A simple method for discovering druggable, specific glycosaminoglycan-protein systems. Elucidation of key principles from heparin/heparan sulfate-binding proteins

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Sarkar, Aurijit ^a   Desai, Umesh R ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 O SULFOTRANSFERASE 1; 3 O SULFOTRANSFERASE 1; 3 O SULFOTRANSFERASE 3A1; ANTITHROMBIN; ARGININE; ASPARAGINE; CARBOHYDRATE BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 2; GLUTAMINE; HEPARAN SULFATE BINDING PROTEIN; HEPARIN; HEPARIN BINDING PROTEIN; LYSINE; SERUM ALBUMIN; SULFOTRANSFERASE; THROMBIN; UNCLASSIFIED DRUG; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; PROTEIN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING SITE; ENTHALPY; GENE MUTATION; HYDROGEN BOND; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN STRUCTURE; STATIC ELECTRICITY; HUMAN; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY;

ANTITHROMBINS; ARGININE; BINDING SITES; FIBROBLAST GROWTH FACTOR 2; GLYCOSAMINOGLYCANS; HEPARIN; HEPARITIN SULFATE; HUMANS; HYDROGEN BONDING; LYSINE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEINS;

EID: 84949492234     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141127     Document Type: Article

References (60)

1. Yamada S, Sugahara K, Ozbek S. Evolution of glycosaminoglycans: Comparative biochemical study. Commun Integr Biol. 2011; 4: 150-8. doi: 10.4161/cib.4.2.14547 PMID: 21655428
2. Ori A, Wilkinson MC, Fernig DG. A systems biology approach for the investigation of the heparin/heparan sulfate interactome. J Biol Chem. 2011; 286: 19892-904. doi: 10.1074/jbc.M111.228114 PMID: 21454685
3. Raman R, Sasisekharan V, Sasisekharan R. Structural insights into biological roles of protein-glycosaminoglycan interactions. Chem Biol. 2005; 12: 267-77. doi: 10.1016/j.chembiol.2004.11.020 PMID: 15797210
4. Cardin A, Weintraub H. Molecular modeling of protein-glycosaminoglycan interactions. Arter Throm Vas. 1989; 9: 21-32. doi: 10.1161/01.ATV.9.1.21
5. Sobel M, Soler DF, Kermode JC, Harris RB. Localization and characterization of a heparin binding domain peptide of human von Willebrand factor. J Biol Chem. 1992; 267: 8857-62. PMID: 1577724
6. Hileman RE, Fromm JR, Weiler JM, Linhardt RJ. Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays. 1998; 20: 156-167. doi: 10.1002/(SICI)1521-1878(199802)20:2<156::AID-BIES8>3.0.CO;2-R PMID: 9631661
7. 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. doi: 10.1042/BST0340431 PMID: 16709179
8. Mulloy B, Forster MJ. Application of drug discovery software to the identification of heparin-binding sites on protein surfaces: a computational survey of the 4-helix cytokines. Mol Simul. 2008; 34: 481-489. doi: 10.1080/08927020701784754
9. Gandhi NS, Coombe DR, Mancera RL. Platelet endothelial cell adhesion molecule 1 (PECAM-1) and its interactions with glycosaminoglycans: 1. Molecular modeling studies. Biochemistry. 2008; 47: 4851-62. doi: 10.1021/bi702455e PMID: 18393439
10. Gandhi NS, Mancera RL. Prediction of heparin binding sites in bone morphogenetic proteins (BMPs). Biochim Biophys Acta. Elsevier B.V.; 2012; 1824: 1374-81. doi: 10.1016/j.bbapap.2012.07.002 PMID: 22824487
11. Agostino M, Mancera RL, Ramsland PA, Yuriev E. AutoMap: a tool for analyzing protein-ligand recognition using multiple ligand binding modes. J Mol Graph Model. Elsevier Inc.; 2013; 40: 80-90. doi: 10.1016/j.jmgm.2013.01.001 PMID: 23376613
