Interactions that influence the binding of synthetic heparan sulfate based disaccharides to fibroblast growth factor-2

ACS Chemical Biology

Volumn 9, Issue 8, 2014, Pages 1712-1717

  Li, Yi Ching ^a   Ho, I Hsin ^b   Ku, Chiao Chu ^c   Zhong, Yong Qing ^b   Hu, Yu Peng ^b   Chen, Zhi Geng ^b   Chen, Chun Yen ^b   Lin, Wei Chen ^b   Zulueta, Medel Manuel L ^b   Hung, Shang Cheng ^b   Lin, Min Guan ^a,d   Wang, Cheng Chung ^c   Hsiao, Chwan Deng ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b GENOMICS RESEARCH CENTER   (Taiwan)

^c INSTITUTE OF CHEMISTRY   (Taiwan)

^d NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DISACCHARIDE; FIBROBLAST GROWTH FACTOR 2; GLUCOSAMINE; HEPARAN SULFATE;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISSOCIATION CONSTANT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STEREOCHEMISTRY; SULFONATION; X RAY DIFFRACTION; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DISACCHARIDES; FIBROBLAST GROWTH FACTOR 2; HEPARITIN SULFATE; MODELS, MOLECULAR;

EID: 84906231964     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500298q     Document Type: Article

References (30)

