Molecular modeling of the interaction between heparan sulfate and cellular growth factors: Bringing pieces together

Glycobiology

Volumn 21, Issue 9, 2011, Pages 1181-1193

  Sapay, Nicolas ^a   Cabannes, Eric ^b   Petitou, Maurice ^b   Imberty, Anne ^a  

^a CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^b Endotis Pharma   (France)

Author keywords

Cellular growth factor; heparan sulfate; molecular docking; molecular dynamics

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GLYCOSAMINOGLYCAN; GROWTH FACTOR; HEPARAN SULFATE; POLYSACCHARIDE; SOLVENT; STROMAL CELL DERIVED FACTOR 1ALPHA;

ARTICLE; BINDING AFFINITY; CHEMICAL INTERACTION; CONFORMATION; EXTRACELLULAR MATRIX; MOLECULAR DYNAMICS; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL;

ALGORITHMS; BINDING SITES; CHEMOKINE CXCL12; EXTRACELLULAR MATRIX; FIBROBLAST GROWTH FACTOR 2; HEPARITIN SULFATE; HUMANS; MODELS, CHEMICAL; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 80051505598     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwr052     Document Type: Article

References (66)

1. Amara A, Lorthioir O, Valenzuela A, Magerus A, Thelen M, Montes M, Virelizier J-L, Delepierre M, Baleux Fo, Lortat-Jacob H, et al. 1999. Stromal cell-derived factor-1α associates with heparan sulfates through the first β-strand of the chemokine. J Biol Chem. 274:23916-23925.
2. Bayly CI, Cieplak P, Cornell W, Kollman PA. 2002. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. J Phys Chem. 97:10269-10280.
3. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242. (Pubitemid 30047768)
4. Bitomsky W, Wade RC. 1999. Docking of glycosaminoglycans to heparin-binding proteins: Validation for aFGF, bFGF, and antithrombin and application to IL-8. J Am Chem Soc. 121:3004-3013. (Pubitemid 29189745)
5. Capila I, Hernáiz MAJ, Mo YD, Mealy TR, Campos B, Dedman JR, Linhardt RJ, Seaton BA. 2001. Annexin V heparin oligosaccharide complex suggests heparan sulfate mediated assembly on cell surfaces. Structure. 9:57-64. (Pubitemid 32064350)
6. Carlsson P, Presto J, Spillmann D, Lindahl U, Kjellén L. 2008. Heparin/heparan sulfate biosynthesis. J Biol Chem. 283:20008-20014.
7. Case DA, Cheatham TE, Darden T, Gohlke H, Luo R, Merz KM, Onufriev A, Simmerling C, Wang B, Woods RJ. 2005. The Amber biomolecular simulation programs. J Comput Chem. 26:1668-1688. (Pubitemid 43076180)
8. Casu B, Lindahl U. 2001. Structure and biological interactions of heparin and heparan sulfate. Adv Carbohydr Chem Biochem. 57:159-206. (Pubitemid 34121000)
9. Darden T, York D, Pedersen L. 1993. Particle mesh Ewald: An N log(N) method for Ewald sums in large systems. J Chem Phys. 98:10089-10092.
10. DiGabriele AD, Lax I, Chen DI, Svahn CM, Jaye M, Schlessinger J, Hendrickson WA. 1998. Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature. 393:812-817. (Pubitemid 28299496)
11. Dupradeau FY, Cezard C, Lelong R, Stanislawiak E, Pecher J, Delepine JC, Cieplak P. 2008. R.E.DD.B.: A database for RESP and ESP atomic charges, and force field libraries. Nucleic Acids Res. 36:D360-D367. (Pubitemid 351149749)
12. Esko JD, Lindahl U. 2001. Molecular diversity of heparan sulfate. J Clin Invest. 108:169-173. (Pubitemid 32656238)
13. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. 1995. A smooth particle mesh Ewald method. J Chem Phys. 103:8577-8593.
14. Fermas S, Gonnet F, Sutton A, Charnaux N, Mulloy B, Du Y, Baleux F, Daniel R. 2008. Sulfated oligosaccharides (heparin and fucoidan) binding and dimerization of stromal cell-derived factor-1 (SDF-1/CXCL 12) are coupled as evidenced by affinity CE-MS analysis. Glycobiology. 18:1054-1064. (Pubitemid 352762840)
15. Ferro DR, Provasoli A, Ragazzi M, Casu B, Torri G, Bossennec V, Perly B, Sinay P, Petitou M, Choay J. 1990. Conformer populations of L-iduronic acid residues in glycosaminoglycan sequences. Carbohyd Res. 195:157-167.
16. Forster M, Mulloy B. 2006. Computational approaches to the identification of heparin-binding sites on the surfaces of proteins. Biochem Soc Trans. 34:431-434. (Pubitemid 43954004)
17. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA, Vreven T, Kudin KN, Burant JC, et al. 2003. Gaussian 03, Revision C.02.
18. Gandhi NS, Mancera RL. 2009. Free energy calculations of glycosaminogly-can-protein interactions. Glycobiology. 19:1103-1115.
19. Gorsi B, Stringer SE. 2007. Tinkering with heparan sulfate sulfation to steer development. Trends Cell Biol. 17:173-177. (Pubitemid 46507809)
