Docking server for the identification of heparin binding sites on proteins

Journal of Chemical Information and Modeling

Volumn 54, Issue 7, 2014, Pages 2068-2078

  Mottarella, Scott E ^a   Beglov, Dmitri ^b   Beglova, Natalia ^c   Nugent, Matthew A ^d   Kozakov, Dima ^b   Vajda, Sandor ^b  

^a BOSTON UNIVERSITY   (United States)

^b Boston University   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d University of Massachusetts Lowell   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; FAST FOURIER TRANSFORMS; MOLECULAR DYNAMICS; MOLECULES; PROTEINS; SULFUR COMPOUNDS;

COMPUTATIONAL DOCKINGS; ENERGY FUNCTIONS; HEPARIN-BINDING SITE; PROTEIN-PROTEIN DOCKING; ROOT MEAN SQUARE DEVIATIONS; SPECIFIC INTERACTION; STRUCTURE DETERMINATION; TETRASACCHARIDES;

POLYSACCHARIDES;

HEPARAN SULFATE; HEPARIN; PROTEIN; SOLVENT;

BINDING SITE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR DOCKING; MONTE CARLO METHOD; PROTEIN CONFORMATION;

BINDING SITES; HEPARIN; HEPARITIN SULFATE; HUMANS; MOLECULAR DOCKING SIMULATION; MONTE CARLO METHOD; PROTEIN CONFORMATION; PROTEINS; SOLVENTS;

EID: 84904976113     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci500115j     Document Type: Article

References (66)

