Assembly and structural characterization of an authentic complex between human follicle stimulating hormone and a hormone-binding ectodomain of its receptor

Molecular and Cellular Endocrinology

Volumn 260-262, Issue , 2007, Pages 73-82

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

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Crystal structure; Glycoprotein hormones; Gonadotropin receptors; Insect cell expression

Indexed keywords

FOLLITROPIN; FOLLITROPIN RECEPTOR; HETERODIMER;

ANIMAL CELL; ARTICLE; BACULOVIRUS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; INSECT CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING;

ANIMALS; BACULOVIRIDAE; CHORIONIC GONADOTROPIN; CHROMATOGRAPHY, GEL; CRYSTALLIZATION; DIMERIZATION; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GLYCOPROTEIN HORMONES, ALPHA SUBUNIT; GLYCOSYLATION; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, FSH; SOLUBILITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 33751243638     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2005.12.055     Document Type: Article

References (55)

1. Arnold C.J., Liu C., Lindau-Shepard B., Losavio M.L., Patrascu M.T., and Dias J.A. 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 (1998) 1762-1768
2. Ascoli M., Fanelli F., and Segaloff D.L. The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23 (2002) 141-174
3. Bhowmick N., Huang J., Puett D., Isaacs N.W., and 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 (1996) 1147-1159
4. Bhowmick N., Narayan P., and Puett D. Identification of ionizable amino acid residues on the extracellular domain of the lutropin receptor involved in ligand binding. Endocrinology 140 (1999) 4558-4563
5. Campbell R.K., Dean-Emig D.M., and Moyle W.R. Conversion of human choriogonadotropin into follitropin by protein chemistry. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 760-764
6. Carson M. Ribbons. Methods Enzymol. 277 (1997) 493-505
7. Chen F., Wang Y., and 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 (1992) 914-919
8. Dias J.A., Zhang Y., and Liu X. Receptor binding and functional properties of chimeric human follitropin prepared by an exchange between a small hydrophilic intercysteine loop of human follitropin and human lutropin. J. Biol. Chem. 269 (1994) 25289-25294
9. Dias J.A., and Van Roey P. Structural biology of human follitropin and its receptor. Arch. Med. Res. 32 (2001) 510-519
10. Dias J.A., Cohen B.D., Lindau-Shepard B., Nechamen C.A., Peterson A.J., and Schmidt A. Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitam. Horm. 64 (2002) 249-322
11. Dumas J.J., Kumar R., McDonagh T., Sullivan F., Stahl M.L., Somers W.S., and Mosyak L. Crystal structure of the wild-type von Willebrand factor A1-glycoprotein Ibα complex reveals conformation differences with a complex bearing von Willebrand disease mutations. J. Biol. Chem. 279 (2004) 23327-23334
12. Erickson L.D., Rizza S.A., Bergert E.R., Charlesworth M.C., McCormick D.J., and Ryan R.J. Synthetic alpha-subunit peptides stimulate testosterone production in vitro by rat Leydig cells. Endocrinology 126 (1990) 2555-2560
13. Fan Q.R., and Hendrickson W.A. Structure of human follicle-stimulating hormone in complex with its receptor. Nature 433 (2005) 269-277
14. Fan Q.R., and Hendrickson W.A. Structural biology of glycoprotein hormones and their receptors. Endocrine 26 (2005) 179-188
15. Fotiadis D., Liang Y., Filipek S., Saperstein D.A., Engel A., and Palczewski K. The G protein-coupled receptor rhodopsin in the native membrane. FEBS Lett. 564 (2004) 281-288
16. Fox K.M., Dias J.A., and Van Roey P. Three-dimensional structure of human follicle-stimulating hormone. Mol. Endocrinol. 15 (2001) 378-389
