Thyroid stimulating autoantibody M22 mimics TSH binding to the TSH receptor leucine rich domain: A comparative structural study of protein-protein interactions

Journal of Molecular Endocrinology

Volumn 42, Issue 5, 2009, Pages 381-395

  Nunez Miguel R ^a,b   Sanders, J ^a   Chirgadze, D Y ^b   Furmaniak, J ^a   Rees Smith, B ^a  

^a RSR LTD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN MONOCLONAL ANTIBODY; LEUCINE; MONOCLONAL ANTIBODY M22; THYROID STIMULATING IMMUNOGLOBULIN; THYROTROPIN; THYROTROPIN BETA SUBUNIT; THYROTROPIN RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPARATIVE STUDY; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; DISULFIDE BOND; HEAVY CHAIN; HORMONE BINDING; HYDROGEN BOND; HYDROPHOBICITY; IMMUNOGLOBULIN LIGHT CHAIN GENE; LIGHT CHAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACIDS; AUTOANTIBODIES; HUMANS; IMMUNOGLOBULINS, THYROID-STIMULATING; LIGANDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RECEPTORS, THYROTROPIN; STRUCTURE-ACTIVITY RELATIONSHIP; SURFACE PROPERTIES; THYROTROPIN;

EID: 67649361912     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-08-0152     Document Type: Article

References (58)

