Cooperativity of the N- and C-terminal domains of insulin-like growth factor (IGF) binding protein 2 in IGF binding

Biochemistry

Volumn 46, Issue 48, 2007, Pages 13720-13732

  Kuang, Zhihe ^a,b   Yao, Shenggen ^a   McNeil, Kerrie A ^b   Thompson, Julian A ^c   Bach, Leon A ^c   Forbes, Briony E ^b   Wallace, John C ^b   Norton, Raymond S ^a  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGICAL MATERIALS; MOLECULAR INTERACTIONS; NUCLEAR MAGNETIC RESONANCE; PROTEINS; SPECTROSCOPIC ANALYSIS;

BINARY COMPLEXES; BIOAVAILABILITY; CYSTEINE; HIGH AFFINITY; INSULIN-LIKE GROWTH FACTOR;

INSULIN;

GLYCOSAMINOGLYCAN; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN 2;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CROSS LINKING; DISSOCIATION; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

BASE SEQUENCE; DNA PRIMERS; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 2; INSULIN-LIKE GROWTH FACTOR I; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING;

EID: 36849068849     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701251d     Document Type: Article

References (62)

1. Pollak, M. N., Schernhammer, E. S., and Hankinson, S. E. (2004) Insulin-like growth factors and neoplasia, Nat. Rev. Cancer 4, 505-518.
2. Ranke, M. B. (2005) Insulin-like growth factor-1 treatment of growth disorders, diabetes mellitus and insulin resistance, Trends Endocrinol. Metab. 16, 190-197.
3. Firth, S. M., and Baxter, R. C. (2002) Cellular actions of the insulin-like growth factor binding proteins, Endocr. Rev. 23, 824-854.
4. Denley, A., Cosgrove, L. J., Booker, G. W., Wallace, J. C., and Forbes, B. E. (2005) Molecular interactions of the IGF system, Cytokine Growth Factor Rev. 16, 421-439.
5. Hwa, V., Oh, Y., and Rosenfeld, R. G. (1999) The insulin-like growth factor-binding protein (IGFBP) superfamily, Endocr. Rev. 20, 761-787.
6. Bach, L. A., Headey, S. J., and Norton, R. S. (2005) IGF-binding proteins - the pieces are falling into place, Trends Endocrinol. Metab. 16, 228-234.
7. Carrick, F. E., Wallace, J. C., and Forbes, B. E. (2002) The interaction of insulin-like growth factor (IGFs) with insulin-like growth factor binding proteins (IGFBPs): a review, Lett. Pept. Sci. 8, 147-153.
8. Carrick, F. E., Forbes, B. E., and Wallace, J. C. (2001) B1Acore analysis of bovine insulin-like growth factor (IGF)-binding protein-2 identifies major IGF binding site determinants in both the amino- and carboxyl-terminal domains, J. Biol. Chem. 276, 27120-27128.
9. Headey, S. J., Leeding, K. S., Norton, R. S., and Bach, L. A. (2004) Contributions of the N- and C-terminal domains of insulin-like growth factor (IGF) binding protein-6 to IGF binding, J. Mol. Endocrinol. 33, 377-386.
10. Forbes, B. E., Turner, D., Hodge, S. J., McNeil, K. A., Forsberg, G., and Wallace, J. C. (1998) Localization of an insulin-like growth factor (IGF) binding site of bovine IGF binding protein-2 using disulfide mapping and deletion mutation analysis of the C-terminal domain, J. Biol. Chem. 273, 4647-4652.
11. Clemmons, D. R. (2001) Use of mutagenesis to probe IGF-binding protein structure/function relationships, Endocr. Rev. 22, 800-817.
12. Shand, J. H., Beattie, J., Song, H., Phillips, K., Kelly, S. M., Flint, D. J., and Allan, G. J. (2003) Specific amino acid substitutions determine the differential contribution of the N- and C-terminal domains of insulin-like growth factor (IGF)-binding protein-5 in binding IGF-I, J. Biol. Chem. 278, 17859-17866.
13. Yan, X., Forbes, B. E., McNeil, K. A., Baxter, R. C., and Firth, S. M. (2004) Role of N- and C-terminal residues of insulin-like growth factor (IGF)-binding protein-3 in regulating IGE complex formation and receptor activation, J. Biol. Chem. 279, 53232-53240.
14. Horney, M. J., Evangelista, C. A., and Rosenzweig, S. A. (2001) Synthesis and characterization of insulin-like growth factor (IGF)-1 photoprobes selective for the IGF-binding proteins (IGFBPS). photoaffinity labeling of the IGF-binding domain on IGFBP-2, J. Biol. Chem. 276, 2880-2889.