1. Bernfield, M.; Gotte, M.; Park, P. W.; Reizes, O.; Fitzgerald, M. L.; Lincecum, J.; Zako, M. Functions of cell surface heparan sulfate proteoglycans Annu. Rev. Biochem. 1999, 68, 729-77
2. Gandhi, N. S.; Mancera, R. L. The structure of glycosaminoglycans and their interactions with proteins Chem. Biol. Drug Des 2008, 72, 455-482
3. Lindahl, U. Heparan sulfate-protein interactions-a concept for drug design? Thromb Haemostasis 2007, 98, 109-115
4. Bourin, M. C.; Lindahl, U. Glycosaminoglycans and the regulation of blood-coagulation Biochem. J. 1993, 289, 313-330
5. Spencer, J. L.; Bernanke, J. A.; Buczek-Thomas, J. A.; Nugent, M. A. A computational approach for deciphering the organization of glycosaminoglycans PLoS One 2010, 5
6. Raman, R.; Raguram, S.; Venkataraman, G.; Paulson, J. C.; Sasisekharan, R. Glycomics: An integrated systems approach to structure-function relationships of glycans Nat. Methods 2005, 2, 817-24
7. Sasisekharan, R.; Raman, R.; Prabhakar, V. Glycomics approach to structure-function relationships of glycosaminoglycans Annu. Rev. Biomed Eng. 2006, 8, 181-231
8. Capila, I.; Linhardt, R. J. Heparin-protein interactions Angew. Chem., Int. Ed. Engl. 2002, 41, 391-412
9. Fugedi, P. The potential of the molecular diversity of heparin and heparan sulfate for drug development Mini Rev. Med. Chem. 2003, 3, 659-67
10. Esko, J. D.; Lindahl, U. Molecular diversity of heparan sulfate J. Clin Invest 2001, 108, 169-73
11. Forster, M.; Mulloy, B. Computational approaches to the identification of heparin-binding sites on the surfaces of proteins Biochem. Soc. Trans. 2006, 34, 431-4
12. Mulloy, B.; Linhardt, R. J. Order out of complexity-protein structures that interact with heparin Curr. Opin Struct Biol. 2001, 11, 623-628
13. Imberty, A.; Lortat-Jacob, H.; Perez, S. Structural view of glycosaminoglycan-protein interactions Carbohydr. Res. 2007, 342, 430-439
14. Cardin, A. D.; Weintraub, H. J. R. Molecular modeling of protein-glycosaminoglycan interactions Arteriosclerosis 1989, 9, 21-32
15. Gandhi, N. S.; Coombe, D. R.; Mancera, R. L. Platelet endothelial cell adhesion molecule 1 (PECAM-1) and its interactions with glycosarninoglycans: 1. Molecular modeling studies Biochemistry 2008, 47, 4851-4862
16. Ricard-Blum, S.; Feraud, O.; Lortat-Jacob, H.; Rencurosi, A.; Fukai, N.; Dkhissi, F.; Vittet, D.; Imberty, A.; Olsen, B. R.; van der Rest, M. Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling-role of divalent cations J. Biol. Chem. 2004, 279, 2927-2936
17. Mulloy, B.; Forster, M. J. Application of drug discovery software to the identification of heparin-binding sites on protein surfaces: A computational survey of the 4-helix cytokines Mol. Simulat 2008, 34, 481-489
18. Pita, S. S. D.; Fernandes, T. V. A.; Caffarena, E. R.; Pascutti, P. G. Studies of molecular docking between fibroblast growth factor and heparin using generalized simulated annealing Int. J. Quantum Chem. 2008, 108, 2608-2614
19. Kern, A.; Schmidt, K.; Leder, C.; Muller, O. J.; Wobus, C. E.; Bettinger, K.; Von der Lieth, C. W.; King, J. A.; Kleinschmidt, J. A. Identification of a heparin-binding motif on adeno-associated virus type 2 capsids J. Virol 2003, 77, 11072-11081
20. Ballut, L.; Sapay, N.; Chautard, E.; Imberty, A.; Ricard-Blum, S. Mapping of heparin/heparan sulfate binding sites on alpha v beta 3 integrin by molecular docking J. Mol. Recognit 2013, 26, 76-85
21. Carpentier, M.; Denys, A.; Allain, F.; Vergoten, G. Molecular docking of heparin oligosaccharides with hep-ii heparin-binding domain of fibronectin reveals an interplay between the different positions of sulfate groups Glycoconj J. 2013, 31, 161-169
22. Hung, T. J.; Tomiya, N.; Chang, T. H.; Cheng, W. C.; Kuo, P. H.; Ng, S. K.; Lien, P. C.; Lee, Y. C.; Chang, M. D. Functional characterization of ECP-heparin interaction: A novel molecular model PLoS One 2013, 8, e82585
23. Bitomsky, W.; Wade, R. C. Docking of glycosaminoglycans to heparin-binding proteins: Validation for aFGF, bFGF, and antithrombin and application to IL-8 J. Am. Chem. Soc. 1999, 121, 3004-3013
24. Goodford, P. J. A computational-procedure for determining energetically favorable binding-sites on biologically important macromolecules J. Med. Chem. 1985, 28, 849-857
25. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E.; Belew, R. K.; Olson, A. J. Automated docking using a lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 1998, 19, 1639-1662
26. Ewing, T. J. A.; Makino, S.; Skillman, A. G.; Kuntz, I. D. DOCK 4.0: Search strategies for automated molecular docking of flexible molecule databases J. Comput. Aid Mol. Des 2001, 15, 411-428
27. Samsonov, S. A.; Teyra, J.; Pisabarro, M. T. Docking glycosaminoglycans to proteins: Analysis of solvent inclusion J. Comput. Aid Mol. Des 2011, 25, 477-489
28. Brenke, R.; Kozakov, D.; Chuang, G. Y.; Beglov, D.; Hall, D.; Landon, M. R.; Mattos, C.; Vajda, S. Fragment-based identification of druggable hot spots of proteins using Fourier domain correlation techniques Bioinformatics 2009, 25, 621-7
29. Vajda, S.; Guarnieri, F. Characterization of protein-ligand interaction sites using experimental and computational methods Curr. Opin Drug Discov Devel 2006, 9, 354-62
30. Kozakov, D.; Brenke, R.; Comeau, S. R.; Vajda, S. PIPER: An FFT-based protein docking program with pairwise potentials Proteins 2006, 65, 392-406
31. Comeau, S. R.; Gatchell, D. W.; Vajda, S.; Camacho, C. J. ClusPro: An automated docking and discrimination method for the prediction of protein complexes Bioinformatics 2004, 20, 45-50
32. Kozakov, D.; Hall, D. R.; Beglov, D.; Brenke, R.; Comeau, S. R.; Shen, Y.; Li, K.; Zheng, J.; Vakili, P.; Paschalidis, I.; Vajda, S. Achieving reliability and high accuracy in automated protein docking: ClusPro, PIPER, SDU, and stability analysis in CAPRI rounds 13-19 Proteins 2010, 78, 3124-30
33. Lensink, M. F.; Mendez, R.; Wodak, S. J. Docking and scoring protein complexes: CAPRI 3rd edition Proteins 2007, 69, 704-18
34. Lensink, M. F.; Wodak, S. J. Docking and scoring protein interactions: CAPRI 2009 Proteins 2010, 78, 3073-84
35. Lensink, M. F.; Wodak, S. J. Docking, scoring, and affinity prediction in CAPRI Proteins 2013, 81, 2082-95
36. Comeau, S. R.; Kozakov, D.; Brenke, R.; Shen, Y.; Beglov, D.; Vajda, S. ClusPro: Performance in CAPRI rounds 6-11 and the new server Proteins 2007, 69, 781-5
37. Kozakov, D.; Clodfelter, K. H.; Vajda, S.; Camacho, C. J. Optimal clustering for detecting near-native conformations in protein docking Biophys. J. 2005, 89, 867-75
38. Kozakov, D.; Beglov, D.; Bohnuud, T.; Mottarella, S. E.; Xia, B.; Hall, D. R.; Vajda, S. How good is automated protein docking? Proteins 2013, 81, 2159-2166
39. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28, 235-42
40. Moon, A. F.; Edavettal, S. C.; Krahn, J. M.; Munoz, E. M.; Negishi, M.; Linhardt, R. J.; Liu, J.; Pedersen, L. C. Structural analysis of the sulfotransferase (3-o-sulfotransferase isoform 3) involved in the biosynthesis of an entry receptor for herpes simplex virus 1 J. Biol. Chem. 2004, 279, 45185-45193
41. Xue, Y.; Lee, S. W.; Wang, Y. C.; Ha, Y. Crystal structure of the E2 domain of amyloid precursor protein-like protein 1 in complex with sucrose octasulfate J. Biol. Chem. 2011, 286, 29748-29757
42. Xue, Y.; Lee, S.; Ha, Y. Crystal structure of amyloid precursor-like protein 1 and heparin complex suggests a dual role of heparin in E2 dimerization Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 16229-16234
43. Chirgadze, D. Y.; Hepple, J. P.; Zhou, H. J.; Byrd, R. A.; Blundell, T. L.; Gherardi, E. Crystal structure of the NK1 fragment of HGF/SF suggests a novel mode for growth factor dimerization and receptor binding Nat. Struct. Biol. 1999, 6, 72-79
44. Lietha, D.; Chirgadze, D. Y.; Mulloy, B.; Blundell, T. L.; Gherardi, E. Crystal structures of NK1-heparin complexes reveal the basis for NK1 activity and enable engineering of potent agonists of the MET receptor EMBO J. 2001, 20, 5543-5555
45. Huntington, J. A.; Kjellberg, M.; Stenflo, J. Crystal structure of protein C inhibitor provides insights into hormone binding and heparin activation Structure 2003, 11, 205-215
46. Li, W.; Huntington, J. A. The heparin binding site of protein c inhibitor is protease-dependent J. Biol. Chem. 2008, 283, 36039-36045
47. Ago, H.; Kitagawa, Y.; Fujishima, A.; Matsuura, Y.; Katsube, Y. Crystal-structure of basic fibroblast growth-factor at 1.6 a resolution J. Biochem-Tokyo 1991, 110, 360-363
48. Faham, S.; Hileman, R. E.; Fromm, J. R.; Linhardt, R. J.; Rees, D. C. Heparin structure and interactions with basic fibroblast growth factor Science 1996, 271, 1116-1120