12. Agostino M, Gandhi NS, Mancera RL. Development and application of site mapping methods for the design of glycosaminoglycans. Glycobiology. 2014; 24: 840-51. doi: 10.1093/glycob/cwu045 PMID: 24859723
13. Mottarella SE, Beglov D, Beglova N, Nugent MA, Kozakov D, Vajda S. Docking server for the identification of heparin binding sites on proteins. J Chem Inf Model. 2014; 54: 2068-78. doi: 10.1021/ci500115j PMID: 24974889
14. Rogers CJ, Clark PM, Tully SE, Abrol R, Garcia KC, Goddard WA, et al. Elucidating glycosaminoglycan-protein-protein interactions using carbohydrate microarray and computational approaches. Proc Natl Acad Sci U S A. 2011; 108: 9747-52. doi: 10.1073/pnas.1102962108 PMID: 21628576
15. Raghuraman A, Mosier PD, Desai UR. 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. 2006; 49: 3553-62. doi: 10.1021/jm060092o PMID: 16759098
16. Raghuraman A, Mosier PD, Desai UR. Understanding Dermatan Sulfate-Heparin Cofactor II Interaction through Virtual Library Screening. ACS Med Chem Lett. 2010; 1: 281-285. doi: 10.1021/ml100048y PMID: 20835364
17. Torrent M, Nogués MV, Andreu D, Boix E. The "CPC clip motif": a conserved structural signature for heparin-binding proteins. PLoS One. 2012; 7: e42692. doi: 10.1371/journal.pone.0042692 PMID: 22880084
18. Samsonov SA, Gehrcke J, Pisabarro MT. Flexibility and explicit solvent in molecular-dynamics-based docking of protein-glycosaminoglycan systems. J Chem Inf Model. 2014; 54: 582-92. doi: 10.1021/ci4006047 PMID: 24479827
19. Samsonov SA, Bichmann L, Pisabarro MT. Coarse-Grained Model of Glycosaminoglycans. J Chem Inf Model. 2014
20. Spillmann D, Lindahl U. Glycosaminoglycan-protein interactions: a question of specificity. Curr Opin Struct Biol. 1994; 4: 677-682. doi: 10.1016/S0959-440X(94)90165-1
21. Kreuger J, Spillmann D, Li J, Lindahl U. Interactions between heparan sulfate and proteins: the concept of specificity. J Cell Biol. 2006; 174: 323-7. doi: 10.1083/jcb.200604035 PMID: 16880267
22. Muñoz-García JC, Chabrol E, Vivès RR, Thomas A, de Paz JL, Rojo J, et al. Langerin-Heparin Interaction: Two Binding Sites for Small and Large Ligands As Revealed by a Combination of NMR Spectroscopy and Cross-Linking Mapping Experiments. J Am Chem Soc. 2015; 137: 4100-4110. doi: 10.1021/ja511529x PMID: 25747117
23. Munoz-Garcia JC, Garcia-Jimenez MJ, Carrero P, Canales a., Jimenez-Barbero J, Martin-Lomas M, et al. Importance of the polarity of the glycosaminoglycan chain on the interaction with FGF-1. Glycobiology. 2014; 24: 1004-1009. doi: 10.1093/glycob/cwu071 PMID: 25015527
24. Mosier PD, Krishnasamy C, Kellogg GE, Desai UR. On the specificity of heparin/heparan sulfate binding to proteins. Anion-binding sites on antithrombin and thrombin are fundamentally different. PLoS One. 2012; 7: e48632. doi: 10.1371/journal.pone.0048632 PMID: 23152789
25. Jin L, Abrahams JP, Skinner R, Petitou M, Pike RN, Carrell RW. The anticoagulant activation of antithrombin by heparin. Proc Natl Acad Sci U S A. 1997; 94: 14683-8. PMID: 9405673
26. Carter WJ, Cama E, Huntington J a. Crystal structure of thrombin bound to heparin. J Biol Chem. 2005; 280: 2745-9. doi: 10.1074/jbc.M411606200 PMID: 15548541
27. Olson ST, Halvorson HR, Björk I. Quantitative characterization of the thrombin-heparin interaction. Discrimination between specific and nonspecific binding models. J Biol Chem. 1991; 266: 6342-6352. PMID: 2007587
