. Pharmacol. Ther. 115: 410-418.
16. Szidonya, L., M. Cserzo & L. Hunyady. 2008. Dimer-ization and oligomerization of G-protein-coupled receptors: Debated structures with established and emerging functions. J. Endocrinol. 196: 435-453.
17. Christopoulos, A. & T. Kenakin. 2002. G protein-coupled receptor allosterism and complexing. Pharmacol. Rev. 54: 323-374.
18. Svendsen, A.M., M. Vrecl, T.M. Ellis, et al. 2008. Cooperative binding of insulin-like peptide 3 to a dimeric relaxin family peptide receptor 2. Endocrinology 149: 1113-1120.
19. Svendsen, A.M., A. Zalesko, J. Konig, et al. 2008. Negative cooperativity in H2 relaxin binding to a dimeric relaxin family peptide receptor 1. Mol. Cell. Endocrinol. 296: 10-17.
20. Bathgate, R.A.D., R. Ivell, B.M. Sanborn, et al. 2005. Receptors for relaxin family peptides. Ann. N. Y. Acad. Sci. 1041: 61-76.
21. Haugaard-Jonsson, L.M., M.A. Hossain, N.L. Daly, et al. 2008. Structure of the R3/I5 chimeric relaxin peptide, a selective GPCR135 and GPCR142 agonist. J. Biol. Chem. 283: 23811-23818.
22. De Meyts, P. 2004. Insulin and its receptor: Structure, function and evolution. Bioessays 26: 1351-1362.
23. Adams, T.E., V.C. Epa, T.P. Garrett, et al. 2000. Structure and function of the type 1 insulin-like growth factor receptor. Cell. Mol. Life Sci. 57: 1050-1093.
24. Chan, S.J. & D.F. Steiner. 2000. Insulin through the ages: Phylogeny of a growth promoting and metabolic regulatory hormone. Am. Zool. 40: 213-222.
25. Nef, S., S. Verma-Kurvari, J. Merenmies, et al. 2003. Testis determination requires insulin receptor family function in mice. Nature 426: 291-295.
26. Wilkinson, T.N. & R.A.D. Bathgate. 2007. The evolution of the relaxin peptide family and their receptors. Adv. Exp. Med. Biol. 612: 1-13.
27. Urizar, E., L. Montanelli, T. Loy, et al. 2005. Glycoprotein hormone receptors: Link between receptor homodimerization and negative cooperativity. EMBO J. 24: 1954-1964.
28. Wilkinson, T.N., T.P. Speed, G.W Tregear, et al. 2005. Coevolution of the relaxin-like peptides and their receptors. Ann. N. Y. Acad. Sci. 1041: 534-539.
29. Van Loy, T., H.P. Vandersmissen, M.B. Van Hiel, et al. 2008. Comparative genomics of leucine-rich repeats containing G protein-coupled receptors and their ligands. Gen. Comp. Endocrinol. 155: 14-21.
30. Gray, S.G., I. Steinfeldt Mathiasen & P. De Meyts. 2003. The insulin-like growth factors and insulin-signalling systems: An appealing target for breast cancer therapy? Horm. Metab. Res. 35: 857-871.
31. De Meyts, P. & J. Whittaker. 2002. Structural biology of insulin and IGF1 receptors: Implications for drug design. Nat. Rev. Drug Discov. 1: 769-783.
32. De Meyts, P. et al. 2004. Insulin and IGF-I receptor structure and binding mechanism. In Insulin Action. A.R. Saltiel & J. Pessin, Eds.: 1-32. R.C. Landes. Austin, TX.
33. Lawrence, M.C., N.M. McKern & C.W Ward. 2007. Insulin receptor structure and its implications for the IGF-1 receptor. Curr. Opin. Struct. Biol. 17: 699-705.
34. Ullrich, A. & J. Schlessinger. 1990. Signal transduc-tion by receptors with tyrosine kinase activity. Cell 61: 203-212.
35. Heldin, C.H. 1995. Dimerization of cell surface receptors in signal transduction. Cell 80: 213-223.
36. Christoffersen, C.T., K.E. Bornfeldt, C.M. Rotella, et al. 1994. Negative cooperativity in the insulin-like growth factor-I (IGF-I) receptor and a chimeric IGF-I/insulin receptor. Endocrinology 135: 472-475.
37. De Meyts, P., B. Wallach, C.T. Christoffersen, et al. 1994. The insulin-like growth factor-I receptor. Structure, ligand binding mechanism and signal transduction. Horm. Res. 42: 152-169.
38. Gauguin, L., C. Delaine, C.L. Alvino, et al. 2008. Alanine scanning of a putative receptor binding surface of insulin-like growth factor-I. J. Biol. Chem. 283: 20821-20829.
39. Gauguin, L., B. Klaproth, W. Sajid, et al. 2008. Structural basis for the lower affinity of the insulin-like growth factors for the insulin receptor. J. Biol. Chem. 283: 2604-2613.
