Semi-Rigid Solution Structures of Heparin by Constrained X-ray Scattering Modelling: New Insight into Heparin-Protein Complexes

Journal of Molecular Biology

Volumn 395, Issue 3, 2010, Pages 504-521

  Khan, Sanaullah ^a   Gor, Jayesh ^a   Mulloy, Barbara ^b   Perkins, Stephen J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

heparin; modelling; ultracentrifugation; X ray scattering

Indexed keywords

HEPARIN; PROTEIN;

ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; MOLECULAR MODEL; PARTICLE SIZE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; RADIATION SCATTERING; SEDIMENTATION; STRUCTURE ANALYSIS; ULTRACENTRIFUGATION;

EID: 73249136226     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.064     Document Type: Article

References (60)

1. Lane D.A., and Lindahl U. Heparin: Chemical and Biological Properties. Clinical Applications (1989), CRC Press, Boca Raton, FL
2. Kazatchkine M.D., Fearon D.T., Metcalfe D.D., Rosenberg D.D., and Austen F.K. Structural determinants of the capacity of heparin to inhibit the formation of the human amplification C3 convertase. J. Clin. Invest. 67 (1981) 223-228
3. Sharath M.D., Merchant Z.M., Kim Y.S., Rice K.G., Linhardt R.J., and Weiler J.M. Small heparin fragments regulate the amplification pathway of complement. Immunopharmacology 9 (1985) 73-80
4. Folkman J., Langer R., Linhardt R.J., Handeschild C., and Taylor S. Angiogenesis inhibition and tumor regression caused by heparin or a heparin fragment in the presence of cortisone. Science 221 (1983) 719-725
5. Crum R., Szabo S., and Folkman J. Angiogenesis is stimulated by a tumor-derived endothelia cell growth factor. Science 230 (1985) 1375-1387
6. Holondniy M., Kim S., Katzenstein D., Konrad M., Groves E.T., and Merigan T.C. Inhibition of human immunodeficiency virus gene amplification by heparin. J. Clin. Microbiol. 29 (1991) 676-679
7. Shieh M.-T., and Spear P.G. Herpes virus-induced cell fusion that is dependent on cell surface heparan sulfate or soluble heparin. J. Virol. 68 (1994) 1224-1228
8. Capila I., and Linhardt R.J. Heparin-protein interactions. Angew. Chem. Int. Ed. Engl. 41 (2002) 390-412
9. Liu G., Hultin M., Ostergaard P., and Olivercrona T. Interaction of size-fractionated heparins with lipoprotein lipase and hepatic lipase in the rat. Biochem. J. 285 (1992) 731-736
10. Gallagher J.T., and Walker A. Molecular distinctions between heparan sulphate and heparin. Analysis of sulphation patterns indicates that heparan sulphate and heparin are separate families of N-sulphated polysaccharides. Biochem. J. 230 (1985) 665-674
11. Hileman R.E., Fromm J.R., Weiler J.M., and Linhardt R.J. Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. BioEssays 20 (1998) 156-167
12. Mulloy B., Forster M.J., Jones C., and Davies D.B. NMR and molecular-modelling studies of the solution conformation of heparin. Biochem. J. 293 (1993) 849-858
13. Ragazzi M., Ferro D.R., Perly B., Sinay P., Petitou M., and Choay J. Conformation of the pentasaccharide corresponding to the binding site of heparin for antithrombin III. Carbohydr. Res. 195 (1990) 169-185
14. Faham S., Hileman R.E., Fromm J.R., Linhardt R.J., and Rees D.C. Heparin structure and interactions with basic fibroblast growth factor. Science 271 (1996) 1116-1120
15. DiGabriele A.D., Lax I., Chen D.I., Svahn C.M., Jaye M., Schlessinger J., and Hendrickson W.A. Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature 393 (1998) 812-817
16. Pellegrini L., Burke D.F., von Delft F., Mulloy B., and Blundell T.L. Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407 (2000) 1029-1034
17. Schlessinger J., Plotnikov A.N., Ibrahimi O.A., Eliseenkova A.V., Yeh B.K., 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 6 (2000) 743-750
18. Carter W.J., Cama E., and Huntington J.A. Crystal structure of thrombin bound to heparin. J. Biol. Chem. 280 (2005) 2745-2749
19. Jin L., Abrahams J.P., Skinner R., Petitou M., Pike R.N., and Carrell R.W. The anticoagulant activation of antithrombin by heparin. Proc. Natl Acad. Sci. USA 94 (1997) 14683-14688