49. Schmidt, M. W.; Baldridge, K. K.; Boatz, J. A.; Elbert, S. T.; Gordon, M. S.; Jensen, J. H.; Koseki, S.; Matsunaga, N.; Nguyen, K. A.; Su, S. J.; Windus, T. L.; Dupuis, M.; Montgomery, J. A. General atomic and molecular electronic-structure system J. Comput. Chem. 1993, 14, 1347-1363
50. Wang, J.; Wang, W.; Kollman, P. A.; Case, D. A. Automatic atom type and bond type perception in molecular mechanical calculations J. Mol. Graph Model 2006, 25, 247-60
51. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field J. Comput. Chem. 2004, 25, 1157-74
52. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. Charmm-a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 1983, 4, 187-217
53. Capila, I.; Hernaiz, M. J.; Mo, Y. D.; Mealy, T. R.; Campos, B.; Dedman, J. R.; Linhardt, R. J.; Seaton, B. A. Annexin V - heparin oligosaccharide complex suggests heparan sulfate - mediated assembly on cell surfaces Structure 2001, 9, 57-64
54. Colloch, N.; Sopkova-de Oliveira Santos, J.; Retailleau, P.; Vivares, D.; Bonnete, F.; Langlois dEstainto, B.; Gallois, B.; Brisson, A.; Risso, J. J.; Lemaire, M.; Prange, T.; Abraini, J. H. Protein crystallography under xenon and nitrous oxide pressure: Comparison with in vivo pharmacology studies and implications for the mechanism of inhaled anesthetic action Biophys. J. 2007, 92, 217-24
55. 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. 2002, 277, 50629-35
56. DiGabriele, A. D.; Lax, I.; Chen, D. I.; Svahn, C. M.; Jaye, M.; Schlessinger, J.; Hendrickson, W. A. Structure of a heparin-linked biologically active dimer of fibroblast growth factor Nature 1998, 393, 812-7
57. Fernandez, I. S.; Cuevas, P.; Angulo, J.; Lopez-Navajas, P.; Canales-Mayordomo, A.; Gonzalez-Corrochano, R.; Lozano, R. M.; Valverde, S.; Jimenez-Barbero, J.; Romero, A.; Gimenez-Gallego, G. Gentisic acid, a compound associated with plant defense and a metabolite of aspirin, heads a new class of in vivo fibroblast growth factor inhibitors J. Biol. Chem. 2010, 285, 11714-11729
58. Rigden, D. J.; Jedrzejas, M. J. Structures of Streptococcus pneumoniae hyaluronate lyase in complex with chondroitin and chondroitin sulfate disaccharides-insights into specificity and mechanism of action J. Biol. Chem. 2003, 278, 50596-50606
59. Lunin, V. V.; Li, Y. G.; Linhardt, R. J.; Miyazono, H.; Kyogashima, M.; Kaneko, T.; Bell, A. W.; Cygler, M. High-resolution crystal structure of Arthrobacter aurescens chondroitin ac lyase: An enzyme-substrate complex defines the catalytic mechanism J. Mol. Biol. 2004, 337, 367-386
60. Capila, I.; Hernaiz, M. J.; Mo, Y. D.; Mealy, T. R.; Campos, B.; Dedman, J. R.; Linhardt, R. J.; Seaton, B. A. Annexin V-heparin oligosaccharide complex suggests heparan sulfate-mediated assembly on cell surfaces Structure 2001, 9, 57-64
61. Shaya, D.; Zhao, W. J.; Garron, M. L.; Xiao, Z. P.; Cui, Q. Z.; Zhang, Z. Q.; Sulea, T.; Linhardt, R. J.; Cygler, M. Catalytic mechanism of heparinase ii investigated by site-directed mutagenesis and the crystal structure with its substrate J. Biol. Chem. 2010, 285, 20051-20061
62. Shaya, D.; Tocilj, A.; Li, Y. G.; Myette, J.; Venkataraman, G.; Sasisekharan, R.; Cygler, M. Crystal structure of heparinase II from Pedobacter heparinus and its complex with a disaccharide product J. Biol. Chem. 2006, 281, 15525-15535
63. Shao, C. H.; Zhang, F. M.; Kemp, M. M.; Linhardt, R. J.; Waisman, D. M.; Head, J. F.; Seaton, B. A. Crystallographic analysis of calcium-dependent heparin binding to annexin A2 J. Biol. Chem. 2006, 281, 31689-31695
64. Swaminathan, G. J.; Myszka, D. G.; Katsamba, P. S.; Ohnuki, L. E.; Gleich, G. J.; Acharya, K. R. Eosinophil-granule major basic protein, a C-type lectin, binds heparin Biochemistry 2005, 44, 14152-14158
65. Swaminathan, G. J.; Weaver, A. J.; Loegering, D. A.; Checkel, J. L.; Leonidas, D. D.; Gleich, G. J.; Acharya, K. R. Crystal structure of the eosinophil major basic protein at 1.8 angstrom-an atypical lectin with a paradigm shift in specificity J. Biol. Chem. 2001, 276, 26197-26203
66. Han, Y. H.; Garron, M. L.; Kim, H. Y.; Kim, W. S.; Zhang, Z. Q.; Ryu, K. S.; Shaya, D.; Xiao, Z. P.; Cheong, C.; Kim, Y. S.; Linhardt, R. J.; Jeon, Y. H.; Cygler, M. Structural snapshots of heparin depolymerization by heparin lyase i J. Biol. Chem. 2009, 284, 34019-34027