Structural glycobiology of heparin dynamics on the exosite 2 of coagulation cascade proteases: Implications for glycosaminoglycans antithrombotic activity

Glycobiology

Volumn 24, Issue 1, 2014, Pages 97-105

  Pol Fachin, Laercio ^a   Verli, Hugo ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

fXa; glycosylation; hemostasis; molecular dynamics; thrombin

Indexed keywords

BLOOD CLOTTING FACTOR 10A; GLYCOSAMINOGLYCAN; HEPARIN; PROTHROMBIN A; SERINE PROTEINASE; THROMBIN;

ANTICOAGULATION; ARTICLE; BLOOD CLOTTING; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME ACTIVE SITE; ENZYME STABILITY; GLYCOBIOLOGY; GLYCOSYLATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN TERTIARY STRUCTURE;

FXA; GLYCOSYLATION; HEMOSTASIS; MOLECULAR DYNAMICS; THROMBIN;

BLOOD COAGULATION; CATALYTIC DOMAIN; FACTOR XA; HEPARIN; HUMANS; MOLECULAR DYNAMICS SIMULATION; THROMBIN;

EID: 84890397308     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt095     Document Type: Article

References (64)

1. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: A web-based environment for protein structure homology modeling. Bioinformatics. 22:195-201.
2. Benkert P, Biasini M, Schwede T. 2011. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics. 27:343-350.
3. Berendsen HJC, Grigera JR, Straatsma TP. 1987. The missing term in effective pair potentials. J Phys Chem. 91:6269-6271.
4. Berendsen HJC, Postma JPM, DiNola A, Haak Jr. 1984. Molecular dynamics with coupling to an external bath. J Chem Phys. 81:3684-3690.
5. Bode W, Mayr I, Baumann U, Huber R, Stone SR, Hofsteenge J. 1989. The refined 1.9 A crystal structure of human alpha-thrombin: Interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 8:3467-3475.
6. Bode W, Turk D, Karshikov A. 1992. The refined 1.9-A X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human alpha-thrombin: Structure analysis, overall structure, electrostatic properties, detailed activesite geometry, and structure-function relationships. Protein Sci. 1:426-471.
7. Carter WJ, Cama E, Huntington JA. 2005. Crystal structure of thrombin bound to heparin. J Biol Chem. 280:2745-2749.
8. Choay J, Petitou M, Lormeau J-C, Sinay P, Casu B, Gatti G. 1983. Structure-activity relationship in heparin: A synthetic pentasaccharide with high affinity for antithrombin III and eliciting high anti-factor Xa activity. Biochem Biophys Res Commun. 116:492-499.
9. Craig PA, Olson ST, Shore JD. 1989. Transient kinetics of heparin-catalyzed protease inactivation by antithrombin III. Characterization of assembly, product formation, and heparin dissociation steps in the factor Xa reaction. J Biol Chem. 264:5452-5461.
10. 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.
11. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J. 2006. CASTp: Computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res. 34: W116-W118.
12. Eargle J, Luthey-Schulten Z. 2012. Networkview: 3D display and analysis of protein-RNA interaction networks. Bioinformatics. 28:3000-3001.
13. Fernandes CL, Sachett LG, Pol-Fachin L, Verli H. 2010. GROMOS96 43a1 performance in predicting oligosaccharide conformational ensembles within glycoproteins. Carbohydr Res. 345:663-671.
14. Fernández PV, Quintana I, Cerezo AS, Caramelo JJ, Pol-Fachin L, Verli H, Estevez JM, Ciancia M. 2013. Anticoagulant activity of a unique sulfated pyranosic (1?3)-?-L-arabinan through direct interaction with thrombin. J Biol Chem. 288:223-233.
15. Fredenburgh JC, Stafford AR, Weitz JI. 1997. Evidence for allosteric linkage between exosites 1 and 2 of thrombin. J Biol Chem. 272:25493-25499.
16. Fuglestad B, Gasper PM, Tonelli M, McCammon JA, Markwick PRL, Komives EA. 2012. The dynamic structure of thrombin in solution. Biophys J. 103:79-88.
17. Furie B, Furie BC. 1988. The molecular basis of blood coagulation. Cell. 33:505-518.
18. Gandhi NS, Mancera RL. 2008. The structure of glycosaminoglycans and their interactions with proteins. Chem Biol Drug Des. 72:455-482.
19. Gettins PGW. 2002. Serpin structure, mechanism, and function. Chem Rev.102:4751-4803.