20. McCoy A.J., Pei X.Y., Skinner R., Abrahams J.P., and Carrell R.W. Structure of β-antithrombin and the effect of glycosylation on antithrombin's heparin affinity and activity. J. Mol. Biol. 326 (2003) 823-833
21. Johnson D.J., Li W., Adams T.E., and Huntington J.A. Antithrombin-S195A factor Xa-heparin structure reveals the allosteric mechanism of antithrombin activation. EMBO J. 25 (2006) 2029-2037
22. L angdown J., Belzar K.J., Savory W.J., Baglin T.P., and Huntington J.A. The critical role of hinge-region expulsion in the induced-fit heparin binding mechanism of antithrombin. J. Mol. Biol. 386 (2009) 1278-1289
23. Fry E.E., Lea S.M., Jackson T., Newman J.W., Ellard F.M., Blakemore W.E., et al. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 18 (1999) 543-554
24. Lietha D., Chirgadze D.Y., Mulloy B., Blundell T.L., and 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. 20 (2001) 5543-5555
25. Capila I., Hernáiz M.J., Mo Y.D., Mealy T.R., Campos B., Dedman J.R., et al. Annexin V-heparin oligosaccharide complex suggests heparan sulfate-mediated assembly on cell surfaces. Structure 9 (2001) 57-64
26. Shao C., Zhang F., Kemp M.M., Linhardt R.J., Waisman D.M., Head J.F., and Seaton B.A. Crystallographic analysis of calcium-dependent heparin binding to annexin A2. J. Biol. Chem. 281 (2006) 31689-31695
27. Ganesh V.K., Smith S.A., Kotwal G.J., and Murthy K.H. Structure of vaccinia complement protein in complex with heparin and potential implications for complement regulation. Proc. Natl Acad. Sci. USA 101 (2004) 8924-8929
28. Li W., and Huntington J.A. The heparin binding site of protein C inhibitor is protease-dependent. J. Biol. Chem. 51 (2008) 36039-36045
29. Pavlov G., Finet S., Tatarenko K., Korneeva E., and Ebel C. Conformation of heparin studied with macromolecular hydrodynamic methods and X-ray scattering. Eur. Biophys. J. 32 (2003) 437-449
30. Perez Sanchez H., Tatarenko K., Nigen M., Pavlov G., Imberty A., Lortat-Jacob H., et al. Organization of human interferon gamma-heparin complexes from solution properties and hydrodynamics. Biochemistry 45 (2006) 13227-13238
31. Nieduszynski I.A., and Atkins E.D. Conformation of the mucopolysaccharides. X-ray fibre diffraction of heparin. Biochem. J. 135 (1973) 729-733
32. Atkins E.D., and Nieduszynski I.A. Conformation of the mucopolysaccharides: X-ray fibre diffraction of heparin. Fed. Proc. 1 (1977) 78-83
33. Perkins S.J., Okemefuna A.I., Fernando A.N., Bonner A., Gilbert H.E., and Furtado P.B. X-ray and neutron scattering data and their constrained molecular modelling. Methods Cell Biol. 84 (2008) 375-423
34. Perkins S.J., Okemefuna A.I., Nan R., Li K., and Bonner A. Constrained solution scattering modelling of human antibodies and complement proteins reveals novel biological insights. J. R. Soc. Interface 6 (2009) S679-S696
35. Bonner A., Almogren A., Furtado P.B., Kerr M.A., and Perkins S.J. Location of secretory component on the Fc edge of dimeric IgA1 reveals insight into the role of secretory IgA1 in mucosal immunity. Mucosal Immunology (Nat. Publ. Group) 2 (2009) 74-84
36. Perkins S.J. Unravelling antibody and complement structures in immunity using TS-2 neutrons at ISIS: neutron scattering. Biochemist 31 (2009) 32-35
37. Mulloy B., Gee C., Wheeler S.F., Wait R., Gray E., and Barrowcliffe T.W. Molecular weight measurements of low molecular weight heparins by gel permeation chromatography. Thromb. Haemost. 77 (1997) 668-674
38. Cole J.L., Lary J.W., Moody T.P., and Laue T.M. Analytical ultracentrifugation: sedimentation velocity and sedimentation equilibrium. Methods Cell Biol. 84 (2008) 143-211
39. Fernando A.N., Furtado P.B., Clark S.J., Gilbert H.E., Day A.J., Sim R.B., and Perkins S.J. Associative and structural properties of the region of complement factor H encompassing the Tyr402His disease-related polymorphism and its interactions with heparin. J. Mol. Biol. 368 (2007) 564-581
40. Perkins S.J., and Weiss H. Low resolution structural studies of mitochondrial ubiquinol-cytochrome c reductase in detergent solutions by neutron scattering. J. Mol. Biol. 168 (1983) 847-866