20. Gouin SG, Vanquelef E, Fernandez JM, Mellet CO, Dupradeau FY, Kovensky J. 2007. Multi-mannosides based on a carbohydrate scaffold: Synthesis, force field development, molecular dynamics studies, and binding affinities for lectin Con A. J Org Chem. 72:9032-9045. (Pubitemid 350195769)
21. Grünewald FS, Prota AE, Giese A, Ballmer-Hofer K. 2010. Structure-function analysis of VEGF receptor activation and the role of coreceptors in angiogenic signaling. Biochim Biophys Acta. 1804:567-580.
22. Guerrini M, Guglieri S, Casu B, Torri G, Mourier P, Boudier C, Viskov C. 2008. Antithrombin-binding octasaccharides and role of extensions of the active pentasaccharide sequence in the specificity and strength of interaction. J Biol Chem. 283:26662-26675.
23. Hagner-McWhirter A, Li JP, Oscarson S, Lindahl U. 2004. Irreversible glu-curonyl C5-epimerization in the biosynthesis of heparan sulfate. J Biol Chem. 279:14631-14638. (Pubitemid 38618851)
24. Hagner-McWhirter A, Lindahl U, Li J. 2000. Biosynthesis of heparin/heparan sulphate: Mechanism of epimerization of glucuronyl C-5. Biochem J. 347 (Pt 1):69-75. (Pubitemid 30199042)
25. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. 2006. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins. 65:712-725. (Pubitemid 44583220)
26. Hricovíni M, Torri G. 1995. Dynamics in aqueous solutions of the pentasac-charide corresponding to the binding site of heparin for antithrombin III studied by NMR relaxation measurements. Carbohydr Res. 268:159-175.
27. Huey R, Morris GM, Olson AJ, Goodsell DS. 2007. A semiempirical free energy force field with charge-based desolvation. J Comput Chem. 28:1145-1152. (Pubitemid 46506716)
28. Humphrey W, Dalke A, Schulten K. 1996. VMD: Visual molecular dynamics. J Mol Graph. 14:33-38, 27-38. (Pubitemid 26152973)
29. Iozzo R, Zoeller J, Nyström A. 2009. Basement membrane proteoglycans: Modulators Par Excellence of cancer growth and angiogenesis. Mol Cell. 27:503-513.
30. Jastrebova N, Vanwildemeersch M, Rapraeger AC, Giménez-Gallego G, Lindahl U, Spillmann D. 2006. Heparan sulfate-related oligosaccharides in ternary complex formation with fibroblast growth factors 1 and 2 and their receptors. J Biol Chem. 281:26884-26892. (Pubitemid 44401717)
31. Jayaram B, Sprous D, Young MA, Beveridge DL. 1998. Free energy analysis of the conformational preferences of A and B forms of DNA in solution. J Am Chem Soc. 120:10629-10633. (Pubitemid 28498806)
32. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. 1983. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 79:926-935.
33. Kamimura K, Koyama T, Habuchi H, Ueda R, Masu M, Kimata K, Nakato H. 2006. Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J Cell Biol. 174:773-778. (Pubitemid 44373727)
34. Kirschner KN, Yongye AB, Tschampel SM, Gonzalez-Outeirino J, Daniels CR, Foley BL, Woods RJ. 2008. GLYCAM06: A generalizable biomolecu-lar force field. Carbohydrates. J Comput Chem. 29:622-655. (Pubitemid 351238844)
35. Kreuger J, Spillmann D, Li JP, Lindahl U. 2006. Interactions between heparan sulfate and proteins: The concept of specificity. J Cell Biol. 174:323-327. (Pubitemid 44156762)
36. Lietha D, Chirgadze DY, Mulloy B, Blundell TL, Gherardi E. 2001. Crystal structures of NK1-heparin complexes reveal the basis for NK1 activity and enable engineering of potent agonists of the MET receptor. EMBO J. 20:5543-5555. (Pubitemid 33010032)
37. Lindahl U, Li JP. 2009. Interactions between heparan sulfate and proteins-design and functional implications. Int Rev Cell Mol Biol. 276:105-159.
38. Mahoney DJ, Mulloy B, Forster MJ, Blundell CD, Fries E, Milner CM, Day AJ. 2005. Characterization of the interaction between tumor necrosis factor-stimulated gene-6 and heparin: Implications for the inhibition of plasmin in extracellular matrix microenvironments. J Biol Chem. 280:27044-27055. (Pubitemid 41040741)
39. Mobli M, Nilsson M, Almond A. 2008. The structural plasticity of heparan sulfate NA-domains and hence their role in mediating multivalent interactions is confirmed by high-accuracy 15N-NMR relaxation studies. Glycoconj J. 25:401-414.
40. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem. 30:2785-2791.
41. Moy FJ, Seddon AP, Bohlen P, Powers R. 1996. High-resolution solution structure of basic fibroblast growth factor determined by multidimensional heteronuclear magnetic resonance spectroscopy. Biochemistry. 35:13552-13561. (Pubitemid 26359167)