17. Grossmann M., Szkudlinski M.W., Zeng H., Kraiem Z., Ji I., Tropea J.E., Ji T.H., and Weintraub B.D. Role of the carboxy-terminal residues of the alpha-subunit in the expression and bioactivity of human thyroid-stimulating hormone. Mol. Endocrinol. 9 (1995) 948-958
18. Grossmann M., Szkudlinski M.W., Wong R., Dias J.A., Ji T.H., and Weintraub B.D. Substitution of the seat-belt region of the thyroid-stimulating hormone (TSH) β-subunit with the corresponding regions of choriogonandotropin or follitropin confers luteotropic but not follitropic activity to chimeric TSH. J. Biol. Chem. 272 (1997) 15532-15540
19. Huizinga E.G., Tsuji S., Romijn R.A., Schiphorst M.E., de Groot P.G., Sixma J.J., and Gros P. Structures of glycoprotein Ibα and its complex with von Willebrand factor A1 domain. Science 297 (2002) 1176-1179
20. Jiang X., Dreano M., Buckler D.R., Cheng S., Ythier A., Wu H., Hendrickson W.A., and Tayar N.E. Structural predictions for the ligand-binding region of glycoprotein hormone receptors and the nature of hormone-receptor interactions. Structure 3 (1995) 1341-1353
21. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in the models. Acta Crystallogr. A 47 (1991) 110-119
22. Kajava A.V., Vassart G., and Wodak S.J. Modeling of the three-dimensional structure of proteins with the typical leucine-rich repeats. Structure 3 (1995) 867-877
23. Keutmann H.T., Charlesworth M.C., Mason K.A., Ostrea T., Johnson L., and Ryan R.J. A receptor-binding region in human choriogo nadotropin/lutropin beta subunit. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 2038-2042
24. Keutmann H.T., Mason K.A., Kitzmann K., and 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 (1989) 526-531
25. Kleinau G., Jäschke H., Neumann S., Lättig J., Paschke R., and Krause G. Identification of a novel epitope in the thyroid-stimulating hormone receptor ectodomain acting as intramolecular signaling interface. J. Biol. Chem. 279 (2004) 51590-51600
26. Kleywegt G.J. Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D 52 (1996) 842-857
27. Kobe B., and Deisenhofer J. Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature 366 (1993) 751-756
28. Kobe B., and Deisenhofer J. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature 374 (1995) 183-186
29. Kunishima N., Shimada Y., Tsuji Y., Sato T., Yamamoto M., Kumasaka T., Nakanishi S., Jingami H., and Morikawa K. Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407 (2000) 971-977
30. Lapthorn A.J., Harris D.C., Littlejohn A., Lustbader J.W., Canfield R.E., Machin K.J., Morgan F.J., and Isaacs N.W. Crystal structure of human chorionic gonadotropin. Nature 369 (1994) 455-461
31. Leinung M.C., Reed D.K., McCormick D.J., Ryan R.J., and 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. U.S.A. 88 (1991) 9707-9711
32. Liu C., and 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 (1996) 127-135
33. Moyle W.R., Campbell R.K., Myers R.V., Bernard M.P., Han Y., and Wang X. Co-evolution of ligand-receptor pairs. Nature 368 (1994) 251-255
34. Moyle W.R., Campbell R.K., Rao S.N.V., Ayad N.G., Bernard M.P., Han Y., and Wang Y. Model of human chorionic gonadotropin and lutropin receptor interaction that explains signal transduction of the glycoprotein hormones. J. Biol. Chem. 270 (1995) 20020-20031
35. Moyle W.R., Xing Y., Lin W., Cao D., Myers R.V., Kerrigan J.E., and Bernard M.P. Model of glycoprotein hormone receptor ligand binding and signaling. J. Biol. Chem. 279 (2004) 44442-44459
36. Moyle W.R., Lin W., Myers R.V., Cao D., Kerrigan J.E., and Bernard M.P. Models of glycoprotein hormone receptor interaction. Endocrine 26 (2005) 189-205