28. Desai UR, Petitou M, Bjork I, Olson ST. Mechanism of Heparin Activation of Antithrombin. Role of individual residues of the pentasaccharide activating sequence in the recognition of native and activated states of antithrombin. J Biol Chem. 1998; 273: 7478-7487. doi: 10.1074/jbc.273.13.7478 PMID: 9516447
29. Xu D, Esko JD. Demystifying heparan sulfate-protein interactions. Annu Rev Biochem. 2014; 83: 129-57. doi: 10.1146/annurev-biochem-060713-035314 PMID: 24606135
30. Li W, Johnson DJD, Esmon CT, Huntington JA. Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol. 2004; 11: 857-62. doi: 10.1038/nsmb811 PMID: 15311269
31. Schedin-Weiss S, Arocas V, Bock SC, Olson ST, Björk I. Specificity of the basic side chains of Lys114, Lys125, and Arg129 of antithrombin in heparin binding. Biochemistry. 2002; 41: 12369-76. PMID: 12369826
32. Desai UR. New antithrombin-based anticoagulants. Med Res Rev. 2004; 24: 151-81. doi: 10.1002/med.10058 PMID: 14705167
33. He X, Ye J, Esmon CT, Rezaie a R. Influence of Arginines 93, 97, and 101 of thrombin to its functional specificity. Biochemistry. 1997; 36: 8969-76. doi: 10.1021/bi9704717 PMID: 9220985
34. Thompson LD, Pantoliano MW, Springer BA. Energetic characterization of the basic fibroblast growth factor-heparin interaction: identification of the heparin binding domain. Biochemistry. 1994; 33: 3831-40. PMID: 8142385
35. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova A V, Yeh BK, Yayon A, et al. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell. 2000; 6: 743-50. PMID: 11030354
36. Moon AF, Edavettal SC, Krahn JM, Munoz EM, Negishi M, Linhardt RJ, et al. 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: 45185-93. doi: 10.1074/jbc.M405013200 PMID: 15304505
37. Moon AF, Xu Y, Woody SM, Krahn JM, Linhardt RJ, Liu J, et al. Dissecting the substrate recognition of 3-O-sulfotransferase for the biosynthesis of anticoagulant heparin. Proc Natl Acad Sci U S A. 2012; 109: 5265-70. doi: 10.1073/pnas.1117923109 PMID: 22431632
38. Liu C, Sheng J, Krahn JM, Perera L, Xu Y, Hsieh P-H, et al. Molecular mechanism of substrate specificity for heparan sulfate 2-O-sulfotransferase. J Biol Chem. 2014; 289: 13407-18. doi: 10.1074/jbc. M113.530535 PMID: 24652287
39. Mascotti DP, Lohman TM. Thermodynamics of Charged Oligopeptide-Heparin Interactions. Biochemistry. 1995; 34: 2908-2915. doi: 10.1021/bi00009a022 PMID: 7893705
40. Gandhi NS, Mancera RL. Free energy calculations of glycosaminoglycan-Protein interactions. Glycobiology. 2009; 19: 1103-1115. doi: 10.1093/glycob/cwp101 PMID: 19643843
41. Kridel SJ, Chan WW, Knauer DJ. Requirement of Lysine Residues Outside of the Proposed Pentasaccharide Binding Region for High Affinity Heparin Binding and Activation of Human Antithrombin III. J Biol Chem. 1996; 271: 20935-20941. doi: 10.1074/jbc.271.34.20935 PMID: 8702852
42. Desai U, Swanson R, Bock SC, Bjork I, Olson ST. Role of arginine 129 in heparin binding and activation of antithrombin. J Biol Chem. 2000; 275: 18976-84. doi: 10.1074/jbc.M001340200 PMID: 10764763
43. Arocas V, Bock SC, Raja S, Olson ST, Bjork I. Lysine 114 of antithrombin is of crucial importance for the affinity and kinetics of heparin pentasaccharide binding. J Biol Chem. 2001; 276: 43809-17. doi: 10.1074/jbc.M105294200 PMID: 11567021