42. Mulloy B, Forster MJ. 2000. Conformation and dynamics of heparin and heparan sulfate. Glycobiology. 10:1147-1156.
43. Mulloy B, Forster MJ, Jones C, Davies DB. 1993. NMR and molecular-modelling studies of the solution conformation of heparin. Biochem J. 293:849-858. (Pubitemid 23244575)
44. Murphy JW, Cho Y, Sachpatzidis A, Fan C, Hodsdon ME, Lolis E. 2007. Structural and functional basis of CXCL12 (stromal cell-derived factor-1 alpha) binding to heparin. J Biol Chem. 282:10018-10027. (Pubitemid 47104591)
45. Murphy KJ, Merry CLR, Lyon M, Thompson JE, Roberts IS, Gallagher JT. 2004. A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase. J Biol Chem. 279:27239-27245. (Pubitemid 38812562)
46. Murphy JW, Yuan H, Kong Y, Xiong Y, Lolis EJ. 2009. Heterologous quaternary structure of CXCL12 and its relationship to the CC chemokine family. Proteins. 78:1331-1337.
47. Pellegrini L, Burke DF, von Delft F, Mulloy B, Blundell TL. 2000. Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature. 407:1029-1034.
48. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K. 2005. Scalable molecular dynamics with NAMD. J Comput Chem. 26:1781-1802. (Pubitemid 43078511)
49. Raghuraman A, Mosier PD, Desai UR. 2006. 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. (Pubitemid 43902461)
50. Raman R, Venkataraman G, Ernst S, Sasisekharan V, Sasisekharan R. 2003. Structural specificity of heparin binding in the fibroblast growth factor family of proteins. Proc Natl Acad Sci USA. 100:2357-2362. (Pubitemid 36297503)
51. Ricard-Blum S, Féraud O, Lortat-Jacob H, Rencurosi A, Fukai N, Dkhissi F, Vittet D, Imberty A, Olsen BR, van der Rest M. 2004. Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling. J Biol Chem. 279:2927-2936. (Pubitemid 38114285)
52. Rudd TR, Uniewicz KA, Ori A, Guimond SE, Skidmore MA, Gaudesi D, Xu R, Turnbull JE, Guerrini M, Torri G, et al. 2010. Comparable stabilisation, structural changes and activities can be induced in FGF by a variety of HS and non-GAG analogues: Implications for sequence-activity relationships. Org Biomol Chem. 8:5390-5397.
53. Sadir R, Baleux F, Grosdidier A, Imberty A, Lortat-Jacob H. 2001. Characterization of the stromal cell-derived factor-1alpha-heparin complex. J Biol Chem. 276:8288-8296.
54. Sadir R, Imberty A, Baleux F, Lortat-Jacob H. 2004. Heparan sulfate/heparin oligosaccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV. J Biol Chem. 279:43854-43860. (Pubitemid 39390692)
55. Sanderson PN, Huckerby TN, Nieduszynski IA. 1987. Conformational equilibria of alpha-L-iduronate residues in disaccharides derived from heparin. Biochem J. 243:175-181. (Pubitemid 17048898)
56. Sanner MF, Olson AJ, Spehner JC. 1996. Reduced surface: An efficient way to compute molecular surfaces. Biopolymers. 38:305-320.
57. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, 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.
58. Schultz GS, Wysocki A. 2009. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen. 17:153-162.
59. Sitkoff D, Sharp KA, Honig B. 1994. Accurate calculation of hydration free energies using macroscopic solvent models. J Phys Chem. 98:1978-1988.
60. Srinivasan J, Cheatham TE, Cieplak P, Kollman PA, Case DA. 1998. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices. J Am Chem Soc. 120:9401-9409. (Pubitemid 28452628)
61. Stauffer ME, Skelton NJ, Fairbrothe WJ. 2002. Refinement of the solution structure of the heparin-binding domain of vascular endothelial growth factor using residual dipolar couplings. J Biomol NMR. 23:57-61. (Pubitemid 34546146)
62. Stringer SE. 2006. The role of heparan sulphate proteoglycans in angiogen-esis. Biochem Soc Trans. 34:451-453. (Pubitemid 43954009)
63. The R Development Core Team. 2005. R: A language and environment for statistical computing. Vienna: The R Development Core Team.
64. Veldkamp CT, Peterson FC, Pelzek AJ, Volkman BF. 2005. The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci. 14:1071-1081. (Pubitemid 40389378)
65. Vorobjev YN, Almagro JC, Hermans J. 1998. Discrimination between native and intentionally misfolded conformations of proteins: ES/IS, a new method for calculating conformational free energy that uses both dynamics simulations with an explicit solvent and an implicit solvent continuum model. Proteins. 32:399-413. (Pubitemid 28380782)
66. Wickham H. 2009. ggplot2: Elegant Graphics for Data Analysis. New York: Springer.