15. Kibbey, M. M., Jameson, M. J., Eaton, E. M., and Rosenzweig, S. A. (2006) Insulin-like growth factor binding protein-2: contributions of the C-terminal domain to IGF-1 binding, Mol. Pharmacol. 69, 833-845.
16. Headey, S. J., Keizer, D. W., Yao, S., Brasier, G., Kantharidis, P., Bach, L. A., and Norton, R. S. (2004) C-terminal domain of insulin-like growth factor (IGF) binding protein-6: structure and interaction with IGF-II, Mol. Endocrinol. 18, 2740-2750.
17. Headey, S. J., Keizer, D. W., Yao, S., Wallace, J. C., Bach, L. A., and Norton, R. S. (2004) Binding site for the C-domain of insulin-like growth factor (IGF) binding protein-6 on IGF-II; implications for inhibition of IGF actions, FEBS Lett. 568, 19-22.
18. Yao, S., Headey, S. J., Keizer, D. W., Bach, L. A., and Norton, R. S. (2004) C-terminal domain of insulin-like growth factor (IGF) binding protein 6: conformational exchange and its correlation with IGF-II binding, Biochemistry 43, 11187-11195.
19. Kalus, W., Zweckstetter, M., Renner, C., Sanchez, Y., Georgescu, J., Grol, M., Demuth, D., Schumacher, R., Dony, C., Lang, K., and Holak, T. A. (1998) Structure of the IGF-binding domain of the insulin-like growth factor-binding protein-5 (IGFBP-5): implications for IGF and IGF-I receptor interactions, EMBO J. 17, 6558-6572.
20. Zesławski, W., Beisel, H. G., Kamionka, M., Kalus, W., Engh, R. A., Huber, R., Lang, K., and Holak, T. A. (2001) The interaction of insulin-like growth factor-I with the N-terminal domain of IGFBP-5, EMBO J. 20, 3638-3644.
21. Siwanowicz, I., Popowicz, G. M., Wisniewska, M., Huber, R., Kuenkele, K. P., Lang, K., Engh, R. A., and Holak, T. A. (2005) Structural basis for the regulation of insulin-like growth factors by IGF binding proteins, Structure (London) 13, 155-167.
22. Sala, A., Capaldi, S., Campagnoli, M., Faggion, B., Labo, S., Perduca, M., Romano, A., Carrizo, M. E., Valli, M., Visai, L., Minchiotti, L., Galliano, M., and Monaco, H. L. (2005) Structure and properties of the C-terminal domain of insulin-like growth factor-binding protein-1 isolated from human amniotic fluid, J. Biol. Chem. 280, 29812-29819.
23. Sitar, T., Popowicz, G. M., Siwanowicz, I., Huber, R., and Holak, T. A. (2006) Structural basis for the inhibition of insulin-like growth factors by insulin-like growth factor-binding proteins, Proc. Natl. Acad. Sci. U.S.A. 103, 13028-13033.
24. Kuang, Z., Yao, S., Keizer, D. W., Wang, C. C., Bach, L. A., Forbes, B. E., Wallace, J. C., and Norton, R. S. (2006) Structure, dynamics and heparin binding of the C-terminal domain of insulin-like growth factor-binding protein-2 (IGFBP-2). J. Mol. Biol. 364, 690-704.
25. Chandrashekaran, I. R., Yao, S., Wang, C. C., Bansal, P. S., Alewood, P. F., Forbes, B. E., Wallace, J. C., Bach, L. A., and Norton, R. S. (2007) The N-terminal subdomain of insulin-like growth factor (IGF) binding protein 6. Structure and interaction with IGFs, Biochemistry 46, 3065-3074.
26. Ho, P. J., and Baxter, R. C. (1997) Characterization of truncated insulin-like growth factor-binding protein-2 in human milk, Endocrinology 138, 3811-3818.
27. Vorwerk, P., Hohmann, B., Oh, Y., Rosenfeld, R. G., and Shymko, R. M. (2002) Binding properties of insulin-like growth factor binding protein-3 (1GFBP-3), 1GFBP-3 N- and C-terminal fragments, and structurally related proteins mac25 and connective tissue growth factor measured using a biosensor. Endocrinology 143, 1677-1685.
28. Payet, L. D., Wang, X. H., Baxter, R. C. and Firth, S. M. (2003) Amino- and carboxyl-terminal fragments of insulin-like growth factor (IGF) binding protein-3 cooperate to bind IGFs with high affinity and inhibit IGF receptor interactions, Endocrinology 144, 2797-2806.