40. Bullesbach, E.E. & C. Schwabe. 2006. The mode of interaction of the relaxin-like factor (RLF) with the leucine-rich repeat G protein-activated receptor 8. J. Biol. Chem. 281: 26136-26143.
41. Bullesbach, E.E. & C. Schwabe. 2005. LGR8 signal activation by the relaxin-like factor. J. Biol. Chem. 280: 14586-14590.
42. Bullesbach, E.E. & C. Schwabe. 2005. The traplike relaxin-binding site of the leucine-rich G-protein-coupled receptor 7. J. Biol. Chem. 280: 14051-14056.
43. Bullesbach, E.E. & C. Schwabe. 2000. The relaxin receptor-binding site geometry suggests a novel gripping mode of interaction. J. Biol. Chem. 275: 35276-35280.
44. Bullesbach, E.E. & C. Schwabe. 1999. Tryptophan B27 in the relaxin-like factor (RLF) is crucial for RLF receptor-binding. Biochemistry 38: 3073-3078.
45. Schwabe, C. & J.K. Mc Donald. 1977. Relaxin: A disulfide homolog of insulin. Science 197: 914-915.
46. Schwabe, C. & E.E. Bullesbach. 2007. Relaxin, the relaxin-like factor and their receptors. Adv. Exp. Med. Biol. 612: 14-25.
47. Hossain, M.A., K.J. Rosengren, L.M. Haugaard-Jonsson, et al. 2008. The A-chain of human relaxin family peptides has distinct roles in the binding and activation of the different relaxin family peptide receptors. J. Biol. Chem. 283: 17287-17297.
48. Scott, D.J., T.N. Wilkinson, S. Zhang, et al. 2007. Defining the LGR8 residues involved in binding insulin-like peptide 3. Mol. Endocrinol. 21: 1699-1712.
49. 125 nerve growth-factor in embryonic heart and brain. J. Biol. Chem. 249: 5918-5923.
50. Zampieri, N. & M.V Chao. 2004. The p75 NGF receptor exposed. Science 304: 833-834.
51. Prahl, M., T. Nederman, J. Carlsson, et al. 1991. Binding of epidermal growth-factor (EGF) to a cultured human glioma cell line. J. Recept. Res. 11: 791-812.
52. Macdonald, J.L. & L.J. Pike. 2008. Heterogeneity in EGF-binding affinities arises from negative cooper-ativity in an aggregating system. Proc. Natl. Acad. Sci. USA 105: 112-117.
53. Burgess, A.W., H.S. Cho, C. Eigenbrot, et al. 2003. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell 12: 541-552.
54. Jorissen, R.N., E Walker, N. Pouliot, et al. 2003. Epidermal growth factor receptor: Mechanisms of activation and signalling. Exp. Cell Res. 284: 31-53.
55. Webb, S.E.D., S.K. Roberts, S.R. Needham, et al. 2008. Single-molecule imaging and fluorescence lifetime imaging microscopy show different structures for high- and low-affinity epidermal growth factor receptors in A431 cells. Biophys. J. 94: 803-819.
56. Clayton, A.H., E Walker, S.G. Orchard, et al. 2005. Ligand-induced dimer-tetramer transition during the activation of the cell surface epidermal growth factor receptor-A multidimensional microscopy analysis. J. Biol. Chem. 280: 30392-30399.
57. Limbird, L., P.D. Meyts & R.J. Lefkowitz. 1975. Betaadrenergic receptors: Evidence for negative cooperativity. Biochem. Biophys. Res. Commun. 64: 1160-1168.
58. Bulenger, S., S. Marullo & M. Bouvier. 2005. Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol. Sci. 26: 131-137.
59. Latif, R., P. Graves & T.F. Davies. 2001. Oligomerization of the human thyrotropin receptor: Fluorescent protein-tagged hTSHR reveals post-translational complexes. J. Biol. Chem. 276: 45217-45224.
60. Christopoulos, A., A. Lanzafame, A. Ziegler, et al. 1997. Kinetic studies of co-operativity at atrial muscarinic M2 receptors with an "infinite dilution" procedure. Biochem. Pharmacol. 53: 795-800.
61. Pizard, A., J. Marchetti, J. Allegrini, et al. 1998. Negative cooperativity in the human bradykinin B2 receptor. J. Biol. Chem. 273: 1309-1315.
62. Rapoport, B. & S.M. McLachlan. 2007. The thyrotropin receptor in Graves' disease. Thyroid 17:911-922.
63. Christopoulos, A. 2002. Allosteric binding sites on cell-surface receptors: Novel targets for drug discovery. Nat. Rev. Drug Discov. 1: 198-210.
64. Mynarcik, D.C., P.F. Williams, L. Schaffer, et al. 1997. Identification of common ligand binding determinants of the insulin and insulin-like growth factor-I receptors. Insights into mechanisms of ligand binding. J. Biol. Chem. 272: 18650-18655.