1. Ando T, Latif R, Pritsker A, Moran T, Nagayama Y & Davies TF 2002 A monoclonal thyroid-stimulating antibody. Journal of Clinical Investigation 110 1667-1674.
2. Baenziger JU & Green ED 1988 Pituitary glycoprotein hormone oligosaccharides - structure, synthesis and function of the asparagine-linked oligosaccharides on lutropin, follitropin and thyrotropin. Biochimica et Biophysica Acta 947 287-306.
3. Baker EN & Hubbard RE 1984 Hydrogen bonding in globular proteins. Progress in Biophysics and Molecular Biology 44 97-179.
4. Caltabiano G, Campillo M, De Leener A, Smits G, Vassart G, Costagliola S & Pardo L 2008 The specificity of binding of glycoprotein hormones to their receptors. Cellular and Molecular Life Sciences 65 2484-2492.
5. Chazenbalk GD, McLachlan SM, Nagayama Y & Rapoport B 1996 Is receptor cleavage into two subunits necessary for thyrotropin action? Biochemical and Biophysical Research Communications 225 479-484.
6. 2-adrenergic G protein-coupled receptor. Science 318 1258-1265.
7. Claus M, Neumann S, Kleinau G, Krause G & Paschke R 2006 Structural determinants for G-protein activation and specificity in the third intracellular loop of the thyroid-stimulating hormone receptor. Journal of Molecular Medicine 84 943-954.
8. Costagliola S, Sunthorntepvarakul T, Migeotte I, Van Sande J, Kajava AM, Refetoff S & Vassart G 1999 Structure-function relationship of two loss-of-function mutations of the thyrotropin receptor gene. Thyroid 9 995-1000.
9. Costagliola S, Bonomi M, Morgenthaler NG, van Durme J, Panneels V, Refetoff S & Vassart G 2004 Delineation of the discontinuous-conformational epitope of a monoclonal antibody displaying full in vitro and in vivo thyrotropin activity. Molecular Endocrinology 18 3020-3034.
10. Fan QR & Hendrickson WA 2005 Structure of human follicle-stimulating hormone in complex with its receptor. Nature 433 269-277.
11. Farid NR & Szkudlinski MW 2004 Minireview: structural and functional evolution of the thyrotropin receptor. Endocrinology 145 4048-4057.
12. Felding-Habermann B, Lerner RA, Lillo A, Zhuang SF, Weber MR, Arrues S, Gao CS, Mao SL, Saven A & Janda KD 2004 Combinatorial antibody libraries from cancer patients yield ligand-mimetic Arg-Gly-Asp-containing immunoglobulins that inhibit breast cancer metastasis. PNAS 101 17210-17215.
13. Foord SM, Bonner TI, Neubig RR, Rosser EM, Pin J-P, Davenport AP, Spedding M & Harmar AJ 2005 International Union of Pharmacology. XLVI. G protein-coupled receptor list. Pharmacological Reviews 57 279-288.
14. Fox KM, Dias JA & van Roey P 2001 Three-dimensional structure of human follicle-stimulating hormone. Molecular Endocrinology 15 378-389.
15. Fredriksson R, Lagerström MC, Lundin LG & Schiöth HB 2003 The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Molecular Pharmacology 63 1256-1272.
16. Gallivan JP & Dougherty DA 1999 Cation-π interactions in structural biology. PNAS 96 9459-9464.
17. Grossmann M, Szkudlinski MW, Tropea JE, Bishop LA, Thotakura NR, Schofield PR & Weintraub BD 1995 Expression of human thyrotropin in cell lines with different glycosylation patterns combined with mutagenesis of specific glycosylation sites. Characterization of a novel role for the oligosaccharides in the in vitro and in vivo bioactivity. Journal of Biological Chemistry 270 29378-29385.
18. Grossmann M, Weintraub BD & Szkudlinski MW 1997 Novel insights into the molecular mechanisms of human thyrotropin action: structural, and therapeutic implications for the glycoprotein hormone family. Endocrine Reviews 18 476-501.
19. 2A adenosine receptor bound to an antagonist. Science 322 1211-1217.
20. Jeffreys J, Depraetere H, Sanders J, Oda Y, Evans M, Kiddie A, Richards T, Furmaniak J & Rees Smith B 2002 Characterization of the thyrotropin binding pocket. Thyroid 12 1051-1061.
21. Jones S & Thornton JM 1996 Principles of protein-protein interactions. PNAS 93 13-20.
22. Laskowski RA 1995 SURFNET: a program for visualizing molecular surfaces, cavities and intermolecular interactions. Journal of Molecular Graphics 13 323-330.
23. Lee B & Richards FM 1971 The interpretation of protein structures: estimation of static accessibility. Journal of Molecular Biology 55 379-400.
24. Lovell SC, Davis IW, Arendall WB III, deBakker PIW, Word JM, Prisant MG, Richardson JS & Richardson DC 2003 Structure validation by Ca geometry: Φ, Ψ and Cβ deviation. Proteins: Structure, Function, and Bioinformatics 50 437-450.
25. McDonald NQ & Hendrickson WA 1993 A structural superfamily of growth factors containing a cystine knot motif. Cell 73 421-424.
26. McDonald IK & Thornton JM 1994 Satisfying hydrogen bonding potential in proteins. Journal of Molecular Biology 238 777-793.
27. Mizutori Y, Chen C-R, McLachlan M & Rapoport B 2008 The thyrotropin hinge region is not simply a scaffold for the leucine-rich domain but contributes to ligand binding and signal transduction. Molecular Endocrinology 22 1171-1182.
28. Mueller S, Kleinau G, Jaeschke H, Paschke R & Krause G 2008 Extended hormone binding site of the human TSHR: distinctive acidic residues in the hinge region are involved in bovine TSH binding and receptor activation. Journal of Biological Chemistry 283 18048-18055.
29. Murakami M & Kouyama T 2008 Crystal structure of squid rhodopsin. Nature 453 363-368.
30. Murray-Rust J, McDonald NQ, Blundell TL, Hosang M, Oefner C, Winkler F & Bradshow RA 1993 Topogical similarities in TGF-β2, PDGF-BB and NGF define a superfamily of polypeptide growth factors. Structure 1 153-159.