41. Glatter O., and Kratky O. Editors of Small-Angle X-ray Scattering (1982), Academic Press, New York, NY
42. Perkins S.J. X-ray and neutron scattering analyses of hydration shells: a molecular interpretation based on sequence predictions and modelling fits. Biophys. Chem. 93 (2001) 129-139
43. Mulloy B., and Forster M.J. Conformation and dynamics of heparin and heparan sulfate. Glycobiology 10 (2000) 1147-1156
44. Okemefuna A.I., Nan R., Gor J., and Perkins S.J. Electrostatic interactions contribute to the folded-back conformation of wild-type human factor H. J. Mol. Biol. 391 (2009) 98-118
45. Furtado P.B., Huang C.Y., Ihyembe D., Hammond R.A., Marsh H.C., and Perkins S.J. The partly-folded back solution structure arrangement of the 30 SCR domains in human complement receptor type 1 (CR1) permits access to its C3b and C4b ligands. J. Mol. Biol. 375 (2008) 102-118
46. Gilbert H.E., Asokan R., Holers V.M., and Perkins S.J. The flexible 15 SCR extracellular domains of human complement receptor type 2 can mediate multiple ligand and antigen interactions. J. Mol. Biol. 362 (2006) 1132-1147
47. Ortega A., and García de la Torre J. Equivalent radii and ratios of radii from solution properties as indicators of macromolecular conformation, shape, and flexibility. Biomacromolecules 8 (2007) 2464-2475
48. Mulloy B., Forster M.J., Jones C., Drake A.F., Johnson E.A., and Davies D.B. The effect of variation of substitution on the solution conformation of heparin: a spectroscopic and molecular modelling study. Carbohydr. Res. 255 (1994) 1-26
49. Stringer S.E., Forster M.J., Mulloy B., Bishop C.R., Graham G.J., and Gallagher J.T. Characterization of the binding site on heparan sulfate for macrophage inflammatory protein 1α. Blood 100 (2002) 1543-1550
50. Khan S., Gor J., Mulloy B., and Perkins S.J. Solution structure of heparin and its complexes with the factor H SCR-6/8 domains and factor H: implications for disease. Mol. Immunol. 45 (2008) 4126 (Abstract)
51. Saunders R.E., Abarrategui-Garrido C., FrémeauxBacchi V., Goicoechea de Jorge E., Goodship T.H.J., López Trascasa M., et al. The interactive factor H-atypical haemolytic uraemic syndrome mutation database and Website: update and integration of membrane cofactor protein and factor I mutations with structural models. Hum. Mutat. 28 (2007) 222-234
52. Perkins S.J., Gilbert H.E., Aslam M., Hannan J.P., Holers V.M., and Goodship T.H.J. Solution structures of complement components by X-ray and neutron scattering and analytical ultracentrifugation. Biochem. Soc. Trans. 30 (2002) 996-1001
53. Gilbert H.E., Eaton J.T., Hannan J.P., Holers V.M., and Perkins S.J. Solution structure of the complex between CR2 SCR 1-2 and C3d of human complement: an X-ray scattering and sedimentation modelling study. J. Mol. Biol. 346 (2005) 859-873
54. Dam J., and Schuck P. Calculating sedimentation coefficient distribution by direct modeling of sedimentation velocity concentration profiles. Methods Enzymol. 384 (2004) 185-212
55. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78 (2000) 1606-1619
56. Perkins S.J. Protein volumes and hydration effects. The calculations of partial specific volumes, neutron scattering matchpoints and 280-nm absorption coefficients for proteins and glycoproteins from amino acid sequences. Eur. J. Biochem. 157 (1986) 169-180
57. Narayanan T., Diat O., and Bosecke P. SAXS and USAXS on the high brilliance beamline at the ESRF. Nucl. Instrum. Methods Phys. Res. Sect. A 467-468 (2001) 1005-1009
58. Semenyuk A.V., and Svergun D.I. GNOM-a program package for small-angle scattering data processing. J. Appl. Crystallogr. 24 (1991) 537-540
59. Ashton A.W., Boehm M.K., Gallimore J.R., Pepys M.B., and Perkins S.J. Pentameric and decameric structures in solution of the serum amyloid P component by X-ray and neutron scattering and molecular modelling analyses. J. Mol. Biol. 272 (1997) 408-422
60. Garcia de la Torre J., Huertas M.L., and Carrasco B. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 78 (2000) 719-730