29. Mark, S., Kubler, B., Honing, S., Oesterreicher, S., John, H., Braulke, T., Forssmann, W. G., and Standker, L. (2005) Diversity of human insulin-like growth factor (IGF) binding protein-2 fragments in plasma: primary structure, IGF-binding properties, and disulfide bonding pattern, Biochemistry 44, 3644-3652.
30. Qin, X., Strong, D. D., Baylink, D. J., and Mohan, S. (1998) Structure-function analysis of the human insulin-like growth factor binding protein-4, J. Biol. Chem. 273, 23509-23516.
31. Fernandez-Toniero, C., Lozano, R. M., Rivas, G., Jimenez, M. A., Standker, L., Diaz-Gonzalez, D., Forssmann, W. G., Cuevas, P., Romero, A., and Gimenez-Gallego, G. (2005) Synthesis of the blood circulating C-terminal fragment of insulin-like growth factor (IGF)-binding protcin-4 in its native conformation. Crystallization, heparin and IGF binding, and osteogenic activity, J. Biol. Chem. 280, 18899-18907.
32. Arai, T., Busby, W., Jr., and Clemmons, D. R. (1996) Binding of insulin-like growth factor (IGF) I or II to IGF-binding protein-2 enables it to bind to heparin and extracellular matrix. Endocrinology 137, 4571-4575.
33. Russo, V. C., Bach, L. A., Fosang, A. J., Baker, N. L., and Werther, G. A. (1997) Insulin-like growth factor binding protein-2 binds to cell surface proleoglycans in the rat brain olfactory bulb. Endocrinology 138, 4858-4867.
34. Song, H., Shand, J. H., Beattie, J., Flint, D. J., and Allan, G. J. (2001) The carboxy-terminal domain of IGF-binding protein-5 inhibits heparin binding to a site in the central domain, J. Mol. Endocrinol. 26, 229-239.
35. King, R., Wells, J. R., Krieg, P., Snoswell, M., Brazier, J., Bagley, C. J., Wallace, J. C., Ballard, F. J., Ross, M., and Francis, G. L. (1992) Production and characterization of recombinant insulin-like growth factor-I (IGF-I) and potent analogues of IGF-I, with Gly or Arg substituted for Glu3, following their expression in Escherichia coli as fusion proteins, J. Mol. Endocrinol. 8, 29-41.
36. 15N chemical shift referencing in biomolecular NMR, J. Biomol. NMR 6, 135-140.
37. Bartels, C., Xia, T. H., Billeter, M., Güntert, P., and Wüthrich, K. (1995) The program XEASY for computer-supported NMR spectral-analysis of biological macromolecules, J. Biomol. NMR 6, 1-10.
38. Carrick, F. E., Hinds, M. G., McNeil, K. A., Wallace, J. C., Forbes, B. E., and Norton, R. S. (2005) Interaction of insulin-like growth factor (IGF)-1 and -II with IGF binding protein-2: mapping the binding surfaces by nuclear magnetic resonance, J. Mol. Endocrinol. 34, 685-698.
39. Denley, A., Wang, C. C., McNeil, K. A., Walenkamp, M. J., van Duyvenvoorde, H., Wit, J. M., Wallace, J. C., Norton, R. S., Karperien, M., and Forbes, B. E. (2005) Structural and functional characteristics of the Val44Met insulin-like growth factor I missense mutation: correlation with effects on growth and development, Mol. Endocrinol. 19, 711-721.
40. Zuiderweg, E. R. (2002) Mapping protein-protein interactions in solution by NMR spectroscopy, Biochemistry 41, 1-7.
41. Vajdos, F. F., Ultsch, M., Schaffer, M. L., Deshayes, K. D., Liu, J., Skelton, N. J., and de Vos, A. M. (2001) Crystal structure of human insulin-like growth factor-1: detergent binding inhibits binding protein interactions, Biochemistry 40, 11022-11029.
42. Brzozowski, A. M., Dodson, E. J., Dodson, G. G., Murshudov, G. N., Verma, C., Turkenburg, J. P., de Bree, F. M., and Dauter, Z. (2002) Structural origins of the functional divergence of human insulin-like growth factor-1 and insulin. Biochemistry 41, 9389-9397.
43. Haigh, C. W., and Mallion, R. B. (1979) Ring current theories in nuclear magnetic resonance, Prog. NMR Spectrosc. 13, 303-344.
44. Cooke, R. M., Harvey, T. S., and Campbell, I. D. (1991) Solution structure of human insulin-like growth factor-1: a nuclear magnetic resonance and restrained molecular dynamics study, Biochemistry 30, 5484-5491.