20. 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. Evidence for very high affinity induced by an unusual glucuronic acid residue. J Biol Chem. 283:26662-26675.
21. Hansen DF, Kay LE. 2011. Determining valine side-chain rotamer conformations in proteins from methyl 13C chemical shifts: Application to the 360 kDa half-proteasome. J Am Chem Soc. 133:8272-8281.
22. Hansson K, Stenflo J. 2005. Post-translational modifications in proteins involved in blood coagulation. J Thromb Haemost. 3:2633-2648.
23. Henry BL, Monien BH, Bock PE, Desai UR. 2007. A novel allosteric pathway of thrombin inhibition: Exosite II mediated potent inhibition of thrombin by chemo-enzymatic, sulfated dehydropolymers of 4-hydroxycinnamic acids. J Biol Chem. 282:31891-31899.
24. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. 1997. LINCS: A linear constraint solver for molecular simulations. J Comput Chem. 18:1463-1472.
25. Humphrey W, Dalke A, Schulten K. 1996. VMD: Visual molecular dynamics. J Mol Graphics. 14:33-38.
26. Huntington JA, Read RJ, Carrell RW. 2000. Structure of a serpin-protease complex shows inhibition by deformation. Nature. 407:923-926.
27. International Union of Pure and Applied Chemistry and International Union of Biochemistry and Molecular Biology Joint Commission on Biochemical Nomenclature (IUPAC). 1996. Nomenclature of carbohydrates. Pure Appl Chem. 68:1919-2008.
28. Johnson DJD, Li W, Adams TE, Huntington JA. 2006. Antithrombin-S195A factor Xa-heparin structure reveals the allosteric mechanism of antithrombin activation. EMBO J. 25:2029-2037.
29. Kamata K, Kawamoto H, Honma T, Iwama T, Kim SH. 1998. Structural basis for chemical inhibition of human blood coagulation factor Xa. Proc Natl Acad Sci USA. 95:6630-6635.
30. Khan S, Gor J, Mulloy B, Perkins SJ. 2010. Semi-rigid solution structures of heparin by constrained X-ray scattering modelling: New insight into heparinprotein complexes. J Mol Biol. 395:504-521.
31. Lane DL, Denton J, Flynn AM, Thunberg L, Lindahl U. 1984. Anticoagulant activities of heparin oligosaccharides and their neutralization by platelet factor 4. Biochem J. 218:725-732.
32. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallog. 26:283-291.
33. Laurent TC, Tengblad A, Thunberg L, Höök M, Lindahl U. 1978. The molecular-weight-dependence of the anti-coagulant activity of heparin. Biochem J. 175:691-701.
34. Lawson JH, Kalafatis M, Stram S, Mann KG. 1994. A model for the tissue factor pathway to thrombin. I. An empirical study. J Biol Chem. 269:23357-23366.
35. Li W, Johnson DJD, Esmon CT, Huntington JA. 2004. Structure of the antithrombin- thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol. 11:857-862.
36. Lüthy R, Bowie JU, Eisenberg D. 1992. Assessment of protein models with three-dimensional profiles. Nature. 356:83-85.
37. Lütteke T, Bohne-Lang A, Loss A, Goetz T, Frank M, von der Lieth CW. 2006. GLYCOSCIENCES.De: An Internet portal to support glycomics and glycobiology research. Glycobiology. 16:71R-81R.
38. Mulinari F, Becker-Ritt AB, Demartini DR, Ligabue-Braun R, Stanisçuaski F, Verli H, Fragoso RR, Schroeder EK, Carlini CR, Grossi-de-Sá MF. 2011. Characterization of JBURE-IIb isoform of Canavalia ensiformis (L.) DC urease. Biochim Biophys Acta. 1814:1758-1768.
39. Mulloy B, Forster MJ, Jones C, Davies DB. 1993. N.m.r. and molecular- modelling studies of the solution conformation of heparin. Biochem J. 293:849-858.
40. Nader HB, Pinhal MA, Baú EC, Castro RA, Medeiros GF, Chavante SF, Leite EL, Trindade ES, Shinjo SK, Rocha HA, et al. 2001. Development of new heparin-like compounds and other antithrombotic drugs and their interaction with vascular endothelial cells. Braz J Med Biol Res. 34:699-709.
41. Nilsson B, Horne MKr, Gralnick HR. 1983. The carbohydrate of human thrombin: Structural analysis of glycoprotein oligosaccharides by mass spectrometry. Arch Biochem Biophys. 224:127-133.
42. O'Brien LA, Stafford AR, Fredenburgh JC, Weitz JI. 2003. Glycosaminoglycans bind factor Xa in a Ca2+-dependent fashion and modulate its catalytic activity. Biochemistry. 42:13091-13098.
