New frontier in glycoprotein hormones and their receptors structure-function

Frontiers in Endocrinology

Volumn 6, Issue OCT, 2015, Pages

  Szkudlinski, Mariusz W ^a  

^a Trophogen Inc   (United States)

Author keywords

Biobetter; Biosuperior; Charge cluster; Glycoprotein hormone; Glycoprotein hormone receptor; Protein engineering; Structure function; Super agonist

Indexed keywords

CORIFOLLITROPIN ALFA; FOLLITROPIN; GLYCOPROTEIN; HORMONE; HORMONE RECEPTOR; HORMONE RECEPTOR STIMULATING AGENT; THYROTROPIN;

ALPHA CHAIN; ARTICLE; HORMONE ACTION; HUMAN; LIGAND BINDING; MUTAGENESIS; MUTATION; NONHUMAN; OLIGOMERIZATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

EID: 84947058289     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2015.00155     Document Type: Article

References (90)

1. Szkudlinski MW, Fremont V, Ronin C, Weintraub BD. Thyroid-stimulating hormone and thyroid-stimulating hormone receptor structure-function relationships. Physiol Rev (2002) 82(2):473-502. doi:10.1152/physrev.00031.2001
2. Cahoreau C, Klett D, Combarnous Y. Structure-function relationships of glycoprotein hormones and their subunits' ancestors. Front Endocrinol (2015) 6:26. doi:10.3389/fendo.2015.00026
3. Dias JA, Cohen BD, Lindau-Shepard B, Nechamen CA, Peterson AJ, Schmidt A. Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitam Horm (2002) 64:249-322. doi:10.1016/S0083-6729(02)64008-7
4. Roch GJ, Sherwood NM. Glycoprotein hormones and their receptors emerged at the origin of metazoans. Genome Biol Evol (2014) 6(6):1466-79. doi:10.1093/gbe/evu118
5. Taddese B, Upton GJ, Bailey GR, Jordan SR, Abdulla NY, Reeves PJ, et al. Do plants contain g protein-coupled receptors? Plant Physiol (2014) 164(1):287-307. doi:10.1104/pp.113.228874
6. Farid NR, Szkudlinski MW. Minireview: structural and functional evolution of the thyrotropin receptor. Endocrinology (2004) 145(9):4048-57. doi:10.1210/en.2004-0437
7. Moyle WR, Campbell RK, Myers RV, Bernard MP, Han Y, Wang X. Co-evolution of ligand-receptor pairs. Nature (1994) 368(6468):251-5. doi:10.1038/368251a0
8. Kudo M, Chen T, Nakabayashi K, Hsu SY, Hsueh AJ. The nematode leucine-rich repeat-containing, G protein-coupled receptor (LGR) protein homologous to vertebrate gonadotropin and thyrotropin receptors is constitutively active in mammalian cells. Mol Endocrinol (2000) 14(2):272-84. doi:10.1210/mend.14.2.0422
9. Ulloa-Aguirre A, Crépieux P, Poupon A, Maurel MC, Reiter E. Novel pathways in gonadotropin receptor signaling and biased agonism. Rev Endocr Metab Disord (2011) 12(4):259-74. doi:10.1007/s11154-011-9176-2
10. Landomiel F, Gallay N, Jégot G, Tranchant T, Durand G, Bourquard T, et al. Biased signalling in follicle stimulating hormone action. Mol Cell Endocrinol (2014) 382(1):452-9. doi:10.1016/j.mce.2013.09.035
11. Van Hiel MB, Vandersmissen HP, Proost P, Vanden Broeck J. Cloning, constitutive activity and expression profiling of two receptors related to relaxin receptors in Drosophila melanogaster. Peptides (2015) 68:83-90. doi:10.1016/j.peptides.2014.07.014
12. Van Hiel MB, Vandersmissen HP, Van Loy T, Vanden Broeck J. An evolutionary comparison of leucine-rich repeat containing G protein-coupled receptors reveals a novel LGR subtype. Peptides (2012) 34(1):193-200. doi:10.1016/j.peptides.2011.11.004
