Mathematical model of human growth hormone (hGH)-stimulated cell proliferation explains the efficacy of hGH variants as receptor agonists or antagonists

Biotechnology Progress

Volumn 20, Issue 5, 2004, Pages 1337-1344

  Haugh, Jason M ^a  

^a North Carolina State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOASSAY; CELLS; FUNCTIONS; MATHEMATICAL MODELS;

CELL-BASED ASSAYS; HUMAN GROWTH HORMONE (HGH); RECEPTOR VARIANTS;

HORMONES;

EID: 5444235675     PISSN: 87567938     EISSN: None     Source Type: Journal    
DOI: 10.1021/bp0499101     Document Type: Article

References (38)

1. Wells, J. A. Binding in the growth hormone receptor complex. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 1-6.
2. Behncken, S. N.; Waters, M. J. Molecular recognition events involved in the activation of the growth hormone receptor by growth hormone. J. Mol. Recognit. 1999, 12, 355-362.
3. de Vos, A. M.; Ultsch, M.; Kossiakoff, A. A. Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science 1992, 255, 306-312.
4. Cunningham, B. C.; Wells, J. A. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 1989, 244, 1081-1085.
5. Bass, S. H.; Mulkerrin, M. G.; Wells, J. A. A systematic mutational analysis of hormone-binding determinants in the human growth hormone receptor. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 4498-4502.
6. Cunningham, B. C.; Wells, J. A. Rational design of receptor-specific variants of human growth hormone. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 3407-3411.
7. Lowman, H. B.; Bass, S. H.; Simpson, N.; Wells, J. A. Selecting high-affinity binding proteins by monovalent phage display. Biochemistry 1991, 30, 10832-10838.
8. Cunningham, B. C.; Wells, J. A. Comparison of a structural and a functional epitope. J. Mol. Biol. 1993, 234, 554-563.
9. Lowman, H. B.; Wells, J. A. Affinity maturation of human growth hormone by monovalent phage display. J. Mol. Biol. 1993, 234, 564-578.
10. Cunningham, B. C.; Ultsch, M.; de Vos, A. M.; Mulkerrin, M. G.; Clauser, K. R.; Wells, J. A. Dimerization of the extracellular domain of the human growth hormone receptor by a single hormone molecule. Science 1991, 254, 821-825.
11. Fuh, G.; Cunningham, B. C.; Fukunaga, R.; Nagata, S.; Goeddel, D. V.; Wells, J. A. Rational design of potent antagonists to the human growth hormone receptor. Science 1992, 256, 1677-1680.
12. Zhu, T.; Goh, E. L. K.; Graichen, R.; Ling, L.; Lobie, P. E. Signal transduction via the growth hormone receptor. Cell. Signalling 2001, 13, 599-616.
13. Perelson, A. S.; DeLisi, C. Receptor clustering on a cell surface: I. Theory of receptor cross-linking by ligands bearing two chemically identical functional groups. Math. Biosci. 1980, 48, 71-110.
14. Ilondo, M. M.; Damholt, A. B.; Cunningham, B. C.; Wells, J. A.; De Meyts, P.; Shymko, R. M. Receptor dimerization determines the effects of growth hormone in primary rat adipocytes and cultured human IM-9 lymphocytes. Endocrinology 1994, 134, 2397-2403.
15. Uchida, H.; Banba, S.; Wada, M.; Matsumoto, K.; Ikeda, M.; Naito, N.; Tanaka, E.; Honjo, M. Analysis of binding properties between 20 kDa human growth hormone (hGH) and hGH receptor (hGHR): the binding affinity for hGHR extracellular domain and mode of receptor dimerization. J. Mol. Endocrinol. 1999, 23, 347-353.
16. Tsunekawa, B.; Wada, M.; Ikeda, M.; Banba, S.; Kamachi, H.; Tanaka, E.; Honjo, M. The binding between the stem regions of human growth hormone (GH) receptor compensates for the weaker site 1 binding of 20-kDa human GH (hGH) than that of 22-kDa hGH. J. Biol. Chem. 2000, 275, 15652-15656.
17. Pearce, K. H.; Cunningham, B. C.; Fuh, G.; Teeri, T.; Wells, J. A. Growth hormone binding affinity for its receptor surpasses the requirements for cellular activity. Biochemistry 1999, 38, 81-89.
18. Kopchick, J. J.; Parkinson, C.; Stevens, E. C.; Trainer, P. J. Growth hormone receptor antagonists: discovery, development, and use in patients with acromegaly. Endocr. Rev. 2002, 23, 623-646.
19. Lesniak, M. A.; Roth, J. Regulation of receptor concentration by homologous hormone: effect of human growth hormone on its receptor in IM-9 lymphocytes. J. Biol. Chem. 1976, 251, 3720-3729.