43. Olson ST, Swanson R, Raub-Segall E, Bedsted T, Sadri M, Petitou M, Herault J-P, Herbert J-M, Björk I. 2004. Accelerating ability of synthetic oligosaccharides on antithrombin inhibition of proteinases of the clotting and fibrinolytic systems. Comparison with heparin and low-molecular-weight heparin. Thromb Haemostasis. 92:929-939.
44. Oosta GM, Gardner WT, Beeler DL, Rosenberg RD. 1981. Multiple functional domains of the heparin molecule. Proc Natl AcadSci USA. 78:829-833.
45. Pol-Fachin L, Becker CF, Guimarães JA, Verli H. 2011. Effects of glycosylation on heparin binding and antithrombin activation by heparin. Proteins. 79:2735-2745.
46. Pol-Fachin L, Fernandes CL, Verli H. 2009. GROMOS96 43a1 performance on the characterization of glycoprotein conformational ensembles through molecular dynamics simulations. Carbohydr Res. 344:491-500.
47. Pol-Fachin L, Verli H. 2008. Depiction of the forces participating in the 2-O-sulfo-alpha-L-iduronic acid conformational preference in heparin sequences in aqueous solutions. Carbohydr Res. 343:1435-1445.
48. Pol-Fachin L, Verli H. 2011. Assessment of glycoproteins dynamics from computer simulations. Mini Rev Org Chem. 8:229-238.
49. Rand MD, Lock JB, vacute;tVeer C, Gaffney DP, Mann KG. 1996. Blood clotting in minimally altered whole blood. Blood. 88:3432-3445.
50. Rau JC, Beaulieu LM, Huntington JA, Church FC. 2007. Serpins in thrombosis, hemostasis and fibrinolysis. J Thromb Haemost. 5:102-115.
51. Rezaie AR. 1998. Calcium enhances heparin catalysis of the antithrombinfactor Xa reaction by a template mechanism. Evidence that calcium alleviates GLA domain antagonism of heparin binding to factor Xa. J Biol Chem. 273:16824-16827.
52. Rezaie AR. 2000. Identification of basic residues in the heparin-binding exosite of factor Xa critical for heparin and factor Va binding. J Biol Chem. 275:3320-3327.
53. Rezaie AR, Olson ST. 2000. Calcium enhances heparin catalysis of the antithrombin-factor Xa reaction by promoting the assembly of an intermediate heparin-antithrombin-factor Xa bridging complex. Demonstration by rapid kinetics studies. Biochemistry. 39:12083-12090.
54. Rosenfeld L, Danishefsky I. 1984. Effects of enzymatic deglycosylation on the biological activities of human thrombin and antithrombin. Arch Biochem Biophys. 229:359-367.
55. Sanchez R, Pieper U, Mirkovic N, de Bakker PIW, Wittenstein E, Sali A. 2000. Modbase, a database of annotated comparative protein structure models. Nucleic Acids Res. 28:250-253.
56. Schaftenaar G, Noordik JH. 2000. Molden: A pre- and post-processing program for molecular and electronic structures. J Comput AidedMol Des. 14:123-134.
57. Schuettelkopf AW, van Aalten DMF. 2004. PRODRG: A tool for highthroughput crystallography of protein-ligand complexes. Acta Crystallogr Sect D. 60:1355-1363.
58. Scott WRP, Hünenberger PH, Tironi IG, Mark AE, Billeter SR, Fennen J, Torda AE, Huber T, Krüger P, van Gunsteren WF. 1999. The GROMOS biomolecular simulation program package. J Phys Chem A. 103:3596-3607.
59. Sethi A, Eargle J, Black AA, Luthey-Schulten Z. 2009. Dynamical networks in tRNA: Protein complexes. Proc Natl Acad Sci USA. 106:6620-6625.
60. Sheehan JP, Sadler JE. 1994. Molecular mapping of the heparin-binding exosite of thrombin. Proc Natl Acad Sci USA. 91:5518-5522.
61. Sunnerhagen M, Olah GA, Stenflo J, Forsen S, Drakenberg T, Trewhella J. 1996. The relative orientation of Gla and EGF domains in coagulation factor X is altered by Ca2+ binding to the first EGF domain. A combined NMR-small angle X-ray scattering study. Biochemistry. 35:11547-11559. The PyMOL Molecular Graphics System, Version 1.3, Schrödinger, LLC
62. van der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ. 2005. GROMACS: Fast, flexible, and free. J Comput Chem. 26: 1701-1718.
63. Verli H, Guimarães JA. 2004. Molecular dynamics simulation of a decasaccharide fragment of heparin in aqueous solution. Carbohydr Res. 339: 281-290.
64. Verli H, Guimarães JA. 2005. Insights into the induced fit mechanism in antithrombin-heparin interaction using molecular dynamics simulations. J Mol Graph Model. 24:203-212.