Molecular docking of heparin oligosaccharides with Hep-II heparin-binding domain of fibronectin reveals an interplay between the different positions of sulfate groups

Glycoconjugate Journal

Volumn 31, Issue 2, 2014, Pages 161-169

  Carpentier, Mathieu ^a   Denys, Agnès ^a   Allain, Fabrice ^a   Vergoten, Gérard ^a  

^a UNIV LILLE   (France)

Author keywords

Fibronectin; Heparan sulfate; Heparin; Interaction; Molecular docking

Indexed keywords

AMINO ACID MOTIFS; BINDING SITES; FIBRONECTINS; GLYCOSAMINOGLYCANS; HEPARIN; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; OLIGOSACCHARIDES;

EID: 84895185867     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-013-9512-8     Document Type: Article

References (44)

1. Pankov, R., Yamada, K.M.: Fibronectin at a glance. J. Cell Sci. 115, 3861-3863 (2002)
2. Woods, A., Couchman, J.R.: Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol. Biol. Cell 5, 183-192 (1994)
3. Petersen, T.E., Thøgersen, H.C., Skorstengaard, K., Vibe-Pedersen, K., Sahl, P., Sottrup-Jensen, L., Magnusson, S.: Isolation and characterization of cDNA clones for human and bovine fibronectins. Proc. Natl. Acad. Sci. U. S. A. 80, 137-141 (1983)
4. Pierschbacher, M.D., Ruoslahti, E.: Variants of the cell recognition site of fibronectin that retain attachment-promoting activity. Proc. Natl. Acad. Sci. U. S. A. 81, 5985-5988 (1984)
5. Ruoslahti, E.: Fibronectin and its receptors. Annu. Rev. Biochem. 57, 375-413 (1988)
6. Humphries, M.J., Komoriya, A., Akiyama, S.K., Olden, K., Yamada, K.M.: Identification of two distinct regions of the type III connecting segment of human plasma fibronectin that promote cell type-specific adhesion. J. Biol. Chem. 262, 6886-6892 (1987)
7. Sharma, A., Askari, J.A., Humphries, M.J., Jones, E.Y., Stuart, D.I.: Elucidation of the structural features of heparan sulfate important for interaction with the Hep-2 domain of fibronectin. EMBO J. 18, 1468-1479 (1999)
8. Garcia-Pardo, A., Rostagno, A., Frangione, B.: Primary structure of human plasma fibronectin. Characterization of a 38 kDa domain containing the C-terminal heparin-binding site (Hep III site) and a region of molecular heterogeneity. Biochem. J. 241, 923-928 (1987)
9. Kishore, R., Samuel, M., Khan, M.Y., Hand, J., Frenz, D.A., Newman, S.A.: Interaction of the NH2-terminal domain of fibronectin with heparin. Role of the omega-loops of the type I modules. J. Biol. Chem. 272, 17078-17085 (1997)
10. Benecky, M.J., Kolvenbach, C.G., Amrani, D.L., Mosesson, M.W.: Evidence that binding to the carboxyl-terminal heparin-binding domain (Hep II) dominates the interaction between plasma fibronectin and heparin. Biochemistry 27, 7565-7571 (1988)
11. Ingham, K.C., Brew, S.A., Atha, D.A.: Interaction of heparin with fibronectin and isolated fibronectin domains. Biochem. J. 272, 605-611 (1990)
12. Lin, H., Lal, R., Clegg, D.O.: Imaging and mapping heparin-binding sites on single fibronectin molecules with atomic force microscopy. Biochemistry 39, 3192-3196 (2000)
13. Mostafavi-Pour, Z., Askari, J.A., Whittard, J.D., Humphries, M.J.: Identification of a novel heparin-binding site in the alternatively spliced IIICS region of fibronectin: roles of integrins and proteoglycans in cell adhesion to fibronectin splice variants. Matrix Biol. 20, 63-73 (2001)
14. Gui, L., Wojciechowski, K., Gildner, C.D., Nedelkovska, H., Hocking, D.C.: Identification of the heparin-binding determinants within fibronectin repeat III1: role in cell spreading and growth. J. Biol. Chem. 46, 34816-34825 (2006)
15. Esko, J.D., Selleck, S.B.: Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471 (2002)
16. Capila, I., Linhardt, R.J.: Heparin-protein interactions. Angew. Chem., Int. Ed. Engl. 41, 391-412 (2002)
17. Ori, A., Wilkinson, M.C., Fernig, D.G.: The heparanome and regulation of cell function: structures, functions and challenges. Front. Biosci. 13, 4309-4338 (2008)
18. Sugahara, K., Kitagawa, H.: Heparin and heparan sulfate biosynthesis. IUBMB Life 54, 163-175 (2002)
19. Shriver, Z., Capila, I., Venkataraman, G., Sasisekharan, R.: Heparin and heparan sulfate: analyzing structure and microheterogeneity. Handb. Exp. Pharmacol. 207, 159-176 (2012)
20. Barkalow, F.J., Schwarzbauer, J.E.: Localization of the major heparin-binding site in fibronectin. J. Biol. Chem. 266, 7812-7818 (1991)
21. Busby, T.F., Argraves, W.S., Brew, S.A., Pechik, I., Gilliland, G.L., Ingham, K.C.: Heparin binding by fibronectin module III-13 involves six discontinuous basic residues brought together to form a cationic cradle. J. Biol. Chem. 270, 18558-18562 (1995)