31. Nakatake N, Sanders J, Richards T, Burne P, Barrett C, Pra CD, Presotto F, Betterle C, Furmaniak J & Smith BR 2006 Estimation of serum TSH receptor autoantibody concentration and affinity. Thyroid 16 1077-1084.
32. Núñez Miguel R, Sanders J, Jeffreys J, Depraetere H, Blundell TL, Furmaniak J & Rees Smith B 2003 TSH receptor cleavage domain and tissue inhibitor of metalloproteinase-2. Thyroid 13 665-666.
33. Núñez Miguel R, Sanders J, Jeffreys J, Depraetere H, Evans M, Richards T, Blundell TL, Rees Smith B & Furmaniak J 2004 Analysis of the thyrotropin receptor-thyrotropin interaction by comparative modeling. Thyroid 14 991-1011.
34. Núñez Miguel R, Sanders J, Chirgadze DY, Blundell TL, Furmaniak J & Rees Smith B 2008 FSH and TSH binding to their respective receptors - similarities, differences and implication for glycoprotein hormone specificity. Journal of Molecular Endocrinology 41 145-164.
35. Palczewski K, Kamusaka T, Hori T, Behnke CA, Motoshima H, Fox BA, LeTrong I, Teller DC, Okada T, Stenkamp RE et al. 2000 Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 739-745.
36. Rapoport B, Chazenbalk GD, Jaume JC & McLachlan SM 1998 The thyrotropin (TSH) receptor: interaction with TSH and autoantibodies. Endocrine Reviews 19 673-716.
37. Rasmussen SGF, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VRP, Sanishvili R, Fischetti RF et al. 2007 Crystal structure of the human beta(2) adrenergic G-protein-coupled receptor. Nature 450 383-388.
38. Rees Smith B, McLachlan SM & Furmaniak J 1988 Autoantibodies to the thyrotropin receptor. Endocrine Reviews 9 106-121.
39. Rees Smith B, Sanders J & Furmaniak J 2007 TSH receptor antibodies. Thyroid 17 923-938.
40. Richmond TJ 1984 Solvent accessible surface area and excluded volume in proteins. Analytical equations for overlapping spheres and implications for the hydrophobic effect. Journal of Molecular Biology 178 63-89.
41. Sanders J, Jeffreys J, Depraetere H, Richards T, Evans M, Kiddie A, Brereton K, Groenen M, Oda Y, Furmaniak JG et al. 2002 Thyroid-stimulating monoclonal antibodies. Thyroid 12 1043-1050.
42. Sanders J, Evans M, Premawardhana LDKE, Depraetere H, Jeffreys J, Richards T, Furmaniak J & Rees Smith B 2003 Human monoclonal thyroid stimulating autoantibody. Lancet 362 126-128.
43. Sanders J, Jeffreys J, Depraetere H, Evans M, Richards T, Kiddie A, Brereton K, Premawardhana LDKE, Chirgadze DY, Núñez Miguel R et al. 2004 Characteristics of a human monoclonal autoantibody to the thyrotropin receptor: sequence structure and function. Thyroid 14 560-570.
44. Sanders J, Bolton J, Sanders P, Jeffreys J, Nakatake N, Richards T, Evans M, Kiddie A, Summerhayes S, Roberts E et al. 2006 Effects of TSH receptor mutations on binding and biological activity of monoclonal antibodies and TSH. Thyroid 16 1195-1206.
45. Sanders J, Chirgadze DY, Sanders P, Baker S, Sullivan A, Bhardwaja A, Bolton J, Reeve M, Nakatake N, Evans M et al. 2007a Crystal structure of the TSH receptor in complex with a thyroid stimulating autoantibody. Thyroid 17 395-410.
46. Sanders J, Núñez Miguel R, Bolton J, Bhardwaja A, Sanders P, Nakatake N, Evans M, Blundell TL, Furmaniak J & Rees Smith B 2007b Molecular interactions between the TSH receptor and a thyroid stimulating monoclonal autoantibody. Thyroid 17 699-706.
47. Sanders J, Furmaniak J & Rees Smith B 2008a Crystal structure of the TSHR receptor. Patent publication number WO2008025991.
48. Sanders J, Evans M, Betterle C, Sanders P, Bhardwaja A, Young S, Roberts E, Wilmot J, Richards T, Kiddie A et al. 2008b A human monoclonal autoantibody to the thyrotropin receptor with thyroid-stimulating blocking activity. Thyroid 18 735-746.
49. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauß N, Choe H-W, Hofmann KP & Ernst OP 2008 Crystal structure of opsin in its G-protein-interacting conformation. Nature 455 497-503.
50. Smith JW, Tudor Evans A, Costall B & Smythe JW 2002 Thyroid hormones, brain function and cognition: a brief review. Neuroscience and Biobehavioral Reviews 26 45-60.
51. Smits G, Govaerts C, Nubourgh I, Pardo L, Vassart G & Costagliola S 2002 Lysine 183 and glutamic acid 157 of the TSH receptor: two interacting residues with a key role in determining specificity toward TSH and human CG. Molecular Endocrinology 16 722-735.
52. Smits G, Campillo M, Govaerts C, Janssens V, Richter C, Vassart G, Pardo L & Costagliola S 2003 Glycoprotein hormone receptors: determinants in leucine-rich repeats responsible for ligand specificity. EMBO Journal 22 2692-2703.
53. Sunthornthepvarakul T, Gottschalk ME, Hayashi Y & Refetoff S 1995 Resistance to thyrotropin caused by mutations in the thyrotropin-receptor gene. New England Journal of Medicine 332 155-160.
54. Szkudlinski MW, Grossmann M & Weitraub BD 1996 Structure-function studies of human TSH. New advances in design of glycoprotein hormone analogs. Trends in Endocrinology and Metabolism 7 277-286.
55. Szkudlinski MW, Fremont V, Ronin C & Weitraub BD 2002 Thyroid-stimulating hormone and thyroid-stimulating hormone receptor structure-function relationship. Physiological Reviews 82 473-502.
56. 1 adrenergic G-protein-coupled receptor. Nature 454 486-492.
57. Wu H, Lustbader JW, Liu Y, Canfield RE & Hendrickson WA 1994 Structure of human chorionic gonadotropin at 2.6 Angstroms resolution from MAD analysis of the selenomethionyl protein. Structure 2 545-558.
58. Wucherpfennig KW 2001 Structural basis of molecular mimicry. Journal of Autoimmunity 16 293-302.