1. Beenken, A. and Mohammadi, M. (2009) The FGF family: biology, pathophysiology and therapy Nat. Rev. Drug Discovery 8, 235-253
2. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology Nature 446, 1030-1037
3. Gandhi, N. S. and Mancera, R. L. (2008) The structure of glycosaminoglycans and their interactions with proteins Chem. Biol. Drug Des. 72, 455-482
4. Linhardt, R. J. (2003) Heparin: structure and activity J. Med. Chem. 46, 2551-2564
5. Noti, C., de Paz, J. L., Polito, L., and Seeberger, P. H. (2006) Preparation and use of microarrays containing synthetic heparin oligosaccharides for the rapid analysis of heparin-protein interactions Chem.-Eur. J. 12, 8664-8686
6. Baleux, F., Loureiro-Morais, L., Hersant, Y., Clayette, P., Arenzana-Seisdedos, F., Bonnaffe, D., and Lortat-Jacob, H. (2009) A synthetic CD4-heparan sulfate glycoconjugate inhibits CCR5 and CXCR4 HIV-1 attachment and entry Nat. Chem. Biol. 5, 743-748
7. Arungundram, S., Al-Mafraji, K., Asong, J., Leach, F. E., 3rd, Amster, I. J., Venot, A., Turnbull, J. E., and Boons, G. J. (2009) Modular synthesis of heparan sulfate oligosaccharides for structure-activity relationship studies J. Am. Chem. Soc. 131, 17394-17405
8. Wang, Z., Xu, Y., Yang, B., Tiruchinapally, G., Sun, B., Liu, R., Dulaney, S., Liu, J., and Huang, X. (2010) Preactivation-based, one-pot combinatorial synthesis of heparin-like hexasaccharides for the analysis of heparin-protein interactions Chem.-Eur. J. 16, 8365-8375
9. Hu, Y. P., Lin, S. Y., Huang, C. Y., Zulueta, M. M. L., Liu, J. Y., Chang, W., and Hung, S. C. (2011) Synthesis of 3- O -sulfonated heparan sulfate octasaccharides that inhibit the herpes simplex virus type 1 host-cell interaction Nat. Chem. 3, 557-563
10. Zulueta, M. M. L., Lin, S. Y., Lin, Y. T., Huang, C. J., Wang, C. C., Ku, C. C., Shi, Z., Chyan, C. L., Irene, D., Lim, L. H., Tsai, T. I., Hu, Y. P., Arco, S. D., Wong, C. H., and Hung, S. C. (2012) α-Glycosylation by D-glucosamine-derived donors: synthesis of heparosan and heparin analogues that interact with mycobacterial heparin-binding hemagglutinin J. Am. Chem. Soc. 134, 8988-8995
11. Miller, G. J., Hansen, S. U., Avizienyte, E., Rushton, G., Cole, C., Jayson, G. C., and Gardiner, J. M. (2013) Efficient chemical synthesis of heparin-like octa-, deca- and dodecasaccharides and inhibition of FGF2- and VEGF165-mediated endothelial cell functions Chem. Sci. 4, 3218-3222
12. Schwörer, R., Zubkova, O. V., Turnbull, J. E., and Tyler, P. C. (2013) Synthesis of a targeted library of heparan sulfate hexa- to dodecasaccharides as inhibitors of β-secretase: potential therapeutics for Alzheimer's disease Chem.-Eur. J. 19, 6817-6823
13. Copeland, R., Balasubramaniam, A., Tiwari, V., Zhang, F., Bridges, A., Linhardt, R. J., Shukla, D., and Liu, J. (2008) Using a 3- O -sulfated heparin octasaccharide to inhibit the entry of herpes simplex virus type 1 Biochemistry 47, 5774-5783
14. Maccarana, M., Casu, B., and Lindahl, U. (1993) Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor J. Biol. Chem. 268, 23898-23905
15. Guglier, S., Hricovini, M., Raman, R., Polito, L., Torri, G., Casu, B., Sasisekharan, R., and Guerrini, M. (2008) Minimum FGF2 binding structural requirements of heparin and heparan sulfate oligosaccharides as determined by NMR spectroscopy Biochemistry 47, 13862-13869
16. Ornitz, D. M., Herr, A. B., Nilsson, M., Westman, J., Svahn, C. M., and Waksman, G. (1995) FGF binding and FGF receptor activation by synthetic heparan-derived di- and trisaccharides Science 268, 432-436
17. Faham, S., Hileman, R. E., Fromm, J. R., Linhardt, R. J., and Rees, D. C. (1996) Heparin structure and interactions with basic fibroblast growth factor Science 271, 1116-1120
18. Schlessinger, J., Plotnikov, A. N., Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A., Linhardt, R. J., and Mohammadi, M. (2000) Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization Mol. Cell 6, 743-750
19. Kreuger, J., Salmivirta, M., Sturiale, L., Gimenez-Gallego, G., and Lindahl, U. (2001) Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2 J. Biol. Chem. 276, 30744-30752
20. Hu, Y. P., Zhong, Y. Q., Chen, Z. G., Chen, C. Y., Shi, Z., Zulueta, M. M. L., Ku, C. C., Lee, P. Y., Wang, C. C., and Hung, S. C. (2012) Divergent synthesis of 48 heparan sulfate-based disaccharides and probing the specific sugar-fibroblast growth factor-1 interaction J. Am. Chem. Soc. 134, 20722-20727
21. Lawrence, R., Lu, H., Rosenberg, R. D., Esko, J. D., and Zhang, L. (2008) Disaccharide structure code for the easy representation of constituent oligosaccharides from glycosaminoglycans Nat. Methods 5, 291-292
22. Nieto, L., Canales, á., Fernández, I. S., Santillana, E., González-Corrochano, R., Redondo-Horcajo, M., Cañada, F. J., Nieto, P., Martín-Lomas, M., Giménez-Gallego, G., and Jiménez-Barbero, J. (2013) Heparin modulates the mitogenic activity of fibroblast growth factor by inducing dimerization of its receptor. A 3D view by using NMR ChemBioChem. 14, 1732-1744
23. Duchesne, L., Octeau, V., Bearon, R. N., Beckett, A., Prior, I. A., Lounis, B., and Fernig, D. G. (2012) Transport of fibroblast growth factor 2 in the pericellular matrix is controlled by the spatial distribution of its binding sites in heparan sulfate PLoS Biol. 10, e1001361
24. Gasparian, M. E., Elistratov, P. A., Drize, N. I., Nifontova, I. N., Dolgikh, D. A., and Kirpichnikov, M. P. (2009) Overexpression in Escherichia coli and purification of human fibroblast growth factor (FGF-2) Biochemistry (Moscow) 74, 221-225
25. McPherson, A. (1990) Current approaches to macromolecular crystallization Eur. J. Biochem. 189, 1-23
26. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
27. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L.-W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination Acta. Crystallogr., Sect. D: Biol. Crystallogr. 58, 1948-1954
28. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221
29. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta. Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132
30. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. (1994) The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763