22. Sachchidanand, Lequin, O., Staunton, D., Mulloy, B., Forster, M.J., Yoshida, K., Campbell, I.D.: Mapping the heparin-binding site on the 13-14F3 fragment of fibronectin. J. Biol. Chem. 277, 50629-50635 (2002)
23. Ingham, K.C., Brew, S.A., Migliorini, M.M., Busby, T.F.: Heparin binding by fibronectin module III-13 involves six discontinuous basic residues brought together to form a cationic cradle. Biochemistry 32, 12548-12553 (1993)
24. Lyon, M., Rushton, G., Askari, J.A., Humphries, M.J., Gallagher, J.T.: Elucidation of the structural features of heparan sulfate important for interaction with the Hep-2 domain of fibronectin. J. Biol. Chem. 275, 4599-4606 (2000)
25. Mahalingam, Y., Gallagher, J.T., Couchman, J.R.: Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties. J. Bio. Chem. 282, 3221-3230 (2007)
26. Katchalski-Katzir, E., Shariv, I., Eisenstein, M., Friesem, A.A., Aflalo, C., Vakser, I.A.: Molecular surface recognition: determination of geometric fit between proteins and their ligands by correlation techniques. Proc. Natl. Acad. Sci. U. S. A. 89, 2195-2199 (1992)
27. Ausiello, G., Cesareni, G., Helmer-Citterich, M.: ESCHER: a new docking procedure applied to the reconstruction of protein tertiary structure. Proteins 28, 556-567 (1997)
28. Palma, P.N., Krippahl, L., Wampler, J.E., Moura, J.: BiGGER: a new (soft) docking algorithm for predicting protein interactions. J. Proteins 39, 372-384 (2000)
29. Ritchie, D.W., Kozakov, D., Vajda, S.: Accelerating and focusing protein-protein docking correlations using multi-dimensional rotational FFT generating functions. Bioinformatics 24, 1865-1873 (2008)
30. Hex's home page: http://www.loria.fr (∼ritchied/hex) 2013. Accessed 20 April 2013
31. Jones, G., Willet, P., Glen, R.C., Leach, A.R., Taylor, R.: Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267, 727-748 (1997)
32. Gandhi, N.S., Freeman, C., Parish, C.R., Mancera, R.L.: Computational analyses of the catalytic and heparin-binding sites and their interactions with glycosaminoglycans in glycoside hydrolase family 79 endo-β-D-glucuronidase (heparanase). Glycobiology 22, 35-55 (2012)
33. Vergoten, G., Mazur, I., Lagant, P., Michalski, J.C., Zanetta, J.P.: The SPASIBA force field as an essential tool for studying the structure and dynamics of saccharides. Biochimie 85, 65-73 (2003)
34. Lagant, P., Nolde, D., Stote, R., Vergoten, G., Karplus, M.: Increasing normal modes analysis accuracy: the SPASIBA spectroscopic force field introduced into the CHARMM program. J. Phys. Chem. 108, 4019-4029 (2004)
35. Meziane-Tani, M., Lagant, P., Semmound, A., Vergoten, G.: The SPASIBA force field for chondroitin sulfate: vibrational analysis of D-glucuronic and N-acetyl-D-galactosamine 4-sulfate sodium salts. J. Phys. Chem. 110, 11359-11370 (2006)
36. Homans, S.W.: A molecular mechanical force field for the conformational analysis of oligosaccharides: comparison of theoretical and crystal structures of Man alpha 1-3Man beta 1-4GlcNAc. Biochemistry 29, 9110-9118 (1990)
37. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E.: UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004)
38. Halgren, T.A.: MMFF VII. Characterization of MMFF94, MMFF94s, and other widely available force fields for conformational energies and for intermolecular-interaction energies and geometries. J. Comput. Chem. 20, 730-748 (1999)
39. Sapay, N., Cabannes, E., Petitou, M., Imberty, A.: Molecular modeling of the interaction between heparan sulfate and cellular growth factors: bringing pieces together. Glycobiology 21, 1181-1193 (2011)
40. Raghuraman, A., Mosier, P.D., Desai, U.R.: Finding a needle in a haystack: development of a combinatorial virtual screening approach for identifying high specificity heparin/heparan sulfate sequence(s). J. Med. Chem. 49, 3553-3562 (2006)
41. Raghuraman, A., Mosier, P.D., Desai, U.R.: Understanding dermatan sulfate-heparin cofactor II interaction through virtual library screening. ACS Med. Chem. Lett. 1, 281-285 (2010)
42. Gandhi, N.S., Coombe, D.R., Mancera, R.L.: Platelet endothelial cell adhesion molecule 1 (PECAM-1) and its interactions with glycosaminoglycans: 1. Molecular modeling studies. Biochemistry 47, 4851-4862 (2008)
43. Mosier, P.D., Krishnasamy, C., Kellogg, G.E., Desai, U.R.: PLoS One (2012) doi: 7/e48632
44. Samsonov, S.A., Teyra, J., Pisabarro, M.T.: Docking glycosaminoglycans to proteins: analysis of solvent inclusion. J. Comput. Aided Mol. Des. 25, 477-489 (2011)