13. Van Loy T, Vandersmissen HP, Van Hiel MB, Poels J, Verlinden H, Badisco L, et al. Comparative genomics of leucine-rich repeats containing G protein-coupled receptors and their ligands. Gen Comp Endocrinol (2008) 155(1):14-21. doi:10.1016/j.ygcen.2007.06.022
14. Zhang M, Tong KP, Fremont V, Chen J, Narayan P, Puett D, et al. The extracellular domain suppresses constitutive activity of the transmembrane domain of the human TSH receptor: implications for hormone-receptor interaction and antagonist design. Endocrinology (2000) 141(9):3514-7. doi:10.1210/endo.141.9.7790
15. Vassart G, Pardo L, Costagliola S. A molecular dissection of the glycoprotein hormone receptors. Trends Biochem Sci (2004) 29(3):119-26. doi:10.1016/j.tibs.2004.01.006
16. Kreuchwig A, Kleinau G, Kreuchwig F, Worth CL, Krause G. Research resource: update and extension of a glycoprotein hormone receptors web application. Mol Endocrinol (2011) 25(4):707-12. doi:10.1210/me.2010-0510
17. Hershman JM. Physiological and pathological aspects of the effect of human chorionic gonadotropin on the thyroid. Best Pract Res Clin Endocrinol Metab (2004) 18(2):249-65. doi:10.1016/j.beem.2004.03.010
18. Szkudlinski MW, Grossmann M, Weintraub BD. Progress in understanding structure-function relationships of human thyroid-stimulating hormone. Curr Opin Endocrinol Diabetes (1997) 4(5):354-63. doi:10.1097/00060793-199710000-00007
19. Rees Smith B, McLachlan SM, Furmaniak J. Autoantibodies to the thyrotropin receptor. Endocr Rev (1988) 9(1):106-21. doi:10.1210/edrv-9-1-106
20. Wallin E, von Heijne G. Properties of N-terminal tails in G-protein coupled receptors: a statistical study. Protein Eng (1995) 8(7):693-8. doi:10.1093/protein/8.7.693
21. Szkudlinski MW, Teh NG, Grossmann M, Tropea JE, Weintraub BD. Engineering human glycoprotein hormone superactive analogues. Nat Biotechnol (1996) 14(10):1257-63. doi:10.1038/nbt1096-1257
22. Szkudlinski MW. Recombinant human thyrotropins of the twenty-first century. Expert Opin Pharmacother (2004) 5(12):2435-40. doi:10.1517/14656566.5.12.2435
23. Ruddon RW. Super hormones. Nat Biotechnol (1996) 14(10):1224. doi:10.1038/nbt1096-1224
24. Szkudlinski MW. Past, presence and future of thyroid-stimulating hormone (TSH) superactive analogs. Cancer Treat Res (2004) 122:345-56. doi:10.1007/1-4020-8107-3_19
25. Heikoop JC, Huisman-de Winkel B, Grootenhuis PD. Towards minimized gonadotropins with full bioactivity. Eur J Biochem (1999) 261(1):81-4. doi:10.1046/j.1432-1327.1999.00232.x
26. Setlur SR, Dighe RR. Single chain human chorionic gonadotropin, hCGalphabeta: effects of mutations in the alpha subunit on structure and bioactivity. Glycoconj J (2007) 24(1):97-106. doi:10.1007/s10719-006-9016-x
27. Grossmann M, Weintraub BD, Szkudlinski MW. Novel insights into the molecular mechanisms of human thyrotropin action: structural, physiological, and therapeutic implications for the glycoprotein hormone family. Endocr Rev (1997) 18(4):476-501. doi:10.1210/edrv.18.4.0305
28. Jiang X, Dreano M, Buckler DR, Cheng S, Ythier A, Wu H, et al. Structural predictions for the ligand-binding region of glycoprotein hormone receptors and the nature of hormone-receptor interactions. Structure (1995) 3(12):1341-53. doi:10.1016/S0969-2126(01)00272-6
29. Remy JJ, Couture L, Pantel J, Haertlé T, Rabesona H, Bozon V, et al. Mapping of HCG-receptor complexes. Mol Cell Endocrinol (1996) 125(1-2):79-91. doi:10.1016/S0303-7207(96)03955-X
