Structure of human follicle-stimulating hormone in complex with its receptor

Nature

Volumn 433, Issue 7023, 2005, Pages 269-277

  Fan, Qing R ^a   Hendrickson, Wayne A ^a  

^a Howard Hughes Medical Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; CELL MEMBRANES; CONFORMATIONS; MOLECULAR STRUCTURE; PROTEINS;

BINDING SPECIFICITY; CHARGE DENSITY; FOLLICLE-STIMULATING HORMONE (FSH); GLYCOPROTEIN HORMONES; SIGNAL TRANSDUCTION;

HORMONES;

FOLLITROPIN; FOLLITROPIN RECEPTOR; G PROTEIN COUPLED RECEPTOR;

HORMONE;

ALPHA CHAIN; ARTICLE; BETA CHAIN; CELL SURFACE; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; CRYSTAL; DEGLYCOSYLATION; DIMERIZATION; HORMONE RECEPTOR INTERACTION; MAMMAL; OVARY FUNCTION; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR DENSITY; RECEPTOR UPREGULATION; REPRODUCTION; SIGNAL TRANSDUCTION; STIMULATION; STRUCTURE ANALYSIS; TARGET CELL; TESTIS FUNCTION;

AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLIZATION; DIMERIZATION; ELECTROSTATICS; FOLLICLE STIMULATING HORMONE, HUMAN; GLYCOSYLATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RECEPTORS, FSH; SCATTERING, RADIATION; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

MAMMALIA;

EID: 12744280744     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature03206     Document Type: Article

References (50)