45. Laajoki, L. G., Francis, G. L., Wallace, J. C., Carver, J. A., and Keniry, M. A. (2000) Solution structure and backbone dynamics of long-[Arg(3)]insulin-like growth factor-I, J. Biol. Chem. 275, 10009-10015.
46. 1H-NMR and distance geometry, Int. J. Pept. Protein Res. 41, 433-440.
47. Terasawa, H., Kohda, D., Hatanaka, H., Nagata, K., Higashihashi, N., Fujiwara, H., Sakano, K., and Inagaki, F. (1994) Solution structure of human insulin-like growth factor II; recognition sites for receptors and binding proteins, EMBO J. 13, 5590-5597.
48. Torres, A. M., Forbes, B. E., Aplin, S. E., Wallace, J. C., Francis, G. L., and Norton, R. S. (1995) Solution structure of human insulin-like growth factor II. Relationship to receptor and binding protein interactions. J. Mol. Biol. 248, 385-401.
49. Clemmons, D. R., Dehoff, M. L., Busby, W. H., Bayne, M. L., and Cascieri, M. A. (1992) Competition for binding to insulin-like growth factor (IGF) binding protein-2, 3, 4, and 5 by the IGFs and IGF analogs, Endocrinology 131, 890-895.
50. Oh, Y., Mueller, H. L., Lee, D. Y., Fielder, P. J., and Rosenfeld, R. G. (1993) Characterization of the affinities of insulin-like growth factor (IGF)-binding protein -1 to -4 for IGF-I, IGF-II, IGF-1/insulin hybrid, and IGF-1 analogs, Endocrinology 132, 1337-1344.
51. Dubaquie, Y., and Lowman, H. B. (1999) Total alanine-scanning mutagenesis of insulin-like growth factor I (IGF-1) identifies differential binding epitopes for IGFBP-1 and IGFBP-3, Biochemistry 38, 6386-6396.
52. Bach, L. A., Hsieh, S., Sakano, K., Fujiwara, H., Perdue, J. F., and Rechler, M. M. (1993) Binding of mutants of human insulin-like growth factor II to insulin-like growth factor binding proteins 1-6, J. Biol. Chem. 268, 9246-9254.
53. Arai, T., Parker, A., Busby, W., Jr., and Clemmons, D. R. (1994) Heparin, heparan sulfate, and dermatan sulfate regulate formation of the insulin-like growth factor-I and insulin-like growth factor-binding protein complexes, J. Biol. Chem. 269, 20388-20393.
54. Hoeflich, A., Reisinger, R., Lahm, H., Kiess, W., Blum, W. F., Kolb, H. J., Weber, M. M., and Wolf, E. (2001) Insulin-like growth factor-binding protein 2 in tumorigenesis: protector or promoter?, Cancer Res. 61, 8601-8610.
55. Zhang, W., Wang, H., Song, S. W., and Fuller, G. N. (2002) Insulin-like growth factor binding protein 2: gene expression microarrays and the hypothesis-generation paradigm, Brain Pathol. 12, 87-94.
56. Fukushima, T., Tezuka, T., Shimomura, T., Nakano, S., and Kataoka, H. (2007) Silencing of insulin-like growth factor binding protein-2 (IGFBP-2) in human glioblastoma cells reduces both invasiveness and expression of progression-associated gene CD24, J. Biol. Chem. 282, 18634-18644.
57. Bunn, R. C., and Fowlkes, J. L. (2003) Insulin-like growth factor binding protein proteolysis, Trends Endocrinol. Metab. 14, 176-181.
58. Beattie, J., Phillips, K., Shand, J. H., Szymanowska, M., Flint, D. J., and Allan, G. J. (2005) Molecular recognition characteristics in the insulin-like growth factor (IGF)-insulin-like growth factor binding protein -3/5 (IGFBP-3/5) heparin axis, J. Mol. Endocrinol. 34, 163-175.
59. Hua, Q. X., Shoelson, S. E., Kochoyan, M., and Weiss, M. A. (1991) Receptor binding redefined by a structural switch in a mutant human insulin, Nature 354, 238-241.
60. Dong, J., Wan, Z., Popov, M., Carey, P. R., and Weiss, M. A. (2003) Insulin assembly damps conformational fluctuations: Raman analysis of amide I linewidths in native states and fibrils, J. Mol. Biol. 330, 431-442.
61. Hua, Q. X., Nakagawa, S., Hu, S. Q., Jia, W., Wang, S., and Weiss, M. A. (2006) Toward the active conformation of insulin: stereospecific modulation of a structural switch in the B chain, J. Biol. Chem. 281, 24900-24909.
62. Schaffer, M. L., Deshayes, K., Nakamura, G., Sidhu, S., and Skelton, N. J. (2003) Complex with a phage display-derived peptide provides insight into the function of insulin-like growth factor I, Biochemistry 42, 9324-9334.