30. Pantel J, Remy JJ, Salesse R, Jolivet A, Bidart JM. Unmasking of an immunoreactive site on the alpha subunit of human choriogonadotropin bound to the extracellular domain of its receptor. Biochem Biophys Res Commun (1993) 195(2):588-93. doi:10.1006/bbrc.1993.2086
31. Kenakin T. New concepts in drug discovery: collateral efficacy and permissive antagonism. Nat Rev Drug Discov (2005) 4(11):919-27. doi:10.1038/nrd1875
32. Sanders P, Young S, Sanders J, Kabelis K, Baker S, Sullivan A, et al. Crystal structure of the TSH receptor (TSHR) bound to a blocking-type TSHR autoantibody. J Mol Endocrinol (2011) 46(2):81-99. doi:10.1530/JME-10-0127
33. Sanders J, Miguel RN, Furmaniak J, Smith BR. TSH receptor monoclonal antibodies with agonist, antagonist, and inverse agonist activities. Methods Enzymol (2010) 485:393-420. doi:10.1016/B978-0-12-381296-4.00022-1
34. Fan QR, Hendrickson WA. Structure of human follicle-stimulating hormone in complex with its receptor. Nature (2005) 433(7023):269-77. doi:10.1038/nature03206
35. Jiang X, Liu H, Chen X, Chen PH, Fischer D, Sriraman V, et al. Structure of follicle-stimulating hormone in complex with the entire ectodomain of its receptor. Proc Natl Acad Sci U S A (2012) 109(31):12491-6. doi:10.1073/pnas.1206643109
36. Jiang X, Dias JA, He X. Structural biology of glycoprotein hormones and their receptors: insights to signaling. Mol Cell Endocrinol (2014) 382(1):424-51. doi:10.1016/j.mce.2013.08.021
37. Reinfelder J, Maschauer S, Foss CA, Nimmagadda S, Fremont V, Wolf V, et al. Effects of recombinant human thyroid-stimulating hormone superagonists on thyroidal uptake of 18F-fluorodeoxyglucose and radioiodide. Thyroid (2011) 21(7):783-92. doi:10.1089/thy.2010.0394
38. Núñez Miguel R, Sanders J, Chirgadze DY, Blundell TL, Furmaniak J, Rees Smith B. FSH and TSH binding to their respective receptors: similarities, differences and implication for glycoprotein hormone specificity. J Mol Endocrinol (2008) 41(3):145-64. doi:10.1677/JME-08-0040
39. Fan QR, Hendrickson WA. Assembly and structural characterization of an authentic complex between human follicle stimulating hormone and a hormone-binding ectodomain of its receptor. Mol Cell Endocrinol (2007) 26(0-262):73-82. doi:10.1016/j.mce.2005.12.055
40. Szkudlinski MW, Teh NG, Grossmann, M, Tropea JE, Witta, J, Weintraub BD, Role of the 40-51 region of the alpha-subunit in the bioactivity of human thyrotropin and gonadotropins: implications for the design of new hormone analogs based on simultaneous mutagenesis of multiple domains. Program & Abstracts, Abstract OR1-4. 78th Annual Endocrine Society Meeting. San Francisco, CA (1996).
41. Grossmann M, Szkudlinski MW, Wong R, Dias JA, Ji TH, Weintraub BD. Substitution of the seat-belt region of the thyroid-stimulating hormone (TSH) beta-subunit with the corresponding regions of choriogonadotropin or follitropin confers luteotropic but not follitropic activity to chimeric TSH. J Biol Chem (1997) 272(24):15532-40. doi:10.1074/jbc.272.24.15532
42. Bhowmick N, Huang J, Puett D, Isaacs NW, Lapthorn AJ. 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 (1996) 10(9):1147-59. doi:10.1210/mend.10.9.8885249
43. Ulloa-Aguirre A, Zariñán T, Pasapera AM, Casas-González P, Dias JA. Multiple facets of follicle-stimulating hormone receptor function. Endocrine (2007) 32(3):251-63. doi:10.1007/s12020-008-9041-6