37. Narayan P., Wu C., and Puett D. Functional expression of yoked human chorionic gonadotropin in baculovirus-infected insect cells. Mol. Endocrinol. 9 (1995) 1720-1726
38. Pierce J.G., and Parsons T.F. Glycoprotein hormones: structure and function. Annu. Rev. Biochem. 50 (1981) 465-495
39. Santa Coloma T.A., and Reichert L.E.J. Identification of a follicle-stimulating hormone receptor-binding region in hFSH-β-(81-95) using synthetic peptides. J. Biol. Chem. 265 (1990) 5037-5042
40. Schmidt A., MacColl R., Lindau-Shepard B., Buckler D.R., and 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 (2001) 23373-23381
41. Schubert W.D., Urbanke C., Ziehm T., Beier V., Machner M.P., Domann E., Wehland J., Chakraborty T., and Heinz D.W. Structure of Internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111 (2002) 825-836
42. Simoni M., Gromoll J., and Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18 (1997) 739-773
43. Smits G., Govaerts C., Nubourgh I., Pardo L., Vassart G., and Costagliola S. 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. Mol. Endocrinol. 16 (2002) 722-735
44. Smits G., Campillo M., Govaerts C., Janssens V., Richter C., Vassart G., Pardo L., and Costagliola S. Glycoprotein hormone receptors: determinants in leucine-rich repeats responsible for ligand specificity. EMBO J. 22 (2003) 2692-2703
45. Sohn J., Youn H., Jeoung M., Koo Y., Yi C., Ji I., and Ji T.H. Orientation of follicle-stimulating hormone (FSH) subunits complexed with the FSH receptor. J. Biol. Chem. 278 (2003) 47868-47876
46. Song Y.S., Ji I., Beauchamp J., Isaacs N.W., and Ji T.H. Hormone interactions to leu-rich repeats in the gonadotropin receptors. J. Biol. Chem. 276 (2001) 3426-3435
47. Sugahara T., Pixley M.R., Minami S., Perlas E., Ben-Menahem D., Hsueh A.J., and Boime I. Biosynthesis of a biologically active single peptide chain containing the human common α and chorionic gonadotropin β subunits in tandem. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 2041-2045
48. Szkudlinski M.W., Fremont V., Ronin C., and Weintraub B.D. Thyroid-stimulating hormone and thyroid-stimulating hormone receptor structure-function relationships. Physiol. Rev. 82 (2002) 473-502
49. Themmen A.P.N., and Huhtaniemi I.T. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr. Rev. 21 (2000) 551-583
50. Uff S., Clemetson J.M., Harrison T., Clemetson K.J., and Emsley J. Crystal structure of the platelet glycoprotein Ibα N-terminal domain reveals an unmasking mechanism for receptor activation. J. Biol. Chem. 277 (2002) 35657-35663
51. Urizar E., Montanelli L., Loy T., Bonomi M., Swillens S., Gales C., Bouvier M., Smits G., Vassart G., and Costagliola S. Glycoprotein hormone receptors: link between receptor homodimerization and negative cooperativity. EMBO J. 24 (2005) 1954-1964
52. Vischer H.F., Granneman J.C.M., and Bogerd J. Opposite contribution of two ligand-selective determinants in the N-terminal hormone-binding exodomain of human gonadotropin receptors. Mol. Endocrinol. 17 (2003) 1972-1981
53. Vischer H.F., Granneman J.C.M., Noordam M.J., Mosselman S., and Bogerd J. Ligand selectivity of gonadotropin receptors. J. Biol. Chem. 278 (2003) 15505-15513
54. Wu H., Lustbader J.W., Liu Y., Canfield R.E., and Hendrickson W.A. Structure of human chorionic gonadotropin at 2.6 Å resolution from MAD analysis of the selenomethionyl protein. Structure 2 (1994) 545-558
55. Yoo J., Zeng H., Ji I., Murdoch W.J., and Ji T.H. COOH-terminal amino acids of the α subunit play common and different roles in human choriogonadotropin and follitropin. J. Biol. Chem. 268 (1993) 13034-13042