20. Hizuka, N.; Gorden, P.; Lesniak, M. A.; Van Obberghen, E.; Carpentier, J.; Orci, L. Polypeptide hormone degradation and receptor regulation are coupled to ligand internalization. J. Biol. Chem. 1981, 256, 4591-4597.
21. Wiley: H. S.; Cunningham, D. D. A steady-state model for analyzing the cellular binding, internalization and degradation of polypeptide ligands. Cell 1981, 25, 433-440.
22. Starbuck, C.; Lauffenburger, D. A. Mathematical model for the effects of epidermal growth factor receptor trafficking dynamics on fibroblast proliferation responses. Biotechnol. Prog. 1992, 8, 132-143.
23. Fallon, E. M.; Lauffenburger, D. A. Computational model for effects of ligand/receptor binding properties on interleukin-2 trafficking dynamics and T cell proliferation response. Biotechnol. Prog. 2000, 16, 905-916.
24. Sarkar, C. A.; Lauffenburger, D. A. Cell-level pharmacokinetic model of granulocyte colony-stimulating factor: implications for ligand lifetime and potency in vivo. Mol. Pharmacol. 2003, 63, 147-158.
25. Lauffenburger, D. A.; Fallon, E. M.; Haugh, J. M. Scratching the (cell) surface: cytokine engineering for improved ligand/receptor trafficking dynamics. Chem. Biol. 1998, 5, R257-R263.
26. Rowlinson, S. W.; Barnard, R.; Bastiras, S.; Robins, A. J.; Brinkworth, R.; Waters, M. J. A growth hormone agonist produced by targeted mutagenesis at binding site-1: evidence that site-1 regulates bioactivity. J. Biol. Chem. 1995, 270, 16833-16839.
27. Clark, R.; Olson, K.; Fuh, G.; Marian, M.; Mortensen, D.; Teshima, F.; Chang, S.; Chu, H.; Mukku, V.; Canova-Davis, E.; Somer, T.; Cronin, M.; Winkler, M.; Wells, J. A. Long-acting growth hormones produced by conjugation with polyethylene glycol. J. Biol. Chem. 1996, 271, 21969-21977.
28. Schiffer, C.; Ultsch, M.; Walsh, S.; Somers, W.; de Vos, A. M.; Kossiakoff, A. Structure of a phage display-derived variant of human growth hormone complexed to two copies of the extracellular domain of its receptor: evidence for strong structural coupling between receptor binding sites. J. Mol. Biol. 2002, 316, 277-289.
29. Pal, G.; Kossiakoff, A. A.; Sidhu, S. S. The functional binding epitope of a high affinity variant of human growth hormone mapped by shotgun alanine-scanning mutagenesis: insights into the mechanisms responsible for improved affinity. J. Mol. Biol. 2003, 332, 195-204.
30. Silva, C. M.; Weber, M. J.; Thorner, M. O. Stimulation of tyrosine phosphorylation in human cells by activation of the growth hormone receptor. Endocrinology 1993, 132, 101-108.
31. Northrup, S. H.; Erickson, H. P. Kinetics of protein-protein association explained by Brownian dynamics computer simulation. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 3338-3342.
32. Selzer, T.; Albeck, S.; Schreiber, G. Rational design of faster associating and tighter binding protein complexes. Nat. Struct. Biol. 2000, 7, 537-541.
33. Boder, E. T.; Wittrup, K. D. Optimal screening of surface-displayed polypeptide libraries. Biotechnol. Prog. 1998, 14, 55-62.
34. Black, J. W.; Leff, P. Operational models of pharmacological agonism. Proc. R. Soc. London, Ser. B 1983, 220, 141-162.
35. Sarkar, C. A.; Lowenhaupt, K.; Wang, P. J.; Horan, T.; Lauffenburger, D. A. Parsing the effects of binding, signaling, and trafficking on the mitogenic potencies of granulocyte colony-stimulating factor analogues. Biotechnol. Prog. 2003, 19, 955-964.
36. Bernat, B.; Pal, G.; Sun, M.; Kossiakoff, A. A. Determination of the energetics governing the regulatory step in growth hormone-induced receptor homodimerization. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 952-957.
37. Lauffenburger, D. A.; Linderman, J. L. Receptors: Models for Binding, Trafficking, and Signaling; Oxford University Press: New York, 1993.
38. Ishizaka-Ikeda, E.; Fukunaga, R.; Wood, W. I.; Goeddel, D. V.; Nagata, S. Signal transduction mediated by growth hormone receptor and its chimeric molecules with the granulocyte colony-stimulating factor receptor. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 123-127.