44. Angelova K, Fremont V, Jain R, Zhang M, Puett D, Narayan P, et al. Human alpha-subunit analogs act as partial agonists to the thyroid-stimulating hormone receptor: differential effects of free and yoked subunits. Endocrine (2004) 24(1):25-31. doi:10.1385/ENDO:24:1:025
45. Szkudlinski MW, Zhang M, Chen J, Tong KP, Leitolf H, Weintraub BD. Against the dogma: recombinant free alpha-subunit analogs with biological activity: implications for glycoprotein hormone minimization, evolution and hormone-receptor interaction. Program & Abstracts, Abstract-Hot Topic 9. 81th Annual Meeting of the Endocrine Society. San Diego, CA (1999).
46. Mueller S, Kleinau G, Szkudlinski MW, Jaeschke H, Krause G, Paschke R. The superagonistic activity of bovine thyroid-stimulating hormone (TSH) and the human TR1401 TSH analog is determined by specific amino acids in the hinge region of the human TSH receptor. J Biol Chem (2009) 284(24):16317-24. doi:10.1074/jbc.M109.005710
47. Ji I, Zeng H, Ji TH. Receptor activation of and signal generation by the lutropin/choriogonadotropin receptor. Cooperation of Asp397 of the receptor and alpha Lys91 of the hormone. J Biol Chem (1993) 268(31):22971-4.
48. Schaarschmidt J, Huth S, Meier R, Paschke R, Jaeschke H. Influence of the hinge region and its adjacent domains on binding and signaling patterns of the thyrotropin and follitropin receptor. PLoS One (2014) 9(10):e111570. doi:10.1371/journal.pone.0111570
49. Mueller S, Szkudlinski MW, Schaarschmidt J, Günther R, Paschke R, Jaeschke H. Identification of novel TSH interaction sites by systematic binding analysis of the TSHR hinge region. Endocrinology (2011) 152(8):3268-78. doi:10.1210/en.2011-0153
50. Kleinau G, Neumann S, Grüters A, Krude H, Biebermann H. Novel insights on thyroid-stimulating hormone receptor signal transduction. Endocr Rev (2013) 34(5):691-724. doi:10.1210/er.2012-1072
51. Miller TC, Jaques JT, Szkudlinski MW, Mackenzie DS. Thyrotropic activity of recombinant human glycoprotein hormone analogs and pituitary mammalian gonadotropins in goldfish (Carassius auratus): insights into the evolution of thyrotropin receptor specificity. Gen Comp Endocrinol (2012) 177(1):70-5. doi:10.1016/j.ygcen.2012.02.012
52. Grossmann M, Leitolf H, Weintraub BD, Szkudlinski MW. A rational design strategy for protein hormone superagonists. Nat Biotechnol (1998) 16(9):871-5. doi:10.1038/nbt0998-871
53. Leitolf H, Tong KP, Grossmann M, Weintraub BD, Szkudlinski MW. Bioengineering of human thyrotropin superactive analogs by site-directed "lysine-scanning" mutagenesis of the common βL3 loop of human glycoprotein hormones. Analysis of cooperative effects within and between peripheral β-hairpin loops. J Biol Chem (2000) 275(35):27457-65. doi:10.1074/jbc.M003707200
54. Szkudlinski MW, Leitolf H, Dong W, Grossmann M, Weintraub BD. Superagonists of human lutropin (hLH) and human chorionic gonadotropin (hCG) obtained by introduction of charged amino acids in the peripheral β hairpin loops. Program & Abstracts, Abstract OR28-2. 80th Annual Meeting of the Endocrine Society. New Orleans, LA (1998). 88 p.
55. Jiang X, Fischer D, Chen X, McKenna SD, Liu H, Sriraman V, et al. Evidence for follicle-stimulating hormone receptor as a functional trimer. J Biol Chem (2014) 289(20):14273-82. doi:10.1074/jbc.M114.549592