1. Dias, J. A. et al. Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitam. Horm. 64, 249-322 (2002).
2. Simoni, M., Gromoll, J. & Nieschlag, E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18, 739-773 (1997).
3. Themmen, A. P. N. & Huhtaniemi, I. T. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr. Rev. 21, 551-583 (2000).
4. Pierce, J. G. & Parsons, T. F. Glycoprotein hormones: structure and function. Annu. Rev. Biochem. 50, 465-495 (1981).
5. Wu, H., Lustbader, J. W., Liu, Y., Canfield, R. E. & Hendrickson, W. A. Structure of human chorionic gonadotropin at 2.6 Å resolution from MAD analysis of the selenomethionyl protein. Structure 2, 545-558 (1994).
6. Lapthorn, A. J. et al. Crystal structure of human chorionic gonadotropin. Nature 369, 455-461 (1994).
7. Fox, K. M., Dias, J. A. & Van Roey, P. Three-dimensional structure of human follicle-stimulating hormone. Mol. Endocrinol. 15, 378-389 (2001).
8. Ascoli, M., Fanelli, F. & Segaloff, D. L. The lutropin/ choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23, 141-174 (2002).
9. Szkudlinski, M. W., Fremont, V., Ronin, C. & Weintraub, B. D. Thyroid-stimulating hormone and thyroid-stimulating hormone receptor structure-function relationships. Physiol. Rev. 82, 473-502 (2002).
10. Hsu, S. Y. T. New insights into the evolution of the relaxin-LGR signaling system. Trends Endocrinol. Metab. 14, 303-309 (2003).
11. Sugahara, T. et al. Biosynthesis of a biologically active single peptide chain containing the human common α and chorionic gonadotropin β subunits in tandem. Proc. Natl Acad. Sci. USA 92, 2041-2045 (1995).
12. Narayan, P., Wu, C. & Puett, D. Functional expression of yoked human chorionic gonadotropin in baculovirus-infected insect cells. Mol. Endocrinol. 9, 1720-1726 (1995).
13. Schmidt, A., MacColl, R., Lindau-Shepard, B., Buckler, D. R. & Dias, J. A. Hormone-induced conformational change of the purified soluble hormone binding domain of follitropin receptor complexed with single chain follitropin. J. Biol. Chem. 276, 23373-23381 (2001).
14. Jiang, X. et al. Structural predictions for the ligand-binding region of glycoprotein hormone receptors and the nature of hormone-receptor interactions. Structure 3, 1341-1353 (1995).
15. Kobe, B. & Kajava, A. V. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11, 725-732 (2001).
16. Davis, D., Liu, X. & Segaloff, D. L. Identification of the sites of N-linked glycosylation on the follicle-stimulating hormone (FSH) receptor and assessment of their role in FSH receptor function. Mol. Endocrinol. 9, 159-170 (1995).
17. Bhowmick, N., Huang, J., Puett, D., Isaacs, N. W. & Lapthorn, A. J. Determination of residues important in hormone binding to the extracellular domain of the luteinizing hormone/chorionic gonadotropin receptor by site-directed mutagenesis and modeling. Mol. Endocrinol. 10, 1147-1159 (1996).
18. Liu, C. & Dias, J. A. Long loop residues 33-58 in the human glycoprotein hormone common α subunit contain structural components for subunit heterodimerization and human follitropin-receptor binding. Arch. Biochem. Biophys. 329, 127-135 (1996).
19. Arnold, C. J. et al. The human follitropin α-subunit C terminus collaborates with a β-subunit cystine noose and an α-subunit loop to assemble a receptor-binding domain competent for signal transduction. Biochemistry 37, 1762-1768 (1998).
20. Erickson, L. D. et al. Synthetic α-subunit peptides stimulate testosterone production in vitro by rat Leydig cells. Endocrinology 126, 2555-2560 (1990).
21. Leinung, M. C., Reed, D. K., McCormick, D. J., Ryan, R. J. & Morris, J. C. Further characterization of the receptor-binding region of the thyroid-stimulating hormone α subunit: a comprehensive synthetic peptide study of the α-subunit 26-46 sequence. Proc. Natl Acad. Sci. USA 88, 9707-9711 (1991).
22. Keutmann, H. T., Mason, K. A., Kitzmann, K. & Ryan, R. J. Role of the β 93-100 determinant loop sequence in receptor binding and biological activity of human leutinizing hormone and chorionic gonadotropin. Mol. Endocrinol. 3, 526-531 (1989).
23. Moyle, W. R. et al. Co-evolution of ligand-receptor pairs. Nature 368, 251-255 (1994).
24. Dias, J. A., Zhang, Y. & Liu, X. Receptor binding and functional properties of chimeric human follitropin prepared by an exchange between a small hydrophilic intercysteine loop of human foliitropin and human lutropin. J. Biol. Chem. 269, 25289-25294 (1994).
25. Grossmann, M. et al. Substitution of the seat-belt region of the thyroid-stimulating hormone (TSH) β-subunit with the corresponding regions of choriogonadotropin or follitropin confers luteotropic but not follitropic activity to chimeric TSH. J. Biol. Chem. 272, 15532-15540 (1997).
26. Smits, G. et al. Glycoprotein hormone receptors: determinants in leucine-rich repeats responsible for ligand specificity. EMBO J. 22, 2692-2703 (2003).
27. Vischer, H. F., Granneman, J. C. M. & Bogerd, J. Opposite contribution of two ligand-selective determinants in the N-terminal hormone-binding exodomain of human gonadotropin receptors. Mol. Endocrinol. 17, 1972-1981 (2003).
28. Chen, F., Wang, Y. & Puett, D. The carboxy-terminal region of the glycoprotein hormone α-subunit: contributions to receptor binding and signaling in human chorionic gonadotropin. Mol. Endocrinol. 6, 914-919 (1992).
29. Strader, C. D., Fong, T. M., Tota, M. R., Underwood, D. & Dixon, R. A. Structures and function of G protein-coupled receptors. Annu. Rev. Biochem. 63, 101-132 (1994).
30. Palczewski, K. et al. Crystal structure of rhodopsin: a G protein-coupled receptor. Nature 289, 739-745 (2000).
31. Remy, J. et al. Mapping of HCG-receptor complexes. Mol. Cell. Endocrinol. 125, 79-91 (1996).
32. Braun, T., Schofield, P. R. & Sprengel, R. Amino-terminal leucine-rich repeats in gonadotropin receptors determine hormone selectivity. EMBO J. 10, 1885-1890 (1991).
33. Vassart, G., Pardo, L. & Costagliola, S. A molecular dissection of the glycoprotein hormone receptors. Trends Biochem. Sci. 29, 119-120 (2004).
34. Kunishima, N. et al. Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407, 971-977 (2000).
35. Costagliola, S. et al. Tyrosine sulfation is required for agonist recognition by glycoprotein hormone receptors. EMBO J. 21, 504-513 (2002).
36. Szkudlinski, M. W., Teh, N. G., Grossmann, M., Tropea, J. E. & Weintraub, B. D. Engineering human glycoprotein hormone superactive analogues. Nature Biotechnol. 14, 1257-1263 (1996).
37. Heikoop, J. C. et al. Partially deglycosylated human choriogonadotropin, stabilized by intersubunit disulfide bonds, shows full bioactivity. Eur. J. Biochem. 253, 354-356 (1998).
38. Ji, I., Zeng, H. & Ji, T. H. Receptor activation of and signal generation by the lutropin/choriogonadotropin receptor. J. Biol. Chem. 268, 22971-22974 (1993).
39. Terrillon, S. & Bouvier, M. Roles of G-protein-coupled receptor dimerization. From ontogeny to signaling regulation. EMBO Rep. 5, 30-34 (2004).
40. Grasberger, B., Minton, A. P., DeLisi, C. & Metzger, H. Interactions between proteins localized in membranes. Proc. Natl Acad. Sci. USA 83, 6258-6262 (1986).
41. Osuga, Y. et al. Co-expression of defective luteinizing hormone receptor fragments partially reconstitutes ligand-induced signal generation. J. Biol. Chem. 272, 25006-25012 (1997).
42. Ji, I. et al. Trans-activation of mutant follicle-stimulating hormone receptors selectively generates only one of two hormone signals. Mol. Endocrinol. 18, 968-978 (2004).
43. Tao, Y. X., Johnson, N. B. & Segaloff, D. L. Constitutive and agonist-dependent self-association of the cell surface human lutropin receptor. J. Biol. Chem. 279, 5904-5914 (2004).
44. Roess, D. A. & Smith, S. M. L. Self-association and raft localization of functional luteinizing hormone receptors. Biol. Reprod. 69, 1765-1770 (2003).
45. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
46. Navaza, J. Implementation of molecular replacement in AMoRe. Acta Crystallogr. D 57, 1367-1372 (2001).
47. Collaborative Computational Project, Number 4. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D 50, 760-776 (1994).
48. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in the models. Acta Crystallogr. A 47, 110-119 (1991).
49. Brunger, A. T. et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
50. Laue, T. M., Shah, B. D., Ridgeway, T. M. & Pelletier, S. L. in Analytical Ultracentrifugation in Biochemistry and Polymer Science (eds Harding, S. E., Rowe, A. J. & Horton, J. C.) 90-125 (Royal Society of Chemistry, Cambridge, 1992).