44. Meagher JL, Huntington JA, Fan B, Gettins PGW. Role of Arginine 132and Lysine 133in Heparin Binding to and Activation of Antithrombin. J Biol Chem. 1996; 271: 29353-29358. doi: 10.1074/jbc.271.46. 29353 PMID: 8910598
45. Gan ZR, Li Y, Chen Z, Lewis SD, Shafer JA. Identification of basic amino acid residues in thrombin essential for heparin-catalyzed inactivation by antithrombin III. J Biol Chem. 1994; 269: 1301-5. PMID: 8288594
46. Grant JA, Pickup BT, Nicholls A. A smooth permittivity function for Poisson-Boltzmann solvation methods. J Comput Chem. 2001; 22: 608-640. doi: 10.1002/jcc.1032
47. Edavettal SC, Lee KA, Negishi M, Linhardt RJ, Liu J, Pedersen LC. Crystal structure and mutational analysis of heparan sulfate 3-O-sulfotransferase isoform 1. J Biol Chem. 2004; 279: 25789-97. doi: 10.1074/jbc.M401089200 PMID: 15060080
48. Olson ST, Bjork I. Predominant Contribution of Surface Approximation to the Mechanism of Heparin Acceleration of the Antithrombin-Thrombin Reaction. Elucidation from salt concentration effects. J Biol Chem. 1991; 266: 6353-6364. PMID: 2007588
49. Hattori T, Kimura K, Seyrek E, Dubin PL. Binding of bovine serum albumin to heparin determined by turbidimetric titration and frontal analysis continuous capillary electrophoresis. Anal Biochem. 2001; 295: 158-67. doi: 10.1006/abio.2001.5129 PMID: 11488617
50. Brooks BR, Brooks CL III, Mackerell AD, Nilsson L, Petrella RJ, Roux B, et al. CHARMM: The biomolecular simulation program. J Comput Chem. 2009; 30: 1545-1614. doi: 10.1002/jcc.21287 PMID: 19444816
51. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B. 1998; 102: 3586-616. doi: 10.1021/jp973084f PMID: 24889800
52. Sankaranarayanan NV, Desai UR. Toward a robust computational screening strategy for identifying glycosaminoglycan sequences that display high specificity for target proteins. Glycobiology. 2014;0: 1-11.
53. Sapay N, Cabannes E, Petitou M, Imberty A. Molecular modeling of the interaction between heparan sulfate and cellular growth factors: bringing pieces together. Glycobiology. 2011; 21: 1181-93. doi: 10.1093/glycob/cwr052 PMID: 21572110
54. Boothello RS, Sarkar A, Tran VM, Nguyen TKN, Sankaranarayanan NV, Mehta AY, et al. Chemoenzymatically Prepared Heparan Sulfate Containing Rare 2-O-Sulfonated Glucuronic Acid Residues. ACS Chem Biol. 2015; 10: 1485-1494. doi: 10.1021/acschembio.5b00071 PMID: 25742429
55. Atha DH, Lormeau JC, Petitou M, Rosenberg RD, Choay J. Contribution of monosaccharide residues in heparin binding to antithrombin III. Biochemistry. 1985; 24: 6723-9. PMID: 4084555
56. Maccarana M, Casu B, Lindahl U. Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J Biol Chem. 1994; 269: 3903. PMID: 8106436
57. Gilson MK, Rashin A, Fine R, Honig B. On the calculation of electrostatic interactions in proteins. J Mol Biol. 1985; 184: 503-516. PMID: 4046024
58. Bondi A. van der Waals Volumes and Radii. J Phys Chem. 1964; 68: 441-451. doi: 10.1021/j100785a001
59. Halgren TA. Merck molecular force field. II. MMFF94 van der Waals and electrostatic parameters for intermolecular interactions. J Comput Chem. 1996; 17: 520-552. doi: 10.1002/(SICI)1096-987X (199604)17:5/6<520::AID-JCC2>3.0.CO;2-W
60. Ren P, Chun J, Thomas DG, Schnieders MJ, Marucho M, Zhang J, et al. Biomolecular electrostatics and solvation: a computational perspective. Q Rev Biophys. 2012; 45: 427-91. doi: 10.1017/S003358351200011X PMID: 23217364