56. Campbell GA, Kurcz M, Marshall S, Meites J. Effects of starvation in rats on serum levels of follicle stimulating hormone, luteinizing hormone, thyrotropin, growth hormone and prolactin; response to LH-releasing hormone and thyrotropin-releasing hormone. Endocrinology (1977) 100(2):580-7. doi:10.1210/endo-100-2-580
57. Parrott JA, Doraiswamy V, Kim G, Mosher R, Skinner MK. Expression and actions of both the follicle stimulating hormone receptor and the luteinizing hormone receptor in normal ovarian surface epithelium and ovarian cancer. Mol Cell Endocrinol (2001) 172(1-2):213-22. doi:10.1016/S0303-7207(00)00340-3
58. Puett D, Angelova K, da Costa MR, Warrenfeltz SW, Fanelli F. The luteinizing hormone receptor: insights into structure-function relationships and hormone-receptor-mediated changes in gene expression in ovarian cancer cells. Mol Cell Endocrinol (2010) 329(1-2):47-55. doi:10.1016/j.mce.2010.04.025
59. Mertens-Walker I, Baxter RC, Marsh DJ. Gonadotropin signalling in epithelial ovarian cancer. Cancer Lett (2012) 324(2):152-9. doi:10.1016/j.canlet.2012.05.017
60. Laugwitz KL, Allgeier A, Offermanns S, Spicher K, Van Sande J, Dumont JE, et al. The human thyrotropin receptor: a heptahelical receptor capable of stimulating members of all four G protein families. Proc Natl Acad Sci U S A (1996) 93(1):116-20. doi:10.1073/pnas.93.1.116
61. Ulloa-Aguirre A, Dias JA, Bousfield G, Huhtaniemi I, Reiter E. Trafficking of the follitropin receptor. Methods Enzymol (2013) 521:17-45. doi:10.1016/B978-0-12-391862-8.00002-8
62. Fremont V, Zhang M, Weintraub BD, Szkudlinski MW. Novel insights into the molecular mechanism of glycoprotein hormone receptor activation. FASEB J (2001) 15(4):A175.
63. Nechamen CA, Thomas RM, Dias JA. APPL1, APPL2, Akt2 and FOXO1a interact with FSHR in a potential signaling complex. Mol Cell Endocrinol (2007) 260-262:93-9. doi:10.1016/j.mce.2006.08.014
64. Arey BJ, Lopez FJ. Are circulating gonadotropin isoforms naturally occurring biased agonists? Basic and therapeutic implications. Rev Endocr Metab Disord (2011) 12(4):275-88. doi:10.1007/s11154-011-9188-y
65. Langmead CJ, Christopoulos A. Supra-physiological efficacy at GPCRs: superstition or super agonists? Br J Pharmacol (2013) 169(2):353-6. doi:10.1111/bph.12142
66. Szkudlinski MW. Challenges and opportunities of trapping ligands. Mol Pharmacol (2007) 72(2):231-4. doi:10.1124/mol.107.038208
67. Dias JA, Mahale SD, Nechamen CA, Davydenko O, Thomas RM, Ulloa-Aguirre A. Emerging roles for the FSH receptor adapter protein APPL1 and overlap of a putative 14-3-3tau interaction domain with a canonical G-protein interaction site. Mol Cell Endocrinol (2010) 329(1-2):17-25. doi:10.1016/j.mce.2010.05.009
68. Calebiro D, Nikolaev VO, Lohse MJ. Imaging of persistent cAMP signaling by internalized G protein-coupled receptors. J Mol Endocrinol (2010) 45(1):1-8. doi:10.1677/JME-10-0014
69. Szkudlinski MW, Grossmann M, Leitolf H, Weintraub BD. Human thyroid-stimulating hormone: structure-function analysis. Methods (2000) 21(1):67-81. doi:10.1006/meth.2000.0976
70. Vlaeminck-Guillem V, Ho SC, Rodien P, Vassart G, Costagliola S. Activation of the cAMP pathway by the TSH receptor involves switching of the ectodomain from a tethered inverse agonist to an agonist. Mol Endocrinol (2002) 16(4):736-46. doi:10.1210/mend.16.4.0816
71. Chen CR, Salazar LM, McLachlan SM, Rapoport B. The thyrotropin receptor hinge region as a surrogate ligand: identification of loci contributing to the coupling of thyrotropin binding and receptor activation. Endocrinology (2012) 153(10):5058-67. doi:10.1210/en.2012-1376
72. Szkudlinski MW, Fremont V, Wolf V, Han Y, Wu D, Weintraub BD. Novel high affinity and long-acting recombinant bovine FSH analogs for veterinary superovulation. Program & Abstracts, Abstract 16. 18th Biennial AAVPT Symposium. Potomac, MD (2013).
73. Galli F, Manni I, Piaggio G, Balogh L, Weintraub BD, Szkudlinski MW, et al. (99m)Tc-labeled-rhTSH analogue (TR1401) for imaging poorly differentiated metastatic thyroid cancer. Thyroid (2014) 24(8):1297-308. doi:10.1089/thy.2013.0429
74. Boime I, Ben-Menahem D. Glycoprotein hormone structure-function and analog design. Recent Prog Horm Res (1999) 54:271-88.
75. Pouwer AW, Farquhar C, Kremer JA. Long-acting FSH versus daily FSH for women undergoing assisted reproduction. Cochrane Database Syst Rev (2012) 6:CD009577. doi:10.1002/14651858.CD009577.pub2
76. Croxtall JD, McKeage K. Corifollitropin alfa: a review of its use in controlled ovarian stimulation for assisted reproduction. BioDrugs (2011) 25(4):243-54. doi:10.2165/11206890-000000000-00000
77. Goletz S, Stockl L. Recombinant Human Follicle-Stimulating Hormone. USPTO US Patent Application 201301376636 (2013).
78. Yang Z, Wang S, Halim A, Schulz MA, Frodin M, Rahman SH, et al. Engineered CHO cells for production of diverse, homogeneous glycoproteins. Nat Biotechnol (2015) 33(8):842-4. doi:10.1038/nbt.3280
79. Clark E, Magner J, Skell J. Formulations for Therapeutic Administration of Thyroid Stimulating Hormone (TSH). USPTO, US Patent Application WO2008036271 (2008).
80. Louet S. Banking on a Big Biobetters Bonanza. Cpb Review (2012) 48-52.
81. Ubaldi F, Vaiarelli A, D'Anna R, Rienzi L. Management of poor responders in IVF: is there anything new? Biomed Res Int (2014) 2014:352098. doi:10.1155/2014/352098
82. Bassett JH, van der Spek A, Logan JG, Gogakos A, Bagchi-Chakraborty J, Murphy E, et al. Thyrostimulin regulates osteoblastic bone formation during early skeletal development. Endocrinology (2015) 156(9):3098-113. doi:10.1210/en.2014-1943
83. Low SC, Nunes SL, Bitonti AJ, Dumont JA. Oral and pulmonary delivery of FSH-Fc fusion proteins via neonatal Fc receptor-mediated transcytosis. Hum Reprod (2005) 20(7):1805-13. doi:10.1093/humrep/deh896
84. Vance D, Martin J, Patke S, Kane RS. The design of polyvalent scaffolds for targeted delivery. Adv Drug Deliv Rev (2009) 61(11):931-9. doi:10.1016/j.addr.2009.06.002
85. Gershengorn MC, Neumann S. Update in TSH receptor agonists and antagonists. J Clin Endocrinol Metab (2012) 97(12):4287-92. doi:10.1210/jc.2012-3080
86. Palmer SS, McKenna S, Arkinstall S. Discovery of new molecules for future treatment of infertility. Reprod Biomed Online (2005) 10(Suppl 3):45-54. doi:10.1016/S1472-6483(11)60390-8
87. Kenakin TP. Biased signalling and allosteric machines: new vistas and challenges for drug discovery. Br J Pharmacol (2012) 165(6):1659-69. doi:10.1111/j.1476-5381.2011.01749.x
88. Calebiro D, Sungkaworn T, Maiellaro I. Real-time monitoring of GPCR/cAMP signalling by FRET and single-molecule microscopy. Horm Metab Res (2014) 46(12):827-32. doi:10.1055/s-0034-1384523
89. Kenakin T. A Pharmacology Primer: Theory, Applications, and Methods. London: Academic Press (2010).
90. Szkudlinski MW, et al. Superagonists of human TSH with increased stability and prolonged plasma half-life. Thyroid (1997) 7(Suppl 1):S-8.